SYSTEMATICS AND PHYLOGENOMICS OF THE EREBINAE (LEPIDOPTERA: NOCTUOIDEA, EREBIDAE)

By

NICHOLAS T. HOMZIAK

A THESIS PRESENTED TO THE GRADUATE SCHOOL

OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF

MASTER OF SCIENCE

UNIVERSITY OF FLORIDA

2016

© 2016 Nicholas T. Homziak

To: Mary, Jurij, Allie, and Maya, and Nichole

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ACKNOWLEDGMENTS

Foremost, I sincerely thank Dr. Kawahara and Dr. Branham for their support

throughout this study. Dr. Kawahara provided assistance in developing this project,

provided funding for field expeditions to French Guiana and Rwanda, and helped me

complete this project, including reviewing countless drafts of this thesis. My sincere

thanks also goes to my co-chair, Dr. Marc Branham for providing a research

assistantship for my first year of my Masters research, and for his guidance and

understanding as I adjusted to life as a graduate student while working in his lab, in

addition to his thoughtful and helpful suggestions regarding the scope of this project.

This project would not have been possible without the help of Dr. Jesse

Breinholt. He spent many hours helping prepare the crucial sequence data so that it

could be analyzed. He was always gladly willing to sit down with me to share his

knowledge of molecular phylogenetics. I thank him for his patience and time taken to

teach me these methods over many days.

I was very fortunate to be able to conduct my research at the McGuire Center for

Lepidoptera and Biodiversity, where in addition to the facilities, there are many people

who make it such a great place to work. I would like to offer my sincere gratitude to Dr.

Lei Xiao for teaching me proper lab protocol and extraction techniques, in addition to

keeping the molecular lab in great shape to work in. I would also like to thank Dr.

Marianne Espeland for answering numerous questions regarding DNA extraction

techniques. My sincere gratitude goes to Samm Epstein and the Kawahara lab

volunteers for their help in preparing the wing vouchers of molecular specimens that I

used in this project. I would not be able to complete a project such as this without their

help. I would also like to thank Geena Hill, Peter Houlihan, Chris Johns, Oliver Keller,

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Jack Kramer, Matt Moore, David Plotkin, Lary Reeves, and the other Kawahara and

Branham lab members. Additional McGuire Center students and staff, including Dale

Halbritter, Shinichi Nakahara, Elena Ortiz Acevedo, and Matt Standridge, were very

helpful and provided enjoyable company.

I also thank Dr. Kelly Miller of the University of New Mexico, who introduced me

to Dr. Kawahara and Dr. Branham during my undergraduate studies, and for his

significant funding contributions to my fieldwork in Kenya in the summer of 2013.

This research would not have been possible without the help from many other

institutions both here and abroad. Dr. Dino Martins of Nature Kenya for granted me

permission to collect samples for this project during that trip, Dr. Nathan Kabanguka

helped procure collecting permits in Rwanda, and Philippe Gaucher and Jerome Chave

helped to arrange our fieldwork in French Guiana. Dr. Seth Bybee and Dr. Gavin

Svenson graciously allowed me to take part in the collecting expedition to Rwanda they

organized in the summer of 2014.

My sincere thanks go to the library staff at both the University of Florida, and the

Florida Department of Plant Industry. I would not have been able to conduct as

extensive a literature review without their help.

I thank my family Mary, Jurij, Allie, and Maya for their unwavering support of my

studies. From paper editing to pep talks, I am sincerely thankful for their love, support

and encouragement with this project, and for my life long interest in Lepidoptera.

Special thanks to Nichole -- I am grateful for her support and encouragement during the

most challenging moments of this project, sharing kind words, inspiration and great

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company. I could not ask for a better person to be by my side as I worked on this

project.

I thank the National Science Foundation for their financial support through the

Graduate Research Fellowship Program, funding the second year of my Masters

research.

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TABLE OF CONTENTS page

ACKNOWLEDGMENTS .................................................................................................. 4

LIST OF TABLES ............................................................................................................ 9

LIST OF FIGURES ........................................................................................................ 10

ABSTRACT ................................................................................................................... 11

CHAPTER

1 INTRODUCTION .................................................................................................... 13

2 REVIEW OF EREBINAE CLASSIFICATION .......................................................... 16

Period 1: Early Classifications (1816-1902) ............................................................ 16

Period 2: Hampson's Division (1902-1984) ............................................................. 19 New Character Systems: Genitalia and Tympanum ............................................... 21 Additional Morphological Character Systems ......................................................... 25

Period 3: Cladistics and Erebine Classification (1984 - Present) ............................ 26 Current Status of the Erebinae ............................................................................... 33

Tribes of the Erebinae............................................................................................. 34 Acantholipini ..................................................................................................... 34 Arytrurini ........................................................................................................... 35

Audeini ............................................................................................................. 35

Catephiini ......................................................................................................... 36 Catocalini .......................................................................................................... 37 Cocytiini ............................................................................................................ 37

Ercheiini............................................................................................................ 38 Erebini .............................................................................................................. 38 Euclidiini ........................................................................................................... 38

Hulodini ............................................................................................................ 40 Hypopyrini ........................................................................................................ 40 Melipotini .......................................................................................................... 40 Ommatophorini ................................................................................................. 42 Omopterini ........................................................................................................ 43

Ophiusini .......................................................................................................... 43

Pandesmini ....................................................................................................... 44

Pericymini ......................................................................................................... 44 Poaphilini .......................................................................................................... 45 Sypnini.............................................................................................................. 47 Thermesiini ....................................................................................................... 47

3 ANCHORED PHYLOGENOMICS RECOVERS A ROBUST PHYLOGENY OF EREBINAE .............................................................................................................. 54

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Methods .................................................................................................................. 56

Taxon and Gene Sampling ............................................................................... 56

DNA Sequencing and Alignment ...................................................................... 57 Phylogenetic Analyses ..................................................................................... 57

Concatenation analyses. ............................................................................ 58 Species-tree methods ................................................................................ 59

Results .................................................................................................................... 60

Sequence Capture ........................................................................................... 60 Rogue Taxa and Maximum Likelihood ............................................................. 60 Parsimony Analysis .......................................................................................... 63 Coalescent-Based Methods ............................................................................. 63 Hypothesis Testing ........................................................................................... 64

Discussion .............................................................................................................. 64

Systematic Relationships of the Erebinae ........................................................ 66 Basal Erebinae. .......................................................................................... 66

Clade A ...................................................................................................... 67

Clade B ...................................................................................................... 69 SH Tests ........................................................................................................... 71

Conclusions ............................................................................................................ 71

LIST OF REFERENCES ............................................................................................... 82

BIOGRAPHICAL SKETCH ............................................................................................ 91

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LIST OF TABLES

Table page 3-1 Complete specimen data, showing all taxa included in this analysis, source of

genetic material (DNA,RNA) and accession number. ......................................... 78

3-2 Results of SH tests implemented in RAxML to test previously proposed classifications of Erebinae. D(LH) is the difference in log likelihood units between the best constrained tree and the best unconstrained tree. ................. 81

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LIST OF FIGURES

Figure page 2-1 Graphical representation of Hampson's 1902 key to the subfamilies of the

Noctuidae. .......................................................................................................... 48

2-2 Redrawn ‘tree’ from Richards (1932), which was based on a morphological analysis of noctuoid tympana. ............................................................................ 49

2-3 "Tree" representing the arrangement of Berio's (1960) "Phyla" (putative monophyletic groups) within the former Catocalinae. ......................................... 50

2-4 Cladogram representing subfamilial relationships of the Noctuoidea by Kitching (1984). .................................................................................................. 51

2-5 Maximum Likelihood tree showing Erebinae relationships according to Zahiri et al. (2011). ....................................................................................................... 52

2-6 Maximum Likelihood tree showing Erebinae relationships proposed by Zahiri et al. (2012). ....................................................................................................... 53

3-1 Pairwise sequence completeness across all included taxa. ............................... 73

3-2 Maximum Likelihood IQ Tree, inferred from the partitioned nucleotide alignment using the k-means algorithm. Bootstrap support values are shown at each node. ...................................................................................................... 74

3-3 Maximum likelihood IQ tree from the unpartitioned nucleotide analysis. Bootstrap support values are shown at each node. ............................................ 75

3-4 Tree inferred from parsimony analysis in TNT. Bootstrap support values are shown after each node. ...................................................................................... 76

3-5 Species tree inferred using ASTRAL from gene trees. Bootstrap values are shown after each node. Nodes with bootstrap support less than 70 are collapsed. ........................................................................................................... 77

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Abstract of Thesis Presented to the Graduate School of the University of Florida in Partial Fulfillment of the Requirements for the Degree of Master of Science

SYSTEMATICS AND PHYLOGENOMICS OF THE EREBINAE

(LEPIDOPTERA: NOCTUOIDEA, EREBIDAE)

By

Nicholas T. Homziak

August 2016

Chair: Akito Kawahara Cochair: Marc Branham Major: Entomology and Nematology

The Erebinae is one of the most speciose subfamilies of the Erebidae, and is

estimated to contain over 4000 species (Poole 1989). Larvae of these moths feed a

broad range of hosts plants. Many genera feed on grasses and legumes, and the

subfamily contains numerous species of economic importance. A number of species

also possess striking aposematic coloration, which consists of black contrasting with a

range of bright colors. Despite these numerous interesting aspects of their biology,

resolving the classification of these moths has challenged researchers for over 200

years.

Here we present a review of the taxonomic history of the Erebinae, followed by a

phylogenomic study based on anchored hybrid enrichment sequencing. The taxonomic

history of the Erebinae is divided into three main periods, with discussion of principal

developments in each. Current hypotheses for relationships within the subfamily are

then reviewed. The phylogenomic study consists of a maximum likelihood (ML) analysis

partitioned by site along with a ML analysis of the unpartitioned dataset, a parsimony

analysis, and a gene tree - species tree analysis. The results of this study recover the

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first backbone phylogeny with robust support for the subfamily. Results of the

unpartitioned likelihood analysis are compared to previous hypotheses based on

morphology (Berio 1960) and molecular data (Zahiri et al. 2012) using the SH test.

Potential implications of this study for future research on various aspects of Erebine

biology are discussed.

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CHAPTER 1 INTRODUCTION

The Erebidae is one of the most diverse families within the order Lepidoptera

(Zahiri et al., 2011), with nearly 25,000 described species (van Nieukerken et al., 2011).

The nominal subfamily Erebinae contains approximately 4500 species, based on the

estimate for the Catocalinae given by Poole (1989). The subfamily is distributed

worldwide, but with the highest diversity in the tropics. Some species (e.g., Zale

phaeograpta) are known to be agricultural pests (Vazquez et al., 2014). Larvae of

Erebinae feed on pines (e.g. Zale), grasses (e.g. Mocis), along with a broad range of

angiosperms (Wagner et al., 2011). Pupae possess an alcohol insoluble bloom, the

origin of which remains unclear (Mosher, 1916; Holloway, 2005)

Erebinae also possess numerous highly derived means of predator defense.

The most readily apparent of these is their wing coloration and patterning. It is

postulated that the wing coloration of these moths confers a selective advantage

through camouflage, aposematic displays, and involvement in mimicry complexes

(Kitching and Rawlins, 1998). Erebine moths also possess sensitive auditory structures

(tympana), which are used to detect the approach of echolocating bats and other

predators (Fullard and Napoleone, 2001). Despite the potential of erebine moths as

model systems for studies of ecology and evolutionary biology, such studies are largely

limited to a handful of temperate genera. Several factors contribute to our limited

understanding of the biology of these moths. The bulk of erebine diversity is located in

tropical areas where the fauna is poorly known, and the accurate identification of most

erebine species remains difficult. Additionally, the the subfamily is distinguished

primarily based on molecular characters and only a limited number of genera have been

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included in molecular phylogenetic studies to date. Consequently, the taxonomic limits

of the subfamily are presently unclear, and the inclusion of numerous genera within the

subfamily needs to be confirmed. This review examines all previously proposed

hypotheses regarding the classification of erebine moths, to serve as a basis for future

studies of the phylogenetics and biology of this subfamily.

Although the Erebidae and the Noctuidae are recognized as distinct families,

they were only recently separated, primarily on the basis of molecular evidence. The

taxonomic history of the Erebinae is intertwined with that of the Noctuidae and other

erebid subfamilies. The first period of Erebine classification began in the early 19th

century, from the division of Noctua Linnaeus by Hübner until to the development of

Hampson's classification at the end of that century. Classifications from this time are

based primarily on temperate fauna, which represents only a fraction of erebine

lineages (Kühne and Speidel, 2004). As authors examined greater numbers of tropical

taxa, they faced with the challenge of classifying a diversity of similar moths belonging

to the Erebinae and other erebid subfamilies. This led to several hypotheses for the

higher-level classification of erebine species. (Kitching 1984). The most significant of

these was the classification proposed by Guenée (1852a; 1852b), which divided

Noctuidae into two groups based on hind wing venation. Under his classification,

Erebinae belonged to the group with a well developed vein M2 in the hindwing, later

known as the"quadrifine" Noctuidae. Many subsequent publications throughout the 19th

century maintained this division of the Noctuoidea. However, the classification below

this division remained largely in flux. Building upon the division proposed by Guenée,

Hampson (1902) proposed new classification, beginning the second period of Erebine

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classification. This classification divided the current Erebinae into two subfamilies based

on the presence or absence of tibial spining. Despite early recognition that this division

was based on a homoplastic trait, Hampson’s system was widely employed for most of

the 20th century. The introduction of cladistic methodology brought about the beginning

of the third period of erebine classification. This period was characterized by significant

efforts to identify homologous characters which could be coded for cladistic analysis

(e.g., Kitching (1984), Mitter and Silverfine (1988)).

