EVOLUTIONARY HISTORY OF THEFUNGAL FAMILY SERPULACEAE

A Written Report Submitted in Partial Fulfillment of the Requirements in the Subject

Biology 140 Evolutionary Biology 1st Semester A.