Molecular studies soon followed, the results of which grouped the families

Arctiidae and Lymantriide with the majority of the quadrifine Noctuidae. Consistent

molecular support for the monophyly of this group led to the recognition of the Erebidae

as a separate family from the Noctuidae. Further molecular analyses of the Erebidae by

Zahiri et al. (2011; 2012) led to the recognition of the Erebinae as currently defined.

Here we provide a review of the taxonomic history of the Noctuoidea from the

perspective of the Erebinae to understand the earlier classifications under which many

erebine genera remain formally placed, and to lay a framework for future studies on the

biology of this diverse group of taxonomically challenging moths.

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CHAPTER 2 REVIEW OF EREBINAE CLASSIFICATION

Period 1: Early Classifications (1816-1902)

Hübner (1816 [1816-1826]) proposed the first higher level classification for the

Noctuoidea Under this system, Hübner separated the genus Noctua Linnaeus into six

taxonomic levels, roughly corresponding to the modern superfamily, family, subfamily,

tribe, genus, and species (Hemming, 1937). Hübner split erebine species among nine

subfamilies within the family Semigeometrae. This family included part of the current

Noctuidae as well as other erebid subfamilies. Further details on the classifications

proposed by Hübner can be found in Hemming (1937) and Kühne and Speidel (2004).

The next major development in erebine classification began in the late 1830s,

when Gueneé started work on a new classification of Lepidoptera, which changed over

the course of its six-part publication. Finalized in 1841, Gueneé placed the current

erebines in the family Noctuélides, which he subdivided into 18 tribes (Gueneé, 1841).

Gueneé and subsequent authors continued this process of uniting similar genera into

groups, forming the foundation of Noctuoidea systematics (Kühne and Speidel, 2004).

Guenée’s classification divided erebine species between the tribes Catocalidi, Noctuo-

phalaenidi and Ophiusidi of the family Noctuélides (Gueneé, 1841). Subsequent studies

of European fauna largely followed this classification. Among these was the

classification of Herrich-Schäffer (1845), who developed an alternative classification

under the family name Noctuidae. This combined Gueneé’s Ophiusidi and Catocalidi

into the subfamily Ophiusidae. This united the majority of known erebine species under

a single subfamily.

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Building upon his previous work as well as ideas proposed by Herrich-Schäffer

(1845) and other, Gueneé developed a second classification (Guenée 1852a; 1852b).

The Noctuidae was split between two "divisions": Noctuélites, and Deltoïdes (Kitching,

1984). The Noctuélites was then divided into two "phalanges": Trifidae and Quadrifidae,

based on the degree of development and location of vein M2 in the hind wing (Kitching,

1984). The classification divided current Erebinae among the eight tribes of the

Quadrifidae (Kitching, 1984). While informal, Gueneé's Trifidae and Quadrifidae formed

the basis of the "trifine" and "quadrifine" division of the Noctuoidea, which is still referred

to today (Kitching, 1984). Guenée's (1852a; 1852b) classification became the

systematic basis for the studies of noctuoid moths for the next half century. Walker

(1857-1858) employed Gueneé's system in his list of specimens in the British Museum

(Kitching, 1984; Kühne and Speidel, 2004). This influential work helped to further

establish Gueneé's classification (Kitching, 1984). Other studies such as Moore (1884-

1887) on Sri Lankan fauna, Cotes and Swinhoe (1888) on Indian fauna, Pagenstecher

(1894) on Javanese fauna, Kirby (1897), covering a subset of global fauna, and Tutt

(1896) on the British fauna were based on Gueneé's classification. A more detailed

review of Guenée's classification can be found in the review by Kitching (1984).

Despite its wide acceptance, some North American authors took issue with the

divisions employed by Gueneé (Kitching, 1984). Packard (1869) criticized Gueneé's

reliance on venation characters, and instead used a combination of characters from the

head, antennae, body vestiture, and wing shape and coloration. This study was based

largely on temperate fauna, divided the Noctuidae between the subfamilies Noctuinae

and Catocalinae with current Erebinae falling under the latter (Kühne and Speidel,

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2004). The Noctuinae and Catocalinae of Packard largely followed Gueneé's Trifidae

and Quadrifidae, respectively (Kitching, 1984).

Other North American authors followed. Grote (1874) adhered to Packard's

divisions, but altered the division of the Noctuidae in a subsequent classification (Grote,

1882). Grote (1882) divided the family into two groups, the “Noctuelitae fasciatae” and

“Noctuelitae nonfasciatae”, which roughly correspond with Packard's Noctuinae and

Catocalinae. All taxa belonging to the Erebinae fell under the Noctuelitae fasciatae,

across several subfamilies. Grote (1889; 1890a; 1890b) further refined this earlier

classification, with current erebine species divided between two tribes, the Catocalini

and the Phaeocymini of a redefined Catocalinae. Grote divided these two tribes

primarily by adult resting position; the Catocalini resting with the hind wings covered by

the forewings, and the Phaeocymini resting with the hind wings partially exposed

(Grote, 1890a). Grote (1895) subsequently revised this classification, dividing the

Catocalinae into 13 tribes based on comparisons of adult morphology, although he did

not list the characters used to separate the groups. Grote (1895) divided current erebine

species among the tribes Ascalaphini, Catocalini, Euclidiini, Melipotini, Ophiderini,

Pheocymini, Pangraptini, and Thysaniini. In addition to the Erebinae, these tribes

included taxa belonging to other erebid and noctuid subfamilies.

Contemporaneously with Grote, Smith (1882-83) proposed an alternative

classification for noctuoid moths. Smith subdivided the Noctuidae and provided

characters used for each division, creating a rough key to facilitate the identification of

specimens (Smith 1882-83). Smith did not assign any formal names to these groups –

he considered them to be completely artificial (Smith 1882-83). He did, however, make

19

note of genera he thought were synonymous or closely related including several within

the current Erebinae (Smith, 1882a; Smith, 1882b).

Period 2: Hampson's Division (1902-1984)

Hampson brought the next major development in the classification of erebine

moths. Initial development began with the publication of a novel classification for the

Noctuidae (including the current Erebinae) in a series of publications from 1893-95 on

the Fauna of British India. This classification divided Gueneé's concept of the

Quadrifidae

between several subfamilies (Kitching, 1984). Developed in part from Guenée’s

classification, the novel classification of Hampson placed most current Erebidae in the

subfamily Quadrifinae, which he distinguished based on characters of the vestiture,

labial palpi, legs, and wing venation (Hampson, 1894). This was the most speciose

subfamily in the Noctuidae, and contained taxa currently belonging to the Erebidae,

Noctuidae, and Nolidae. Soon afterwards, Hampson (1902) proposed a novel

classification of the Noctuoidea, which is redrawn to show its pattern of relationships

(Figure 1-1). Under this classification, current Erebinae belonged to the subfamilies

Noctuinae and Homopterinae, with Homopterinae possessing spined middle tibiae and

the Noctuinae without (Hampson 1902). Hampson’s usage of the name Noctuinae was

at odds with any previous uses of that name. Contrary to established precedent,

Hampson determined that the type of Noctua Linnaeus was Phalaena Noctua strix

Linnaeus, and as it was the first species listed in Linnaeus 1758, it should serve as the

type species of the Noctuidae (Kühne and Speidel, 2004). The description of Phalaena

Noctua strix was based on a mixture of the erebine Thysania agrippina (Cramer) and

Xyleutes strix (Linnaeus), a cossid (Fletcher and Nye (1982:170) in (Kühne and Speidel,

20

2004)). Previous authors attributed the description to the cossid, but Hampson’s

interpretation assigned it to the Noctuidae (Kühne and Speidel, 2004). As such,

Hampson referred to the trifine noctuids as the subfamily Agrotinae (Kitching, 1984;

Kühne and Speidel, 2004). Aside from Hampson and Seitz, authors referred to this

subfamily as the Ophiderinae (Ophideridae, Guenée 1852), which had priority and was

in common use (Kitching, 1984; Kühne and Speidel, 2004). In the Catalogue of the

Lepidoptera Phalaenae of the British Museum, Hampson reverted back to the

Catocalinae from the Homopterinae, which he covered in volumes 12 and 13

(Hampson, 1913a; 1913b). The volume treating the Noctuinae was never published,

although all descriptions of new genera and species of Noctuinae in Hampson's

unfinished manuscript were published separately (Gahan, forward to Hampson 1926).

Hampson was regarded as a global expert on the Noctuidae, and his

classification and nomenclatural changes became widely accepted. However, a number

of contemporary workers found issues with the characters he used to separate the

noctuid subfamilies. Forbes (1914) published a study of eastern North American noctuid

genera, which followed the general format of Smith (1882-1883), forming groupings of

possibly related or synonymous genera, as well as a key and taxonomic notes. He

generally adhered to the classification of Hampson (1913a; 1913b), but noted that a

number of moths could not be readily defined as quadrifine or trifine Noctuidae. These

moths showed an intermediate reduction of the M2 vein in the hind wing, a condition

which he referred to as "intermediid" (Forbes, 1914). More detailed criticism came from

Prout (1921) in a study of global Noctuidae. She presented several lines of evidence

suggesting that Linnaeus' description of N. strix actually referred to the South Asian

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cossid, and not the Neotropical T. agrippina. She proposed reinstatement of Gueneé's

Ophiderinae as a replacement for Hampson's Noctuinae, but noted that Othreis Hübner

had priority over Ophideres Boisduval (Prout, 1921). Many subsequent workers followed

the opinions of Prout, and referred to Hampson's Noctuinae as the Ophiderinae or

Othreinae. Prout also criticized the use of tibial spining to separate the Catocalinae and

the Ophiderinae. She noted that Hampson himself remarked that many catocaline

genera appear to have close relatives within the Noctuinae. The numerous instances

Prout observed of genera in separate subfamilies closely resembled each other led her

believe that an alternative method of classifying this group of moths would eventually be

necessary (Prout, 1921).

Still, subsequent large-scale treatments of noctuoid taxa largely adopted

Hampson’s classification system. In a check list of North American Lepidoptera, Barnes

and McDunnough (1917) renamed Hampson's Noctuinae the Erebinae, but otherwise

followed Hampson's system (Kitching, 1984). Seitz's influential Macrolepidoptera of the

World series also largely adopted Hampson's system although Gaede, in the treatment

of the African noctuid fauna (in Seitz 1913-39) noted that the division between the

Catocalinae and Noctuinae was arbitrary (Kitching, 1984).

New Character Systems: Genitalia and Tympanum

Earlier studies of the Noctuoidea relied on characters of the habitus for

identification and classification. This began to change in the late 19th century, as

advances in microscopy permitted more detailed study of moth anatomy. During this

time, some noctuid workers began to study the morphology of the genitalia and the

tympanal region, and found that these areas contained characters potentially useful for

classification of this group of moths. These studies further demonstrated the

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shortcomings of Hampson's division between the Catocalinae and Ophiderinae. Smith

(1908) pioneered the taxonomic use of genitalia within the Noctuoidea, providing some

of the first figures of erebine genitalia in revision of taxa presently belonging to Zale

Hübner. In the Palearctic, John (1909; 1910) was one of the first to employ genitalia

characters in treatments of erebine genera, and provided numerous figures of male and

female genitalia.

The use tympanal morphology brought another approach to the study of

Noctuoidea classification in the early 20th century. Eggers (1919) was the first to give

detailed descriptions of Lepidoptera tympanal morphology. Most of his studies were

based on the erebine genus Catocala Schrank; the large size of these moths facilitating

the observation of the internal structures (Eggers, 1919). He also surveyed the

tympanal morphology of a range of moths from around the world, including a number of

current Erebine genera. In these observations, Eggers noted instances where

similarities in tympanal structure may indicate relatedness among genera. Richards

(1932) published a detailed study of the noctuoid tympanum, covering taxa belonging to

the current Noctuidae and Erebidae. In this study, he proposed groups of genera based

on similarities in tympanal morphology, but did not assign any formal names to the

groups. Six of these belonged to what he termed the "Erebine and Catocaline complex",

and included Hampson's Catocalinae and Noctuinae (Richards, 1932). Richards divided

the current Erebinae between four of these groups (Figure 1-2). In the course of his

study, he found no evidence supporting the division between the Catocalinae and

Ophiderinae, and noted numerous instances where the division separated otherwise

very similar genera (Richards, 1932). Further studies by Richards (1935a; 1935b; 1936;

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1939) on erebine species continued the process of grouping potentially related genera

based on similarities on tympanal morphology. In a widely used checklist of North

American Lepidoptera, McDunnough (1938) opted to combine Hampson's two

subfamilies under the Catocalinae. This decision was informed by the recent work by

Richards, and comparative study of male genitalia (Kitching, 1984). In a summary of his

research on the Lepidoptera tympanum, Kiriakoff (1963) proposed a classification that

differed radically from previous classifications of the superfamily. Under this scheme, a

broadly inclusive Noctuidae contained two subfamilies, the Arctiinae, and the Noctuinae

(Kiriakoff, 1963). Of the quadrifine Noctuidae, the Herminiinae was treated as an

infrafamily (Herminiini) of the subfamily Arctiinae, along with the infrafamilies Arctiidi and

Lymantriidi, based on the presence of a prespiracular tympanal hood. Kiriakoff placed

the remaining quadrifine Noctuidae Noctuinae, infrafamily Noctuini, along with the trifine

Noctuidae on the basis of the shared postspiracular tympanal hood (Kiriakoff, 1963).

Although it excluded the quadrifine Noctuidae which contains numerous erebid

subfamilies, this concept of the Arctiinae provides an early indication of the current

Erebidae.

Although many Noctuoidea workers adopted the use of genitalia morphology to

identify species and define genus groups, a limited number of studies attempted to use

genitalia morphology to investigate taxonomic relatioships above the genus level among

current Erebinae. Studies by Berio (1960; 1965) and Wiltshire (1970) used genitalia, but

also a range of additional characters to identify groups of related species and redefine

the limits of numerous old world Erebine genera. Tikhomirov (1979) undertook a

detailed study of noctuoid genitalia morphology, examining a number of taxa currently

24

belonging to the Erebidae and Noctuidae and noting characters within the male genitalia

that could serve to unite taxonomic groups. Particularly, all erebid moths he examined

share a reduction of the genital muscle M2, although he was unable to find other

characters which could reliably separate noctuid subfamilies (Tikhomirov 1979). Mitter

(1988) also explored relationships among erebine genera using genitailia morphology.

Specifically, he examined internal reproductive structures of several erebine genera

related to Catocala, describing their variation and identifying some characters of

potential taxonomic utility. Speidel and Naumann (1995b) followed with a similar study,

using internal characters of the female genitalia to define limits of the erebine tribe

Euclidiini Following Speidel and Naumann (1995b), Matov (2003) reviewed the old

world Euclidiini and Synedini [Melipotini] in a study based on external and internal

genitalia of both sexes. He concluded that definition of the Euclidiini (sensu Speidel and

Naumann 1995b) contained several unrelated groups of species united by convergent

features. On this basis, Matov (2003) re-elevated the Synedini to tribal status, citing a

number of differences in adult morphology, as well as larval feeding habits. He

determined that this tribe was most closely related to the Melipotini based on a number

of similarities in the male genitalia. Matov also noted several features of both the

Synedini and Euclidiini indicating relatedness to the Catocalini. These included

similarities in the sternite VII and ovipositor of the Synedini, as well as similar features of

the male genitalia and a distinctive subreniform spot in the Euclidiini. Although Speidel

and Naumann suggested that the Anumetini was closely related to the Euclidiini, Matov

found several characters which indicated only a distant relationship between the two

tribes. Matov found that the Ercheiini also was close to the Euclidiini, with notably

25

similar female genitalia. The distinguishing feature of female Ercheiini is an appendix

connected to the bursa copulatrix by a narrow canal, while males have distinctively

sclerotized claspers and symmetric valvae (Matov, 2003). He also found that male

Ercheiini also share an elongated and widened costa with the Euclidiini and the

Catocalini (Matov, 2003). Matov disagreed with the placement of Tinolius Walker in the

Euclidiini, noting that the genitalia of Tinolius only vaguely resembles the rest of the

Euclidiini, and possesses distinctive enough morphology to question its placement

within the Catocalinae. Recent molecular data confirms this hypothesis, placing Tinolius

in a subfamily only distantly related to the Erebinae (Zahiri et al., 2012).

Additional Morphological Character Systems

In addition to genitalia and tympanal morphology, some authors used other

character systems to define groups currently in the Noctuoidea. For instance, after

studying European and North American pupae, Mosher (1916) determined that the

presence of an alcohol insoluble, waxy bloom could serve to separate the Catocalinae

from the rest of the Noctuidae., In a series of papers on Indian noctuid larvae, Gardner

distinguished a number of groups of genera based on larval morphology (1946a; 1946b;

1947; 1948b; Gardner, 1948a). In these larval studies, and another on noctuoid pupae,

Gardner was unable to find any characters that could serve to separate Hampson's

Catocalinae and Noctuinae. Similar studies of North American and European noctuid

larvae followed. Crumb (1956) divided the family into six subgroups based characters of

the larvae, while Beck (1960) divided the European Catocalinae into two tribes. Neither

of these studies found a distinction between the Ophiderinae and the Catocalinae using

larval characters.

26

In a study of the Lepidoptera compound eye, Yagi and Koyama (1963) were also

unable to find any distinction between these two subfamilies. In this study, they

proposed phylogenetic relationships within then-accepted noctuid families based on eye

morphology. However, they did not attempt to test the monophyly of the families.

Included in this concept of the Noctuidae were members of the current Erebidae,

Hyblaeidae, and Noctuidae. In their tree of this group, members of the current Erebinae

belonged to a single clade, along with other erebid and noctuid genera. Still, other

studies attempted to use characters of the proboscis to identify related groups of

noctuoid moths (Speidel and Naumann, 1995a; Speidel et al., 1996b). Speidel et al.

(1996b) proposed the dorsally located sensilla styloconica on the proboscis as an

apomorphy supporting the Catocalini.

Period 3: Cladistics and Erebine Classification (1984 - Present)

The efforts by Berio (1960; 1965) and Wiltshire (1970; 1976) to identify

phylogenetic units based upon putatively shared, derived character states marked the

begnnings of the application of cladistic methodology to research on Erebinae. Berio

(1960) undertook a systematic study of mostly Old World genera to assess the division

between the subfamilies Catocalinae and Othreinae [Ophiderinae]. In this study, Berio

found evidence to thoroughly demonstrate the artificiality of Hampson's division of the

two subfamilies based on tibial spining. In addition to reviewing evidence presented in

previous studies, he assigned each included genus to one of eight grades based on the

number of tibial spines. Berio found some cases where the degree or presence of tibial

spining varied between sexes within the same species. Berio also noted that Hampson

overlooked the presence of tibial spines in some genera. From these data, Berio came

to several conclusions: that the degree of tibial spining is variable among genera, and

27

decreases as the complexity of the androconia increases; that spined tibia is the

ancestral condition; and that genera with tibial spining can be quite dissimilar to each

other, while spined and spineless genera can be closely related.

After demonstrating the flaws with Hampson's classification, Berio proposed

groups of genera united by putative synapomorphies, which he termed "phyla" (Figure

1-3). He determined that the relative location of the "phyla" within the phylogeny could

be determined based on the position of the androconia. A number of these "phyla"

correspond to groups currently supported by molecular evidence, with only the Phylum

of Cyligramma paraphyletic with respect to the phylogeny of Zahiri et al. (2012).

Informed by the studies of Berio and Wiltshire, (Kitching, 1984) conducted a

morphological cladistic analysis of the Noctuoidea (Figure 1-4). Like the earlier

morphological studies, Kitching was unable to find any other morphological characters

that supported the separation of the Catocalinae and Ophiderinae, and united all taxa of

these two subfamilies under a broadly defined Catocalinae, with the exception of

Catocala and Othreis (Kitching, 1984).

Mitter and Silverfine (1988) continued to apply cladistic principles to the study of

erebine taxa, using characters of the tympana and genitalia selected for their potential

to resolve the phylogenetic relationships between Catocala and several closely related

genera. Following Kitching (1984), Speidel et al. (1996a) conducted the next

morphological phylogenetic study of the Noctuoidea. Although the authors did not

conduct a formal phylogenetic analysis, they identified putative synapomorphies based

on morphological surveys. The authors primarily examined genitalia and tympana, but

also used the presence of an abdominal brush organ, length of tibial spurs, and the

28

presence or absence of some larval characters. None of the characters examined by

Speidel et al. were consistent throughout the current Erebinae. In the classification of

Speidel et al. (1996a), all erebine species fell within a group termed “Clade 4", within an

unresolved polytomy. This clade contains a large number of the former Catocalinae, a

group that has been traditionally defined by an absence of characters (Speidel et al.,

1996a). Based on their findings, Speidel et al. (1996a) claimed that the presence of a

finger-like adenosoma and elongate tibial spurs supported a monophyletic Noctuidae,

contrary to the results of Weller et al. (1992; 1994). Informed by this analysis and

previous studies, Speidel et al. (1997) transferred the enigmatic erebine genus Cocytia

Boisduval from its monobasic subfamily to the Catocalini.

Fibiger et al. (2003) presented a phylogeny of European Catocalinae based on

putative synapomorphies identified from morphological studies. The characters used

included features of wing patterning, resting position of the wings, scaling of the frons,

and features of the male and female genitalia. Although his study focused on European

taxa, Fibiger et al. (2003) examined a number of genera occurring outside of Europe.

Fibiger et al. (2003) divided the current Erebinae among several subtribes within the

Catocalini. Potential synapomorphies are given for several of these subtribes, which the

authors further divided into numerous genus-groups, some of which correspond to

currently recognized tribes of the Erebinae

By the 1990s, advances in sequencing technology had made it possible to

include molecular characters in phylogenetic analyses of the Noctuoidea. Weller et al.

(1992) conducted a phylogenetic analysis of the Noctuoidea based on conserved rRNA

regions. Their study included current Aganainae, Arctiinae, Erebinae, Hypeninae, and

29

Lymantriinae. In their study, the Arctiidae grouped with the Catocalinae and the other

noctuid subfamilies in a large, unresolved polytomy. Following this study, Weller et al.

(1994) conducted a parsimony analysis of noctuoid moths using regions of a ribosomal

gene (28s), and a mitochondrial locus (ND1). Surprisingly, the Noctuidae was not

recovered as monophyletic in the analyses of either gene (Weller et al., 1994). Despite

low branch support values, the quadrifine Noctuidae [Erebidae] consistently grouped

with the Arctiidae [= Arctiinae], and often with the Lymantriidae [= Lymantriinae]. Weller

et al. (1994) considered these results to be preliminary, and recommended further

studies including additional genes and taxa before making any taxonomic changes.

Support for the monophyly of the clade consisting of the Lymantriidae, Arctiidae, and

quadrifine Noctuidae increased with subsequent studies. Phylogenetic studies using

regions of one nuclear gene by Mitchell et al. (1997), EF-1α, Fang et al. (2000), DDC,

and using two nuclear genes, DDC and EF-1α (Mitchell et al., 2000), united current

erebid subfamilies in a single clade. The results of these studies brought further

evidence against the monophyly of the Noctuidae.

Kitching and Rawlins (1998) reviewed developments in the classification of the

Noctuoidea as of 1992 (Yela and Kitching, 1999). The authors included a morphology-

based key to its subfamilies and proposed several changes in the classification of the

noctuid subfamilies, notably by restricting the subfamily Calpinae to moths with

proboscides modified for fruit piercing; the genera removed were placed into an

explicitly paraphyletic Catocalinae. Kitching and Rawlins also noted that the pupae of

genera related to Catocala and Mocis Hübner are often covered in a waxy bloom. The

noctuid phylogeny proposed by Yela (1997) followed the same view, placing current

30

Erebinae within an inclusive, paraphyletic Catocalinae. Yela and Kitching (1999) again

reviewed developments in the classification of the Noctuidae. In this review, Yela and

Kitching maintained the restriction of the Calpinae to specialized fruit-piercing taxa, and

followed Speidel et al. (1997) in placing Cocytia within the Catocalinae. Under this

classification, all Erebinae were united within a single, though polyphyletic subfamily.

The next major development in the classification of erebine moths arrived with a

review of Noctuoidea classification by Fibiger and Lafontaine (2005). The authors

reviewed recent developments in the classification of the Noctuoide, and proposed a

new classification based on their findings, which aimed to reconcile recent molecular

and morphological evidence. This classification was partially based on that of Kitching

and Rawlins (1998), but incorporated findings from other recent phylogenetic studies,

especially Fibiger (2003). They elevated the quadrifine Noctuidae to family status,

based on morphological evidence that generally agreed with molecular hypotheses, and

proposed the name Erebidae for the group. Although Kühne and Speidel (2004)

proposed use of the name Catocalidae, both the Herminiidae and Erebidae have priority

over that name, and have equal priority to each other. At the time of publication, the

name Erebidae had not been used since Forbes (1954) as a subfamily, while the name

Herminiidae currently was applied as a subfamily to a well-defined and long-standing

group of the Noctuidae. Fibiger and Lafontaine chose the name Erebidae, citing

concerns about the use of a name long associated with a group as well-defined as the

Herminiinae for such a large and heterogeneous family of moths. This classification

divided the current Erebinae among the subfamilies Erebinae, Catocalinae, and

Cocytiinae. Fibiger and Lafontaine followed Kitching and Rawlins (1998), and restricted

31

the subfamily Calpinae to a monophyletic group of fruit piercing moths, removing over

1000 genera from the Calpinae of Fibiger (2003). Fibiger and Lafontaine placed these

genera in the subfamily Erebinae, which they recognize as a para- or polyphyletic

group. They give a combination of morphological characters distinguishing the

Erebinae, but note that they are all plesiomorphic. The concept of the Catocalinae

proposed by Fibiger and Lafontaine contained genera which are currently placed in

several erebid subfamilies. Fibiger and Lafontaine followed the definition of the

Catocalinae proposed by Fibiger (2003) but removed two tribes (Tytini, Armadini) and

one subtribe (Aediina) to the Noctuidae. They define the Catocalinae (after the removal

of these genera) using the combination of characters given in Fibiger (2003), and give

two synapomorphies for the group. Regarding the Cocytiinae, Fibiger and Lafontaine

proposed no changes aside from its placement within the Erebidae rather than the

Noctuidae.

Following their previous study, Mitchell et al. (2006) conducted three

phylogenetic analyses based on two protein-coding nuclear genes, DDC and EF-1α.

The study focused mainly on trifine Noctuidae, but included several current erebine

taxa. The results of the final study, which included 144 species, showed significant

support (BP ≥ 90 %) for a clade consisting of Lymantriidae, Arctiidae, and quadrifine

Noctuidae, termed the "L.A.Q. clade". Notably, Mitchell found that the "LAQ clade"

excluded the Pantheinae and several other noctuid subfamilies with a quadrifine hind

wing venation. With this further evidence against the monophyly of the Noctuidae s.l.,

Mitchell et al. (2006) elevated the non-trifine noctuid subfamilies to family status, and

restricted the Noctuidae to the trifine subfamilies. Under this classification, current

32

Erebinae fell under the family Catocalidae, along with several other erebine subfamilies.

The authors also note the scant fossil record of the Noctuoidea, the earliest of which

date only to the Eocene (Mitchell et al. 2006).

Following Mitchell et al. (2006), Lafontaine and Fibiger (2006) again reviewed

recent developments in the classification of the Noctuoidea. Based in part on the

findings of Mitchell et al. (2006) and those of earlier morphological and molecular

studies, they concluded that the concept of the Erebidae as proposed in Fibiger and

Lafontaine (2005) was paraphyletic with respect to the Arctiidae and Lymantriidae. The

authors note that maintaining the Arctiidae and Lymantriidae as separate families would

require the elevation of numerous poorly defined subfamilies to family status. Rather

than adopt this approach, used by Mitchell et al. (2006), Lafontaine and Fibiger opted

instead to make the Noctuidae more broadly inclusive, including the Arctiidae and

Lymantriidae as subfamilies. This would ensure monophyly of the Noctuidae, and allow

the family to be easily diagnosed (Lafontaine and Fibiger, 2006). Under this

classification, current Erebinae fell under the subfamilies Catocalinae, Erebinae and

Cocytiinae. Within the Catocalinae, current Erebinae belonged to the tribes

Acantholipini, Arytrurini, Catephiini, Catocalini, Ercheini, Euclidiini, Melipotini, Ophiusini,

Hulodini, Hypopyrini, Ommatophorini, Pandesmini, Pericymini, and Sypnini.

Zahiri et al. (2011) compared the phylogenetic hypotheses proposed by

Lafontaine and Fibiger (2006) with a molecular phylogeny based on eight genes and

152 taxa from across the Noctuoidea (Figure 1-5). The study recovered the erebid

clade, including the Arctiinae and Lymantriinae, as one of six well-supported clades in

the superfamily. The authors re-elevated the Erebidae to family status. Within the

33

Erebidae, the analysis recovered the concepts proposed by Lafontaine and Fibiger of

the Catocalinae as paraphyletic with respect to the Erebinae, although support was low

for relationships within family level clades. Minet et al. (2011) developed a

morphological key and described potential synapomorphies for the families of the

Noctuoidea, as Zahiri et al. (2011) established these families solely on molecular

characters,. Minet et al. (2011) identified three potential synapomorphies for the

Erebidae: subalare sclerites that are distinctively shaped, with an narrow, elongated,

and flanged posterior arm, although they state that this character appears absent from

the subfamilies Rivulinae and Hypenodinae; the loss of a particular muscle (M2) in the

male genitalia; and long sensilla chaetica on male antennae. However, they note that

this character appears to be lost many times (Minet et al., 2011)

After Zahiri et al. (2011) was published online in 2010, Lafontaine and Schmidt

(2010) produced an updated checklist of the Noctuoidea of North America, which was

organized phylogenetically. Lafontaine and Schmidt separated the "quadrifine"

Noctuoidea, reflecting the results of the study by Zahiri et al. (2011). The authors

employed a concept of the Erebinae in this checklist that included genera currently

belonging to both the Toxocampinae and Erebinae. The tribal level classifications

mostly followed Fibiger and Lafontaine (2005), with current Erebinae belonging to the

tribes Thermesiini, Catocalini, Melipotini, Euclidiini, Poaphilini, and Ophiusini.

Current Status of the Erebinae

Zahiri et al. (2012) sought to better understand relationships within the Erebidae.

Their study was based on 237 taxa, sampling the eight genes used in their previous

study (Zahiri et al., 2011). The phylogenetic analysis of Zahiri et al. (2012) recovered 18

lineages with at least moderate support that were classified as subfamilies (Figure 1-6).

34

This forms the basis for the current concept of the Erebinae. Zahiri et al. (2012)

identified several synapomorphies of the Erebinae from previous studies, particularly,

Fibiger and Lafontaine (2005), Lafontaine and Fibiger (2006), and Speidel et al. (1997).

Distinguishing features of the adult are a proboscis with sensilla styloconica located

dorsally and a smooth apex, and the seventh sternite of the female reduced and cleft

into two lobes, with the ostium bursae located between the cleft (Zahiri et al., 2012).

Pupae often have a waxy bloom, while larvae are of a characteristic, slender,

streamlined shape, with a pair of dorsolateral tubercles on A8, and often with black

patches on the abdominal prolegs (Zahiri et al., 2012).

Tribes of the Erebinae

Zahiri et al. (2012) included 19 named tribes of Erebinae in their analysis, basing

tribal limits on molecular characters. Below we list the 21 tribes, which are presently

recognized in the Erebinae, and reivew morphological characters pertaining to each.

Acantholipini

Fibiger and Lafontaine 2005: Type genus Acantholipes Lederer 1857. Wiltshire

(1990) first used the name Acantolipini as a heading for two species of Acantholipes

which occur in Saudi Arabia. Wiltshire did not describe, diagnose, or give any indication

that the name was new, leaving the name a nomen nudum (Speidel and Naumann,

2004). Fibiger (2003) assumed that the name was valid from Wiltshire (1976), and

included the Acantholipina as a subtribe of the Catocalini, which contained the single

genus . Fibiger (2003) only included Acantholipes in the subtribe, and gave a list of

morphological synapomorphies for the group; its status as a nomen nudum was

identified by Kühne and Speidel (2004). Fibiger and Lafontaine (2005) formally

proposed the name Acantholipini, based on the diagnosis given in Fibiger (2003).

35

Fibiger and Lafontaine (2005) noted that the tribe is restricted to the old world. Zahiri et

al. (2012) included two species of Acantholipes in their molecular phylogeny. Several

other genera with uncertain subfamily affinity grouped with Acantholipes in their

analysis, forming the most basal clade within the Erebinae, which they identified . These

included the North American genus Euaontia Barnes & McDunnough, Ugia Walker of

the Old World tropics, and the African genus Ugiodes Hampson. Lafontaine and

Schmidt (2010) placed Euaontia within the Phytometrinae incertae sedis. Holloway

(2005) placed Ugia in his "Series of Miscellaneous Genera II" which he united on the

basis of a strikingly modified eighth abdominal segment in the male. Hampson

described the genus Ugiodes in the subfamily Noctuinae [= Ophiderinae], but was

otherwise not placed in subsequent classifications.

Arytrurini

Fibiger and Lafontaine 2005: Type genus Arytrura John 1912. As with the

Acantholipini, the name was first used in a catalogue heading by Wiltshire (1990) but it

was not formally proposed until its treatment in Fibiger and Lafontaine (2005). Fibiger et

al. (2003) diagnosed the tribe based on morphological features of the type genus. The

Arytrurini have not been included in any molecular analyses to date. However, their

morphology shows some similarities to erebine genera (Fibiger et al. (2003). It is

tentatively included within the Erebinae until further studies using molecular data

establish its position with greater certainty.

Audeini

Wiltshire 1990: Type genus Audea Walker 1858. Wiltshire proposed the name

Audeini in reference to the "Phylum of Audea" of Berio (1960), which contained species

belonging to Audea and Davea [Audea]. Berio separated the group on the basis of a

36

lack of femoral spines, and male femora with the proximal part enlarged to contain

androconia. Fibiger and Lafontaine (2005) included the tribe as a synonym of the

Catocalini, though Zahiri et al. (2012) maintained the separation of the two tribes in their

analysis. Two species of Audea represented the tribe in the phylogeny of Zahiri et al.

(2012), which strongly grouped as sister to the Catocalini. In their cladistic study of the

genera related to Audea and Catocala. Mitter and Silverfine (1988) found Hypotacha

Hampson to be more closely related to Audea than Catocala Schrank based on

morphology, while the phylogeny of Zahiri et al. (2012) indicated that Hypotacha may be

more closely related to Catocala. Berio (1960) separated Hypotacha from Audea,

instead placing the genus in the "Phylum of Tachosa", along with Tachosa Walker and

Metatacha Hampson, united by the feature of the male valvae possessing a large,

externally everted sac with a patch of long setae.

Catephiini

Gueneé 1852: Type genus Catephia Ochsenheimer 1816. Holloway (2005)

revised the genus Catephia, removing many superficially similar species belonging to

the genus Aedia Hübner [1823] (Noctuidae s.s.). He united this genus and Paranagia

Hampson on the basis of similarities of the male eighth abdominal segment, weakly

asymmetrical valve processes and a similar juxta in the male genitalia, and wing

patterning. Holloway (2005) found that some aspects of both male and female genitalia

show similarities to the Catocalini. In the phylogeny of Zahiri et al. (2012) the genus

Heteranassa Smith associated with Catephia although this association is weakly

supported.

37

Catocalini

Boisduval 1828: Type genus Catocala Schrank 1802. Berio (1960) recognized

similarities between Ulotrichopus Wallengren and Catocala. However, he did not include

Ulotrichopus in his "Phylum of Catocala". Berio (1960) included only Catocala and

numerous synonyms of this genus in this group. Mitter and Silverfine (1988) conducted

a formal phylogenetic analysis which united the genera Crypsotidia Rothschild,

Hypotacha, Tachosa, Audea and Ulotrichopus with Catocala, primarily based on

similarities of the female genitalia. They found that these genera feature a strongly

tapered and elongated papilla analis, which possesses a discrete dorsal band of

sclerotization and is articulated to the distinctively elongated posterior apophyses. Mitter

and Silverfine (1988) found that the genitalia of Catocala were nearly undistinguishable

from Ulotrichopus and suggested that Catocala may be paraphyletic. The study of Zahiri

et al. (2012), which united Ulotrichopus and Catocala with strong molecular support,

and suggested expanding the Catocalini to include the Audeini.

Cocytiini

Boisduval 1874: Type genus Cocytia Boisduval 1828. Until recently, Cocytia was

thought to belong to a monobasic subfamily of the Noctuidae. Speidel et al. (1997)

transferred Cocytia from the Cocytiinae to the subfamily Catocalinae, tribe Catocalini,

on the basis of tympanal and proboscis morphology, although Fibiger and Lafontaine

(2005) and Lafontaine and Fibiger (2006) maintained the Cocytiinae as a separate

subfamily. Zahiri et al. (2012) confirmed the placement of the genus within the Erebinae,

where it grouped with Serrodes Guenée and Avatha Walker, members of the "Serrodes

group of genera" of Holloway (2005). In addition to these two genera, the “Serrodes

group” includes the genus Anereuthina Hübner.

38

Ercheiini

Berio 1992: Type genus Ercheia Walker 1858. The tribe was proposed as a

name for the "Phylum of Ercheia" of Berio (1960), which he distinguished on the basis

of a large, upward facing spine on the middle of the outer surface of the male femur,

and the presence of serrated claws. Berio included the single genus Ercheia in the

group. Holloway (2005) noted that the genus Anophiodes Hampson likely belongs to

this group as well. Zahiri et al. included Ercheia in their analysis, where it associated

with the Hulodini in a large, poorly supported clade along with a number of unplaced

genera.

Erebini

Leach [1815]: Type genus Erebus Latreille 1810. Holloway (2005) included the

genera Erebus and Lygniodes Guenée, in the Erebini, which he associated the genera

on the basis of similarities of the male and female genitalia. Holloway (2005) also

remarked that the genus Metopta Swinhoe may also be associated with the tribe, on the

basis of wing patterns similar to Erebus, and larvae with a similar dorsolateral ocellus on

each side of A1. Holloway later tentatively included the genus Erygia Guenée based on

a weakly supported molecular association with Erebus (Holloway, 2011)

Euclidiini

Guenée 1852: Type genus Euclidia Ochsenheimer 1816. The earliest grouping

reflecting the current composition of the Euclidiini is the "Phylum of Mocis" (Berio,

1960). Berio united the genera Caenurgia Walker, Trigonodes Guenée, Mocis Hübner,

Remigia Guenée, Remigiodes Hampson, Celiptera Guenée, Nymbis Guenée, and

Parachalciope Hampson on the basis of the location of the androconial groove on the

trochanter and first coxa, and a distinctive femoral spine, which, when present, is

39

located at the apex of the femur. Speidel and Naumann (1995b) determined that a very

long, spiraled, ductus receptaculi with a thread-like sclerotization internally to be a

synapomorphy for the Euclidiini. Additionally, Speidel and Naumann (1995b) suggested

that similarities in the morphology of the ductus seminalis indicated a sister group

relationship between the Euclidiini and the Anumetini. They also determined that the

Melipotini and Panopodini were distinct from the Euclidiini and each other, and should

not be grouped together (1995b). Matov (2003) examined the Euclidiini and related

tribes, and characterized the tribe based on wing patterns and features of the male and

female genitalia, although he divided the current concept of the Euclidiini between the

tribes Synedini and Euclidini. Within the Euclidiini, Matov included the genera Perasia

Hübner, Ptichodis Hübner, Nymbis, Celiptera, Gonospeilia Hübner, Cuneisigna

Hampson, Plecopterodes Hampson, Trigonodes, Remigia, Mocis, Remigiodes,

Paramocis Roepke, Pelamia Guenée, Euclidia, and Leucomelas Hampson. Matov

(2003) removed the genus Remigia from synonymy with Mocis, based on features of

the male genitalia, and considered most species classified under Mocis in the western

hemisphere to belong to Remigia.

Fibiger and Lafontaine (2005) revised the status of the Euclidiini. The authors

based their concept of the tribe on the Ectypina of Fibiger (2003), to which they added

the New World genera Caenurgia Walker, Caenurgina McDunnough, Mocis Hübner,

Celiptera Guenée, Cutina Walker, Focillidia Hampson, Ptichodis Hübner, Argyrostrotis

Hübner, and Doryodes Guenée. Fibiger and Lafontaine note from Crumb (1956) that the

larvae of this group share some distinctive setal characteristics. Lafontaine and Schmidt

(2010) removed several to a newly elevated tribe, Poaphilini, on the basis of genitalia

40

morphology and molecular data, which is discussed further below. The genera

Pantydia, Euclidia, Callistege, and Mocis represented the Euclidiini in the phylogeny of

Zahiri et al. (2012), where they formed a well supported clade.

Hulodini

Guenée 1852: Type genus Hulodes Guenée 1852. Holloway (2005) tentatively

associated the genera Lacera Guenée, Speiredonia Hübner, and Ericeia Walker with

Hulodes on the basis of similarities in the male and female genitalia, and the presence

of similar maculation on the fore and hindwings. Zahri et al. (2012) included the genera

Ericeia and Hulodes in their analysis, which formed a weakly supported pair associated

with the Ercheiini. Zahiri et al. (2012) note that both genera possess "... on the

aedeagus vesica, an unusually long and tapering diverticulum, with reversed spining

extending for most of its length, and being stronger on one side."

Hypopyrini

Guenée 1852: Type genus Hypopyra Guenée 1852. Holloway (2005) included

the genera Hypopyra and Spirama Guenée, based on similarities in wing patterning and

coloration. Zahiri et al. (2012) included both genera in their analysis, which formed a

well-supported clade. This group corresponds to the “Phylum of Entomogramma”

proposed by Berio (1965), which he united on the basis of similarities in leg scaling, and

bright coloration on the ventral surface of the wings and abdomen.

Melipotini

Grote 1895: Type genus Melipotis Hübner 1818. (= Synedini Forbes 1954, =

Drasteriini Wiltshire 1976). Although the close relationships between Bulia Walker (=

Cirrhobolina, = Drasteria Hübner, = Synedoida Edwards), and Melipotis were noted at

least as early as Smith (1882b), the composition of this tribe originates with the

41

"Melipotis-Syneda Series" of Richards (1932). This included the current genera

Phoberia Hübner, Cissusa Walker, Melipotis, Bulia, Drasteria, Litocala Harvey, Panula

Guenée and Hypocala Guenée (Hypocalinae). Richards (1932) united this group on the

basis of a particularly distinctive tympanal membrane and nodular sclerite. Soon after

this treatment, Richards (1935a) described the genus Forsebia Richards within this

group of moths. In a further review of this group, Richards (1936) included the current

genera Boryza Walker and Orodesma Herrich-Schäffer and described the genus

Boryzops Richards. He removed Hypocala from the group, as the male genitalia differed

considerably from the other included genera. Richards divided the remaining genera

into five groups based on a range of morphological features. Richards also remarked

that Old World genus Anumeta Walker was related to this group of genera. Richards

(1939), again revised this group of moths, and described the genus Ianius Richards.

Forbes (1954) characterized the Synedini by reference to Group 3 of Richards (1932)

which included Hypocala. The current Melipotini corresponds to Group 1 of Crumb

(1956) which includes the current genera Drasteria, Melipotis, Phoberia, Cissusa, and

Litocala. Crumb found that the larvae of this group possess distinctively short labial

palpi, which are half or less than the length of the spinnerets. Matov (2003) examined

Palearctic members of this tribe, and characterized the Synedini based on wing

patterning and coloration, as well as features of the male and female genitalia. He

considered the Melipotini to be the tribe most closely related to the Synedini, although

his concept of the Synedini included several genera currently considered part of the

Euclidiini. Matov referred the current euclidiine genera Callistege Hübner,

Pseudocallistege Matov, Melapia Sugi, and Doryodes Guenée to the Synedini based on

42

the curved, distal portion of the sacculus, though he considered these genera to form a

group within the tribe. Within the Melipotini, Matov examined the genera Litocala,

Cissusa, and Melipotis, finding very few differences from the Synedini. He identified a

short uncus covered by very broad and stiff bristles as a synapomorphy for this group.

Matov (2003) also found that all genera examined possess a sacculus with a weakly

sclerotized distal portion, usually without a process. Additionally, Matov (2003) identified

number of characteristics shared by the Melipotini and Synedini. These included male

genitalia possessing ampullae and a flattened scaphium, as well as similarities in the

structure of the female genitalia. Although Matov maintained the separation between the

two tribes, he noted that further examination of non-Palearctic genera might reduce the

Synedini to a synonym of the Melipotini.

The current definition of the Melipotini originated with Fibiger and Lafontaine

(2005), who synonymized the Synedini with the Melipotini, but referred to the diagnosis

of the tribe (as Synedina) given by Fibiger (2003). Fibiger and Lafontaine (2005)

specifically included the North American genera from the revision of Richards (1936),

although the diagnosis of the tribe by Fibiger (2003) is based solely on Drasteria. In fact,

the genus Melipotis was explicitly excluded from the subfamily, so many of the

characters given by Fibiger (2003) may not accurately characterize the current

composition of the tribe. Zahiri et al. (2012) represented the Melipotini in their

phylogenetic analysis with the genera Bulia, Forsebia, Melipotis, and Phoberia, where

they formed a well-supported clade.

Ommatophorini

Guenée 1852: Type genus Ommatophora Guenée 1852. Holloway (2005)

distinguished the tribe based on the features of the type genus, Ommatophora. The

43

most distinctive feature of the tribe is the reniform spot on the forewing modified to

resemble an upturned snail shell (Holloway 2005). Zahiri (2012) confirmed that the tribe

belonged within the Erebinae, but its position within the family remains unsupported.

Omopterini

Gueneé 1833: Type genus Omoptera Guérin-Méneville 1832 (= Zale Hübner

1818). Zahiri et al. (2012) demonstrated that the tribe Ophiusini was restricted to the Old

World, and placed Zale within the tribe Omopterini in their analysis. Based on these

findings, Lafontaine and Schmidt (2013) assigned the name Omopterini to the Ophiusini

of their 2010 checklist, after the reassignment of Achaea Hübner, Ophisma Guenée,

and Mimophisma Hampson to the Poaphilini, which is discussed below. This leaves the

following genera in the tribe, from the checklist of Lafontaine and Schmidt (2010):

Acritogramma Franclemont, Amolita Grote, Bendisodes Hampson, Coenipeta Hübner,

Coxina Guenée, Elousa Walker, Epidromia Guenée, Eubolina Harvey, Euclystis

Hübner, Euparthenos Grote, Helia Hübner, Heteranassa, Itomia Hübner, Kakopoda

Smith, Lesmone Hübner, Matigramma Grote, Metria Hübner, Pseudanthracia Grote,

Selenisa Hayward, Toxonprucha Möschler, Tyrissa Walker, Zale, and Zaleops

Hampson. In the phylogeny of Zahiri et al. (2012), this concept of the Omopterini is

paraphyletic with respect to the Catephiini and Thermesiini, although many relationships

in this clade are not well supported.

Ophiusini

Guenée 1837: Type genus Ophiusa Ochsenheimer 1816. The "Phylum of Anua"

of Berio (1960) contains members of this tribe, which he united by the location of the

androconial groove on the femur and trochanter, and a spined femora. This group

contained members of the current genera Ophiusa, Clytie, Thyas, Hypanua Hampson,

44

and Euminucia Hampson. Holloway (2005) divided the Ophiusini into two groups

reflecting the current Ophiusini and Poaphilini, distinguishing the current Ophiusini by

the absence or reduction of coremata on the male valves, a secondary loss of the pupal

bloom, and similarities in forewing patterning. Molecular studies have changed the

composition of this tribe considerably since its treatment by Fibiger (2003). In the

phylogeny of Zahiri et al. (2012), the genera Clytie Hübner, Thyas Hübner, and Artena

Walker grouped with the two representatives of Ophiusa in a well supported clade. The

authors note that the apex of the proboscis is strongly modified in all members of this

clade, with enlarged spines and erectile hooks used for fruit piercing and lachrymal

feeding (Zahiri et al., 2012).

Pandesmini

(nomen nudum of Wiltshire 1990): Type genus Pandesma Guenée 1852.

Holloway (2005) included the Pandesma and Polydesma Boisduval on the basis of

similarities in both male and female genitalia and the larvae. He also identified several

characters of the male and female genitalia to unite the group. Lafontaine and Fibiger

(2006) listed the Pandesmini as one of the tribes of the Catocalini, but noted that the

name was not valid. Pandesma represents the tribe in the analysis of Zahiri et al.

(2012). Holloway (2005) notes that the name may serve as a replacement name for

Polydesmini Guenée 1852, which is preoccupied in by Polydesmidae (Myriapoda).

Pericymini

Wiltshire 1976: Type genus Pericyma Herrich-Schäffer 1851. Wiltshire (1976) proposed

this name for the "Phylum of Pericyma" of Berio (1960). In addition to Pericyma, Berio

included the genera Heteropalpia Berio, Cortyta Walker, Moepa Walker, Homaea

Guenée, Alamis Guenée [= Pericyma], Dugaria Walker [= Pericyma], Hansa Berio [=

45

Beriohansa Nye], Polydesma, and Lophotavia Hampson. Berio united these genera on

the basis of the following shared characteristics (Translated from Berio (1960)): "Femur

without spines, male genitalia with complex scaphium (uncus), androconial groove more

or less developed on the second tibia, with genae protruding in some genera." Wiltshire

(1970) reviewed Pericyma and related genera, and described a new genus Tytroca for a

group of Cortyta species with similar distinctive genitalia. Wiltshire (1970) associated

the genus Gnamptonyx Hampson with Pericyma, based on similarities in the genitalia,

unlike Berio, who associated the genus with Cerocala Boisduval based on similarities in

tibial spining. When Wiltshire (1976) proposed a tribal name for the group, he expanded

the definition to include Tytroca, and Gnamptonyx. Holloway (2005) distinguished the

tribe by the unusual form of the scaphium, and the distinctive, finely fasciated wings.

Fibiger (2003) associated the Pericymini with the Pandesmini due to both possessing "a

long juxta, a prominent process for the sacculus, and a ventero-lateral projection of the

vesica." Zahiri et al. (2012) found other potential relationships, with Heteropalpia,

Pandesma, Pericyma, and Sphingomorpha Guenée forming a single clade. Although

support is minimal, the authors mention that four genera feed on Acacia or its close

relatives (Zahiri et al. (2012). Zahri et al. (2012) also noted that species currently

belonging to Heteropalpia were described in the both Pandesma and Pericyma.

Additionally, Wiltshire (1976) included Polydesma in his original concept of the

Pericymini and Holloway (2005) included the Polydesma in the Pandesmini, further

illustrating the similarities between the two tribes.

Poaphilini

Guenée 1852: Type genus Poaphila Guenée 1852 [= Argyrostrotis Hübner 1821]

Lafontaine and Schmidt (2010) elevated this tribe from synonymy with the Euclidiini

46

based on morphological and molecular evidence. Lafontaine and Schmidt (2010) placed

the genera Allotria Hübner, Argyrostrotis, Cutina Walker, Focillidia Hampson,

Neadysgonia Sullivan [= Gondysia Berio], and Parallelia Hübner in the Poaphilini.

Bastilla Swinhoe, Achaea, Chalciope Hübner, and Allotria formed a well supported

clade, with Allotria representing the concept of the Poaphilini of Lafontaine and Schmidt

(2010) in the study by Zahiri et al. (2012). Based on the results of Zahiri et al. (2012),

Lafontaine and Schmidt (2013) transferred the genera Ophisma, Mimophisma, and

Achaea to the tribe, discussed previously under the Omopterini. The Parallelia complex

and related genera of Holloway and Miller (2003) closely reflects the current concept of

the Poaphilini. Holloway and Miller (2003) united these genera on the basis of

similarities in genitalia morphology and forewing patterning. The genera included in the

complex are: Parallelia, Macaldenia Moore, Pindara Moore, Dysgonia Hübner, Bastillla,

Buzara Walker, and possibly including Gondysia Berio, Euphiusa Hampson. Outside

this group Holloway and Miller included the genera Ophisma, Grammodes Guenée [=

Coenipeta Hübner], Chalciope, and Achaea. Holloway and Miller (2003) note that many

genera within this group are known to feed on the Euphorbiaceae, which is unusual

within the family (Holloway and Miller, 2003). Most taxa in this group also possess

coremata on the male valves (Holloway, 2005). This tribe corresponds in part to group II

of Forbes (1954), who united the genera Parallelia, Argyrostrotis, Allotria, and Doryodes

(Euclidiini) on the basis of genitalia morphology and larval characters. Berio (1960) also

united a number of genera belonging to the Poaphilini on the basis of distinctive, highly

evolved male genitalia, well-developed androconia on the mesotibia, and four or more

spines at the apices of the femora. The "Phylum of Achaea" contains representatives of

47

the following genera: Gondysia, Grammodes, Achaea, Dysgonia, Chalciope, Ophisma,

Parallelia, and Parallelura Berio. He united these genera

Sypnini

Holloway 2005: Type genus Sypna Guenée 1852. This tribe includes Daddala

Walker, Hypersypnoides Berio, Pterocyclophora Hampson, Sypna Guenée and

Sypnoides Hampson (Holloway 2005). The tribe is sister to all Erebinae except for

Acantholipini (Zahiri et al., 2012). The tribe was revised by Berio and Fletcher (1958),

except Pterocyclophora Hampson. The forewings of the Sypnini possess distinctive,

irregular maculation, and the margins of all wings are generally scalloped, extending

into slight tails in some genera (Holloway, 2005). The clypeofrons is unscaled, and

possess a well-developed pair of extensions between the first and second abdominal

segments (Holloway, 2005). The male genitalia are distinctive; the tegumen flexed to

project the uncus posteriorly, and the valvae often possessing a flap or flange-like

projection associated with the sacculus, aedeagus slender, saccus slender and

elongated (Holloway, 2005).

Thermesiini

Guenée 1852: Type genus Thermesia Hübner 1825 (= Hemeroblemma Hübner

1818). Includes the following genera from Lafontaine and Schmidt (2010):

Hemeroblemma, Latebraria Guenée, Thysania Dalman, Ascalapha Hübner 1821. The

authors separated these genera from the Erebini on the basis of molecular evidence

and morphological differences. It is represented by Thysania in the phylogeny of Zahiri

et al. (2012).

48

Figure 2-1. Graphical representation of Hampson's 1902 key to the subfamilies of the Noctuidae. Each node is labeled with its corresponding couplet in his key. The trifine noctuids fall under couplet ‘a’ while the quadrifine subfamilies fall under couplet ‘b’. The subfamilies are divided based on tibial spining at couplets a4 and b4. The Homopterinae under a4 possessing spined middle tibiae, while the remaining subfamilies under couplet b4 are without.

49

Figure 2-2. Redrawn ‘tree’ from Richards (1932), which was based on a morphological analysis of noctuoid tympana.

Members of the current Erebinae fall among Richards' group III-VI Erebinae, marked with an asterisk.

50

Figure 2-3. "Tree" representing the arrangement of Berio's (1960) "Phyla" (putative

monophyletic groups) within the former Catocalinae. The number of genera Berio assigned to each group is listed in parentheses behind the group name. The width of each terminal branch represents the relative generic diversity of each "phylum". With the exception of the Phylum of Arcte [Noctuidae] and the Phylum of Miniodes [Calpinae], all groups are members of the current Erebinae.

51

Figure 2-4. Cladogram representing subfamilial relationships of the Noctuoidea by

Kitching (1984). Groups containing taxa that are of the currently recognized as Erebinae are marked with an asterisk.

52

Figure 2-5. Maximum Likelihood tree showing Erebinae relationships according to

Zahiri et al. (2011). The width of each terminal branch represents the relative quantities of taxa included in each group. The number of taxa in each is listed in parentheses. Bootstrap support values above 50% are shown above branches.

53

Figure 2-6. Maximum Likelihood tree showing Erebinae relationships proposed by

Zahiri et al. (2012). The number of taxa included in the analysis for each named tribe is listed in parentheses after tribal names. Bootstrap support values are shown below branches.

54

CHAPTER 3 ANCHORED PHYLOGENOMICS RECOVERS A ROBUST PHYLOGENY OF

EREBINAE

The Noctuoidea is one of the most diverse superfamilies within the order

Lepidoptera (Zahiri et al., 2011). Within the superfamily, the most diverse family is the

Erebidae, containing over 24,000 described species and 1,760 genera (van Nieukerken

et al., 2011). The present study focuses on the phylogenetics of one of its principal

subfamilies, the Erebinae. The subfamily includes approximately 4500 species based

on the estimate for the Catocalinae given by Poole (1989). Some erebines possess

striking warning coloration, while many others are drably colored with intricate

patterning to cryptically match the surface of leaves or bark. Still, others are members

of diurnal mimicry complexes (Kitching and Rawlins, 1998). Several genera are of

economic importance, including Mocis (Kitching and Rawlins 1998), and Zale (Vazquez

et al. 2014). Erebine species are known to possess some of the most sophisticated

hearing organs (tympana) of the Lepidoptera, which are thought to have evolved as

defensive strategies against bats (Fullard, 1984). The Erebinae as currently defined is a

recently recognized grouping. The subfamily is based primarily on molecular evidence

presented the studies of Zahiri et al. (2011; 2012); there is currently no morphology-

based diagnosis for subfamily. For most of its 200-year history, classification of these

moths varied widely between authors, due to putative convergence of morphological

traits.

The taxonomic history of the Erebinae can be separated into three main

overlapping periods. The first period began with the division of Noctua Linnaeus by

Hübner (1816 [1816-1826]). In a modified version of Hübner’s classification, Gueneé

(1852a; 1852b) proposed the division between quadrifine and trifine Noctuidae, with the

55

Erebinae belonging to the former. A number of significant monographic works treating

erebine moths and other Noctuoidea used Guenée’s 1852 classification, which became

widely adopted in both Europe and North America. However, it soon became evident

that a more detailed classification was needed to for the quadrifine Noctuidae.

The second period featured the arrival of Hampson’s (1902) classification, which

split the current Erebinae into the Homopterinae [Catocalinae] and the Noctuinae

[Ophiderinae or Calpinae], largely based on the presence or absence of spines on the

mesothoracic tibia. Despite criticism that this “Hampsonian division” frequently placed

taxa that otherwise appeared closely related in different subfamilies (Richards (1932), it

was employed in several key monographs throughout the twentieth century.

The introduction of cladistic methods marked the beginning of the third period.

Berio (1960; 1965) and Wiltshire (1970; 1976) used shared characters to distinguish

putative monophyletic groups of erebine genera. Kitching (1984) published the first

formal cladistic analysis of the Noctuoidea, combining Hampson’s Catocalinae and

Calpinae into an explicitly paraphyletic Catocalinae. The applicaiton of molecular

phylogenetic methods to Noctuoidea systematics brought major changes to the

classification of erebine moths. These molecular studies led to mounting evidence for

the unification of the quadrifine Noctuidae with the then recognized Arctiidae and

Lymantriidae (Weller et al., 1992; Weller et al., 1994; Fang et al., 2000; Mitchell et al.,

2000; Mitchell et al., 2006). Based on these findings, Fibiger and Lafontaine (2005)

proposed the family name Erebidae to contain species formally in the Arctiidae,

Lymantriidae, and Noctuidae.

56

Of the erebid subfamilies, the systematics of the Erebinae remains among the

most poorly understood. The bulk of this diverse family is distributed in the tropics, and

few workers have been able to undertake systematic studies Erebinae at a global scale

(Kühne and Speidel, 2004). Zahiri et al. (2012) published the most comprehensive

phylogenetic study of the Erebinae to date, including 55 genera, and eight genes (seven

nuclear and one mitochondrial). Zahiri et al. (2012) identified 18 moderately to well-

supported tribes within the Erebinae. However, despite sampling 59 erebine species,

the backbone of their phylogeny was weakly supported, and placement and composition

of many tribes could not be satisfactorily resolved. The present study uses an anchored

hybrid enrichment (Lemmon et al. 2012) probe set of more than 600 loci for Lepidoptera

(Breinholt et al. unpublished) to construct a robust phylogeny and test prior

classifications of the Erebinae.

Methods

Taxon and Gene Sampling

We sampled 68 species of the Erebinae from 66 genera, representing all named

tribes in Zahiri et al (2012) except for the Catephiini. The dataset comprised of 92

species sampled across 90 genera, representing 23 valid family group names (Table 2-

1). No exemplar from the Catephiini could be included in the present study because a

high quality tissue sample for this taxon could not be obtained. However, four tribes not

sampled by Zahiri et al. (2012) are included in the present study: Amphigoniini, Focillini,

Hypogrammini, and Yriasini. All specimens were collected alive at light and placed

directly in 100% ethanol. Tissues are stored in 100% ethanol at -80°C at the McGuire

Center for Lepidoptera and Biodiversity, Florida Museum of Natural History, Gainesville,

57

Florida, USA. The right pair of wings for each specimen sampled was removed and

stored separately as an identification voucher.

DNA Sequencing and Alignment

DNA extractions were performed using the Qiagen DNeasy Blood and Tissue Kit

(Valencia, CA, USA) and the extracts quantified using a Qubit 2.0 Fluorometer. The first

set of quantified extracts was sent to Florida State University (Tallahassee, USA) and a

second set sent to RAPiD Genomics (Gainesville, FL, USA) for anchored hybrid

enrichment sequencing. Extracted genomic DNA were fragmented to ~250 bp inserts

using a sonicator, then sample specific barcodes and Illumina sequencing adapters

were ligated to the inserts (Lemmon et al., 2012). The barcoded inserts were pooled

and the Agilent Custom SureSelect probe kit, LEP1 (Breinholt et al. (unpublished) was

used to isolate selected loci. This probe set targets up to 855 loci, with an average

probe length of 254 bp. The enriched libraries were then sequenced on a single lane of

100 bp paired-end Illumina HiSeq 2000. Raw sequencing reads were filtered for quality,

separated to species by index, and assembled using a pipeline developed by Breinholt

et al. (in prep.). Missing data and nucleotide sites in alignments that appeared to be

randomly distributed were trimmed using ALICUT v. 2.2 (Kück, 2009).

Phylogenetic Analyses

Concatenation and coalescent-based phylogenetic approaches have inherent

biases that can affect the resulting tree (Pyron et al., 2014). To account for such bias,

we conducted phylogenetic analyses that utilized either a an approach concatenating all

genes or a species-tree analysis that accounts for the independence of each locus and

coalescence.

58

Concatenation analyses.

In a concatenation analysis, it is assumed that the overall gene history

represents the true species phylogeny (McVay and Karstens, 2013). Problems arise

with concatenation methods when gene trees differ from the species tree, due to factors

such as incomplete lineage sorting (ILS). In such cases, concatenation analyses may

produce incorrect estimates of the species tree (Bayzid and Warnow, 2013). However,

concatenation-based analyses may can be better suited to analyze anchored hybrid

enrichment data due to the difficulties posed by incomplete genes in species tree

methods, which are discussed further below.

All loci were concatenated using FASconCAT-G (Kueck and Longo, 2014), and

phylogenetic analyses were conducted in a maximum likelihood (ML) and parsimony

framework. ML analyses were conducted using both partitioned and unpartitioned

approaches. We first conducted an unpartitioned analysis in IQ-TREE v 1.3 (Nguyen et

al., 2015), employing the GTR+G model of nucleotide substitution on the concatenated

alignment. We then conducted a separate ML analysis in IQ-TREE, in which we first

partitioned the dataset using the k-means approach within PartitionFinder v 1.1 (Lanfear

et al., 2012), which selects partitions to unite sites with similar rates of evolution

(Frandsen et al., 2015). For all ML analyses that utilized IQ-TREE, we conducted 1000

rapid bootstrap searches and 100 independent tree searches with a random starting

tree.

We ran RAxML 8.0 (Stamatakis, 2014), with the ‘-J MR_DROP’, and ‘-J

STRICT_DROP’ commands to identify potential rogue taxa from 1000 bootstrap trees

generated in IQ-TREE. Rogue taxa are phylogenetically unstable taxa that can change

positions due to insufficient phylogenetic signal and reduce overall branch support,

59

leading to incorrect trees (Aberer et al. 2013). RAxML identifies rogue taxa that when

removed from the analysis, increases branch support (Pattengale et al., 2011; Aberer et

al., 2013). Rogue taxa are statistically identified in RAxML using the Relative Bipartition

Information Criterion (RBIC), then removed.

We conducted parsimony analysis on the concatenated dataset to examine the

effect of different optimality criteria on branch support and overall topology. We used the

parsimony program TNT v 1.0 (Goloboff et al., 2009) to conduct a ‘new technology

search’ with three rounds of tree fusing, two rounds of drifting, and 10 rounds of tree

ratcheting for 100 random addition replicates (xmult=rss, fuse 3, drift 2, ratchet 10,

replications 100). One hundred TNT bootstrap searches were conducted using the

following commands: xmult=rss, fuse 1, drift 5, ratchet 5, replications 5, resample boot

replications 100.

Species-tree methods

A coalescent species-tree analysis was conducted to account for independent

gene histories that are ignored by concatenation methods. For species-tree methods

that account for coalescent factors, we assume that the gene trees represent the true

evolutionary history of each gene. The validity of the assumptions can be examined by

comparing the topologies resulting from each gene-tree analysis. Due to the large

number of characters in this data set, it was necessary to use summary species tree

methods that use gene trees as input. RAxML was used to generate gene trees and

100 bootstraps for each gene, before applying ASTRAL v 4.7 (Mirarab et al., 2014) to

estimate species trees from the gene trees.

Hypothesis testing. To compare confidence between our results and prior

hypotheses for erebine classification, we conducted separate ML analyses in RAxML

60

with trees constrained to match prior hypotheses. We compared our concatenated

RAxML tree with constrained trees that were artificially created to match a proposed

topology based on molecular data (Zahiri et al. (2012), and on morphological data

(Berio (1960). We applied the Shimodaira-Hasegawa (SH) test (Shimodaira and

Hasegawa, 1999) in RAxML on the concatenated alignment and compared the best tree

unconstrained and constrained trees.

Results

Sequence Capture

Anchored hybrid enrichment captured 662 loci for a total of 158,678 sites. The

average locus length was 240 bp, and coverage completeness per locus averaged

93%. Sequence completeness is visualized in Figure 2-1, which shows pairwise overlap

of the data set per taxon.

Rogue Taxa and Maximum Likelihood

Rogue taxon analysis in RAxML did not identify any taxa exhibiting rogue

behavior, so no taxa were removed from the analysis. The ML tree from the partitioned

and unpartitioned analyses are shown in Figure 2-2 and Figure 2-3, respectively. Both

the partitioned and unpartitioned ML analyses resulted in nearly identical topologies with

strong support for the monophyly of Erebinae (BS=100), although the partitioned

analysis had averaged higher node support across all nodes. The Pandesmini and

Erebini, represented by Pandesma+Erygia and Erebus+Sphingomorpha varied in

placement between these two trees.

The Acantholipini, which is represented here by Acantholipes Lederer, Chilkasa

Swinhoe, Hamodes Guenee, Metaprosphera Hampson, Tochara Moore, and Ugia

Walker was recovered with strong support as the most basally divergent erebine tribe

61

(BS=100). The Sypnini, represented by Daddala Walker, is recovered with strong

support as the next most basal erebine lineage (BS=100). The remainder of the

Erebinae is divided into two clades. The one containing fewer taxa in this study, here

termed “Clade A”, consists of Pericymini+Omopterini/Thermesiini.

The Pericymini consists of Heteranassa Smith sister to Pericyma Herrich-

Schäffer and Heteropalpia Berio + Matigramma Grote. The Omopterini/Thermesiini

clade here consists of a large assemblage of mostly tropical New World genera, which

is further divided into two clades. One of these, here termed “Clade C” (BS=95) consists

of Mazacyla Walker +Euclystis Hübner as sister to Zale Hübner+Thermesiini. The other

principal clade, here “Clade D”, is recovered with moderate support (BS=81). At the

base is Zaleops+Toxonprucha, with Pseudyrias+Selenisa diverging from the remaining

clade. The next diverging clade contains Metria Hübner, the type genus of the Yriasiini,

paired with Cymosafia Hampson. The remaining clade contains the type genus of the

Hypogrammini, Coenipeta Hübner. It consists of the pair of Hypogrammodes

Hampson+Coenipeta, and Boryzops Richards as sister to Orodesma Herrich-

Schäffer+Pseudbarydia Hampson.

The remainder of the Erebinae is a heterogenous and global assemblage of

genera, which is here termed “Clade B”. This consists of two principal clades, “Clade E”,

and “Clade F”. Clade E consists of Catocalini, Hypopyrini, Melipotini, and Pandesmini,

while clade F contains the Cocytiini, Ercheiini, Euclidiini, Hulodini,

Ommatophorini/Amphigoniini, Ophiusini, and Poaphilini. The results of both likelihood

analyses are largely congruent, but vary in the placement of the Erebini. This tribe is

represented here by Erebus Latreille+Sphingomorpha Guenée (BS=100). The

62

unpartitioned likelihood analysis placed the Erebini as part of a polytomy within Clade E,

while the partitioned likelihood analysis placed the tribe at the base of clade F with

strong support (BS=82). The Melipotini is represented here by Bulia Walker, Melipotis

Hübner, Phoberia Hübner, and Forsebia Richards (BS=100), and pairs with the

Pandesmini (BS=99). Here, the Pandesmini is represented by Pandesma Guenée

+Erygia Guenée (BS=100). In the unpartitioned analysis, Pandesmini associated with

Catocalini+Hypopyrini but with low support, while the partitioned analysis indicated an

association with the Melipotini. In the partitioned likelihood analysis, the

Melipotini+Pandesmini formed the sister clade to the Hypopyrini+Catocalini+Audeini

(BS=100). Hypopyra Guenée and Entomogramma Guenée represent the Hypopyrini in

this study (BS=100), which pairs with the Catocalini+Audeini (BS=100). The Catocalini

is represented by Catocala and Ulotrichopus (BS=100). This tribe grouped as sister to

Audea+Hypotacha+Tachosa (BS=100). The Audeini is represented here by two species

of Audea, which pairs with Hypotacha+Tachosa (BS=100).

At the base of Clade F is a group containing mostly Southeast Asian genera and

the North American Euparthenos (BS=81). Within this clade, three well-supported

groups are recovered (BS=100): Lacera Guenée +Amphigonia, Sympis Guenée

+Oxyodes Guenée, and Platyja Hübner+Ischyja Hübner. However, the relationships

between these pairs vary between the two likelihood analyses (Figures 2-2, 2-3, 2-4, 2-

5).

While the Erebini is placed basal to the remainder of C lade F in the partitioned

likelihood analysis, both analyses recover Euclidiini as the sister group to the remaining

tribes of Clade F (BS=99). The monophyly of the tribe, which consists here of Calyptis

63

Guenée, Pantydia Guenée, Mocis Hübner, and Callistege Hübner, is strongly supported

(BS=100). The remainder of Clade F is divided between two clades; one consisting of

the Hulodini+Ercheini, and the other consisting of the Cocytiini and

Ophiusini+Poaphilini. Hulodes Guenée+Ericeia Walker represent the Hulodini in this

analysis (BS=100). Hulodini is the sister taxon to Ercheiini (BS=99), the latter which is

represented by two species of Ercheia (BS=100). The Cocytiini, represented here by

Serrodes Guénee, Avatha Walker, and Anereuthina Hübner, is placed as sister to the

Ophiusini+Poaphilini (BS=100. The monophyly of these latter tribes is strongly

supported (BS=100) in this analysis.

Parsimony Analysis

The TNT analysis found a single most parsimonious tree (Figure 2-4; score:

898593 steps), and recovered many of the same relationships as the likelihood

analyses. Bootstrap support is moderate (71%) for the monophyly of the Erebidae.

There are some differences between the relationships recovered in the parsimony

analysis and the partitioned likelihood analysis. Compared to the maximum likelihood

analyses, the positions of the Focillini and Zaleops+Toxonprucha switch relative to each

other, with the former associating with Pseudyrias+Selenisa (Parsimony, BP=85), while

Zaleops+Toxonprucha pair are only weakly associated with the Omopterini/Thermesiini

clade. Although the next higher clade of Erebinae has moderately strong support

(BS=87), relationships within the group are poorly resolved.

Coalescent-Based Methods

The best tree generated by ASTRAL achieved a quartet score of 656225167,

and a normalized quartet score of 0.4636502447982232. This tree is shown in Figure 2-

5 with nodes with BS<70 collapsed. Bootstrap support values for the relationships in this

64

tree are much lower than both the parsimony and likelihood analyses. Unlike the

likelihood analyses, the ASTRAL analysis excluded Heteranassa from the Pericymini

clade, and placed the genus at the base of the Omopterini/Thermesiini clade. Support

for the Omopterini/Thermesiini clade, including Heteranassa, is moderate (BS=70),

while support for the remainder of the clade less Heteranassa is high (BS=97). Zale was

recovered as sister to the Thermesiini, with a weak association to the Focillini.

The monophyly of the remaining erebine tribes is well supported (BS=100), but

resolution within this clade is poor with many nodes collapsed into a polytomy. The

Ommatophorini/Amphigoniini clade found in both likelihood analyses is not recovered

here, although there some pairs from that clade are recovered, including Ischyja+Platyja

(BS=71), Lacera+Amphigonia (BS=100), and Sympis+Oxyodes (BS=91). Unlike the

likelihood analyses, the ASTRAL analysis did not pair Erebus with Sphingomorpha.

Here, Sphingomorpha is weakly associated with the Melipotini, similar to the placement

of the Erebini in the unpartitioned likelihood analysis, while Erebus falls closer to the

Euclidiini, similar to the placement of the Erebini in the partitioned likelihood analysis.

Hypothesis Testing

The results of the SH tests implemented in RAxML indicate that the tree

presented by Zahiri et al. (2012) and the tree inferred from the study by Berio (1960) are

significantly less likely than the tree inferred from the unpartitioned maximum likelihood

analysis. The results of these two tests are shown in Table 2-2.

Discussion

The present study provides the most robust support for any phylogenetic study of

Erebinae to date. Nearly all nodes received BS > 85% in the partitioned ML analysis,

and there is overall congruence between all phylogenetic analyses. The greatest

65

discrepancy between the two ML analyses is the placement of the Erebini and

Pandesmini. The unpartitioned analysis placed the Erebinae in clade E, while the

partitioned ML analysis placed the tribe in clade F. Relationships also differ within the

Ommatophorini/Amphigoniini clade between the two analyses. In the unpartitioned

analysis, the Pandesmini are sister to the Hypopyrini+Catocalini, while the partitioned

analysis supports a relationship with the Melipotini. These relationships are presumably

due to the effects of the different models of nucleotide evolution, as model selection is a

crucial component of phylogenetic analyses (Frandsen et al., 2015). The unpartitioned

analysis applies a single model of nucleotide evolution to the entire dataset. On the

other hand, partitioning the dataset allows multiple models of evolution to be applied to

an alignment, to better fit the differing rates of evolution among sites.

The positions of the Focillini and Zaleops+Toxonprucha are switched in the

parsimony tree, relative to their positions in the ML analyses. The parsimony analysis

includes Heteranassa in the Omopterini/Thermesiini clade but with low support. One

possible explanaition for this variability is that parsimony does not require a model of

evolution and the approach aims to minimize the number of nucleotide steps necessary

to estimate the shortest tree. However, since no model of nucleotide evolution is input,

saturation can reduce support in parsimony analyses, particularly at deeper

phylogenetic levels. Additionally, long-branch attraction may interfere with support

values in both parsimony and ML analyses. However, groups recovered with robust

support in both the ML analyses and the parsimony analysis can be given greater

credibility due to their estimation using different optimality criteria which employ different

assumptions regarding nucleotide evolution.

66

The ASTRAL analysis did not recover the Ommatophorini+Amphigoniini clade as

monophyletic and did not pair Erebus with Sphingomorpha (as in other analyses). The

discrepancies and poor resolution in the ASTRAL analysis may be attributed to the fact

that anchored hybrid enrichment produces short gene fragments rather than complete

genes. This interferes with gene-tree analyses such as ASTRAL, which are very

sensitive to missing data and inaccurate gene trees (Mirarab et al., 2014). Additionally,

a large number of taxa/loci can cause difficulty in estimating species trees (Degnan and

Rosenberg, 2006). Further analyses emphasizing gene completeness are needed to

appropriately test the reasons behind these discrepancies.

Systematic Relationships of the Erebinae

Our results provide some of the first strong molecular evidence on the

composition of and relationships within Erebinae. These results support a number of

previously proposed hypotheses regarding the composition of erebine tribes, and their

relationships to one another. Unless otherwise noted, the partitioned ML analysis

resulted in the most robust results, so we focus our discussion on this tree. Our

discussion follows the topology shown in Figure 2-2, starting at the base of the

Erebinae.

Basal Erebinae.

At the base of the Erebinae is the well-supported Acantholipini (BP = 100),

followed by Daddala, which is the sole representative of the Sypnini in the present

study. This well-supported relationship (Acantholipini (Sypnini + remaining Erebinae; BP

= 100) is congruent with Zahiri et al. (2012), although morphological characters

supporting this grouping have not yet been recognized. The remainder of the Erebinae

is divided into two principal clades, A and B.

67

Clade A

Relationships among taxa in Clade A were well supported (all nodes except one

had BP >/= 95%). Berio (1960) included both Pericyma and Heteropalpia, along with

several other genera in his “Phylum of Pericyma”, a group united by similarities in wing

coloration and pattern, and genitalia characters. The present study places these two

genera together with strong support (BP = 100). Berio’s analysis was limited to African

genera, thus Heteranassa and Matigramma were not included. Further comparisons are

needed to determine if Heteranssa and Matigramma share further morphological

features with genera in Percymini. The four genera of Percymini included in this

analysis live in semi-arid to arid habitats, and the larvae feed on legumes.

The remainder of clade A consists of a large assemblage of polyphagous, New

World, mostly tropical genera. The concept of the Omopterini used by Lafontaine and

Schmidt (2013) is found to be paraphyletic with respect to the Thermesiini. The type

genus of the Omopterini, Zale, groups with strong support as the sister genus to the

Thermesiini (Figure 2-2).

The Thermesiini consists of large moths, and is represented in this analysis by

Ascalapha, Letis, Thysania. Lafontaine and Schmidt (2010) placed Hemeroblemma in

the Thermesiini. The name Thysaniini Grote 1895 (Type genus Thysania), should apply

to this clade if Hemeroblemma is found to belong to a separate clade. Further study of

the genera related to Zale will determine whether the Thermesiini should be maintained

as a separate Tribe from the Omopterini. Euclystis which here represents Follicini, was

previously placed in the Pangraptinae {Kühne, 2004, The system of the Catocalinae - a

historical survey (Lepidoptera`, Noctuidae)}. However, the anchored hybrid enrichment

68

results from the present study provide strong support for the placement of Euclystis in

the Erebinae.

At the base of Clade D is Zaleops+Toxonprucha, a group that is moderately well

supported as the group sister to the remaining members of this clade (BP = 75%).

Pseudyrias+Selenisa forms a well-supported sister group (BP =100) to Yriasiini +

Hypogrammini + Pandesmini. The consistent support for the pairing of the Neotropical

Pseudyrias and Selenisa suggests at least one origin of ultrasound production within the

subfamily. Preliminary results of field experiments by Kawahara et al. (unpublished),

indicate that both of these genera produce ultrasound in response to palpation.

The remainder of Clade D is represented by the Yriasiini and Hypogrammini.

Metria+Cymosafia, which here represents the Yriasiini, forms the sister clade to the

Hypogrammini. Although these moths appear distinct from the species in the

Hypogrammini, it would be necessary to assign tribal level names to both

Pseudyrias+Selenisa, and Zaleops+Toxonprucha to maintain the Yriasiini as a separate

tribe, while the Hypogrammini applies to the clade consisting of Hypogrammodes +

Coenipeta, along with Boryzops and Orodesma + Pseudbarydia. These genera are all

Neotropical with cryptic colored wings.

The Focillini, Hypogrammini, and Yriasini have hitherto not been represented in

any molecular analyses. Denser sampling at the generic level and examination of

morphological data will likely improve our understanding of relationships within this

clade. Findings of such studies will determine the validity of these assemblages and the

utility of synonymizing any of these names.

69

Clade B

Clade B is divided into two clades E and F, both which are well supported (BP =

100). Clade E included the Audeini, Catocalini, Hypopyrini, Melipotini, Pandesmini, and

Tachosini; the monophyly of each was well supported (BP >/= 99%). Mitter and

Silverfine (1988) united genera of the Audeini, Catocalini, Tachosini based on

characters of the female genitalia. The results of Zahiri et al. (2012) and the present

study provide further support for this relationship, despite considerable differences in

size, shape, and wing coloration of taxa within the group. Results of the present study

support the studies of Zahiri et al. (2012) and Mitter and Silverfine (1988), which

postulated the sister-group relationship of the Audeini + Catocalini. Zahiri et al. (2012)

suggested that the Audeini be synonymized with the Catocalinae.

Of the genera included by Berio (1965) in the “Phylum of Entomogramma”, three

have been included in molecular phylogenetic analyses to date: Entomogramma

(present study), Spirama (Zahiri et al. 2012) and both genera were sister to Hypopyra in

the respective studies, suggesting that the characters of the leg scaling and abdominal

coloration that Berio used have phylogenetic signal and may be used to define these

clades. Results of the present study provide support for the “Melipotis-Syneda” series of

Richards (1936). The molecular evidence provided in this study also supports the

monophyly of "Group 1" of Crumb (1956), which he united on the basis of larval

morphology and corresponds to the Melipotini.

Clade F includes the Ommatophorini/Amphigoniini, and contains a number of

Southeast Asian genera that are monobasic or unplaced (Hollway 2005). Holloway, in

his studies of moths from Borneo, notes morphological similarities that may indicate

relatedness between Ischyja and Platyja due to similiarities in male genitalia. This

70

pairing that is strongly supported in this study (BP = 100; Figure 2-2). However, there

are no additional records of larval and adult morphology uniting this group. One

unexpected finding of this study was the placement of the North American Euparthenos

Grote within this clade of Southeast Asian genera,. A neighbor-joining search on BOLD

indicates the east-Asian Chrysorithrum Butler is the most closely related genus to

Euparthenos, lending some evidence in support of its placement within this clade.

Holloway (2005) places a single genus Amphigonia in the tribe, but notes that

larval characters may indicate a relationship with Lacera. The results of this study

provide strong support for this pairing in all analyses, and suggest that the Amphigoniini

should be expanded to include Lacera.

Hulodes +Ericeia was recovered in the analysis of Zahiri et al. (2012), but with

low support. Holloway (2005) includes these genera, along with Speiredonia Hübner

and Lacera in his concept of the Hulodini based on similarities in genitalia morphology,

but noted that assemblage is tentative. The present molecular evidence provides strong

support for the inclusion of Lacera within this tribe. The species of the Cocytiini included

in this analysis reflect the composition of the “Serrodes Group” of (Holloway, 2005), who

united these genera on the basis of genitalia morphology, along with wing shape and

pattern.

The composition of the Ophusini and Poaphilini proposed in Zahiri et al (2012)

are supported in this analysis. The concept of the Ophiusini used by Holloway (2005)

includes the present Ophiusini and Poaphilini, although he noted that the tribe could be

divided into two groups based on features of the genitalia. These divisions reflect the

71

concepts of the Ophiusini and Poaphilini supported by this study and that of Zahiri et al.

(2012).

SH Tests

The results of the SH tests indicate that the previous molecular and

morphological hypotheses are significantly less likely than the topology found in this

analysis. Although the monophyly of many clades proposed by Berio (1960) are

supported in the current study, he did not propose any relationships between these

clades, and the composition of some of these clades are not supported in the present

study. The results of this study are also largely congruent with the topology proposed by

Zahiri et al. (2012). However, the placements of many taxa in that study were not

strongly supported, and differed from the topology presented here in several instances.

Conclusions

This study represents the most comprehensive phylogenetic study of the

Erebinae to date. Results are largely consistent with the conclusions of Zahiri et al.

(2012) – the subfamily is monophyletic and some of the historical groupings based on

morphology are retained. For instance, the most basal group in the Erebinae is the

Acantholipini, followed by the Sypnini, a result consistent with Zahiri et al. (2012).

Anchored hybrid enrichment sequencing now permits sufficient genetic sampling to

resolve the backbone and many terminal relationships within the Erebinae. I believe that

this approach will greatly facilitate future research on the phylogeny of the subfamily,

and hope to include additional taxa into the study, including many type taxa for tribes

with uncertain subfamily affinity. Combining these new molecular tools with morphology

will aid in identifying synapomorphies for this diverse subfamily of Lepidoptera.

Understanding the evolution of the remarkable aposematic coloration of many Erebinae

72

will be valuable to research on predator-prey interactions, and associated studies of

evolutionary biology and ecology. A review of host records for erebine moths has not

yet been compiled. However, such an endeavor would be very valuable, as there are

many host plant associations in the Erebinae, which would provide insight into the

evolution of specialized and economically important host preferences, such as grasses,

legumes, pines, and a wide variety of other plants.

73

Figure 3-1. Pairwise sequence completeness across all included taxa.

74

Figure 3-2. Maximum Likelihood IQ Tree, inferred from the partitioned nucleotide

alignment using the k-means algorithm. Bootstrap support values are shown at each node.

75

Figure 3-3. Maximum likelihood IQ tree from the unpartitioned nucleotide analysis.

Bootstrap support values are shown at each node.

76

Figure 3-4. Tree inferred from parsimony analysis in TNT. Bootstrap support values are

shown after each node.

77

Figure 3-5. Species tree inferred using ASTRAL from gene trees. Bootstrap values are

shown after each node. Nodes with bootstrap support less than 70 are collapsed.

78

Table 3-1. Complete specimen data, showing all taxa included in this analysis, source of genetic material (DNA,RNA) and accession number.

Family Subfamily Tribe Genus Species Data Type Acc#

Bombycidae Bombyx mori RNA -- Erebidae Erebinae Oxyodes scrobiculata DNA LEP-15780

Erebidae Erebinae Cocytiini Serrodes partita DNA NTH-14-RW082

Erebidae Erebinae Audeiini Audea nr. bipunctata DNA NTH-14-RW083 Erebidae Erebinae Audeiini Audea nr. tegulata DNA NTH-14-RW028 Erebidae Erebinae Hulodini Hulodes donata DNA LEP-12932 Noctuidae Aediinae Aedia leucomelas DNA LEP-12147 Erebidae Erebinae Focillini Mazacyla relata DNA LEP-19813 Erebidae Erebinae Thermesiini Thysania agrippina DNA LEP-19896 Erebidae Erebinae Euclidiini Mocis sp. DNA LEP-05662 Erebidae Erebinae Omopterini Toxonprucha repentis DNA LEP-13394 Erebidae Erebinae Hulodini Ericeia sp. DNA NTH-13-090605 Erebidae Erebinae Cocytiini Anereuthina renosa DNA LEP-13272 Erebidae Erebinae Amphigoniini Lacera nyarlathotepi DNA LEP-12271 Erebidae Erebinae Poaphiliini Dysgonia expediens DNA LEP-19904 Erebidae Erebinae Pandesmini Pandesma muricolor DNA NTH-13180612 Erebidae Erebinae Hypopyrini Entomogramma pardus DNA NTH-14-RW073 Erebidae Erebinae Thermesiini Ascalapha odorata DNA LEP-13791

Erebidae Erebinae Melipotini Melipotis perpendicularis DNA LEP-13462

Noctuidae Hemicephalis DNA NTH-14-FG19 Erebidae Erebinae Omopterini Zale colorado DNA LEP-13397 Erebidae Erebinae Yriasiini Cymosafia DNA NTH-14-FG167 Erebidae Erebinae Selenisa DNA FG-230 Erebidae Erebinae Focillini Euclystis insana DNA LEP-19897 Erebidae Erebinae Pericymini Pericyma mendax DNA NTH-13-090604 Erebidae Erebinae Sympis rufibasis DNA LEP-13144 Erebidae Eulepidotinae Chamyna aetheriopasta DNA LEP-05822 Erebidae Erebinae Ommotophorini Ommatophora luminosa DNA LEP-12935 Erebidae Erebinae Ischyja paraplesius DNA LEP-12861 Erebidae Erebinae Catocalini Ulotrichopus nr. Variegatus DNA NTH-13-160612 Erebidae Erebinae Pericymini Matigramma sp. DNA LEP-13889 Erebidae Erebinae Euparthenos nubilis DNA LEP-14125

79

Table 3-1. Continued Family Subfamily Tribe Genus Species Data Type Acc#

Erebidae Erebinae Hypopyrini Hypopyra sp. DNA LEP-12970

Erebidae Erebinae Poaphiliini Bastilla joviana DNA LEP-12917 Erebidae Calpinae Gonodonta sp. DNA LEP-06182 Erebidae Erebinae Acantholipini Chilkasa falcata DNA LEP-14955 Erebidae Erebinae Yriasiini Metria celia DNA LEP-19899 Erebidae Erebinae Hypogrammini Coenipeta tanais DNA NTH-14-FG20 Erebidae Erebinae Ercheiini Ercheia pulchrivena DNA LEP-16068 Erebidae Erebinae Thermesiini Letis scops DNA LEP-12638 Erebidae Erebinae Pericymini Heteranassa mima DNA LEP-15078 Erebidae Erebinae Euclidiini Calyptis idonea DNA NTH-14-FG29 Erebidae Erebinae Tachosini Tachosa nr. Fumata DNA NTH-14-RW125 Erebidae Eulepidotinae Dolichosomastis sp. DNA LEP-19902 Erebidae Ereibinae Amphigoniini Amphigonia motisigna DNA LEP-15781 Erebidae Pangraptinae Libysticta sp. DNA NTH-14-RW053 Erebidae Eulepidotinae Obroatis sp. DNA NTH-14-FG115 Erebidae Erebinae Melipotini Bulia deducta DNA LEP-14438 Erebidae Erebinae Hypogrammini Hypogrammodes balma DNA LEP-19894 Mimallonidae Cicinnus hamata RNA -- Erebidae Erebinae Platyja umminia DNA LEP-12572 Erebidae Erebinae Pericymini Heteropalpia sp. DNA NTH-14-RW102 Erebidae Erebinae Zaleops umbrina DNA LEP-13777 Erebidae Erebinae Pandesmini Erygia apicalis DNA LEP-15910 Erebidae Erebinae Ophiusini Ophiusa trapezium DNA LEP-13205 Erebidae Erebinae Poaphiliini Achaea catocaloides DNA NTH-14-RW061 Erebidae Pangraptinae Pseudogerespa usipetes DNA LEP-05653 Erebidae Erebinae Cocytiini Avatha pulcherrima DNA LEP-12474 Erebidae Eulepidotinae Eulepidotis sp. DNA LEP-05992

Erebidae Erebinae Erebini Sphingomorpha chlorea DNA NTH-14-RW115

Erebidae Erebinae Sypnini Daddala lucilla DNA LEP-12293

Erebidae Erebinae Pseudyrias sp. DNA LEP-19893 Erebidae Erebinae Tachosini Hypotacha sp. DNA NTH-14-RW121

80

Table 3-1. Continued Family Subfamily Tribe Genus Species Data Type Acc#

Erebidae Erebinae Acantholipini Ugia signifera DNA LEP-12871 Erebidae Erebinae Euclidiini Pantydia scissa DNA NTH-14-RW098 Pyralidae Stemorrhages amphitritalis RNA -- Erebidae Erebinae Hypogrammini Boryzops similis DNA NTH-14-FG06 Erebidae Lymantriinae Nygmia sp. DNA Erebidae Boletobiinae Metalectra sp. DNA LEP-13820 Erebidae Erebinae Acantholipini Tochara creberrima DNA LEP-15769 Euteliidae Stictopterinae Anigraea sp. RNA SW130103 Erebidae Erebinae Hypogrammini Pseidbarydia crespula DNA NTH-14-FG67 Erebidae Erebinae Hypogrammini Orodesma sp. DNA LEP-19895 Erebidae Eulepidotinae Ctypansa sp. DNA NTH-14-FG67 Erebidae Erebinae Acantholipini Hamodes propitia DNA LEP-06341 Erebidae Erebinae Acantholipini Metaprosphera thyriodes DNA LEP-19903 Erebidae Lymantriinae Micromorphe linta DNA LEP-15436 Erebidae Erebinae Euclidiini Callistege intercalaris DNA LEP-13681 Lasiocampidae Trabala hantu Geometridae Geometridae Geometra dieckmanni DNA LEP-13546 Erebidae Erebinae Acantholipini Metaprosphera thyriodes DNA NTH-14-FG70 Nolidae Manoba major RNA SW130224 Erebidae Ereibinae Erebini Erebus walkeri DNA NTH-13-090602 Erebidae Erebinae Acantholipini Acantholipes trimeni DNA NTH-14-RW109 Erebidae Erebinae Melipotini Forsebia cinis DNA LEP-13933 Erebidae Pangraptinae Bareia incidens DNA NTH-13-160617 Notodontidae Notoplusia minuta DNA FG12-015 Erebidae Erebinae Catocalini Catoala violenta DNA LEP-13417 Erebidae Erebinae Anisoneura salebrosa DNA LEP-12863 Erebidae Erebinae Ercheiini Ercheia cyllaria DNA LEP-12149 Erebidae Erebinae Ophiusini Artena rubida DNA LEP-14693 Noctuidae Heliothis virescens Erebidae Erebinae Melipotini Phoberia atomaris DNA GA-14-04

81

Table 3-2. Results of SH tests implemented in RAxML to test previously proposed classifications of Erebinae. D(LH) is the difference in log likelihood units between the best constrained tree and the best unconstrained tree.

Hypothesis (Constraint Tree)

Likelihood

D(LH)* Significantly Worse (P≤0.01)

Berio 1960 -3645448.934 -1132.742667 Yes Zahiri et al. 2012

-3651597.926 -7281.795895 Yes

Unconstrained Tree (Unpartitioned ML)

-3644316.191

82

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BIOGRAPHICAL SKETCH

Nicholas T. Homziak was born in Ocean Springs, Mississippi. He spent his early

childhood in Fairfax, VA (1992-94) and Managua, Nicaragua (1994-96), before settling

in Burlington, Vermont. A 2009 graduate of Burlington High School, he enrolled in the

University of New Mexico, graduating in 2013 with a BS in biology, BA in Spanish, and

economics minor. Nicholas entered the Department of Entomology and Nematology as

a MS student in the fall of 2013, where he was co-advised by Dr. Akito Kawahara and

Dr. Marc Branham.

While in Nicaragua, Nicholas developed an interest in the brightly colored tropical

butterflies. With the help of his father, he began to assemble a butterfly collection. The

move to Vermont brought a significant decrease in the Lepidoptera fauna, but also the

opportunity to study the smaller, less showy moths. His interest in these moths

continues to this day.

As an undergraduate, Nicholas worked first as a curatorial assistant and later as

an NSF-funded Undergraduate Opportunities (UnO) student. With this support, he

conducted an undergraduate honors research project on the systematics of

Heteranassa Smith, a taxonomically challenging southwestern genus of Erebinae.

Upon completion of his master’s program in August 2016, he plans to continue studying

the Erebidae as a PhD student at the University of Florida under Dr. Kawahara.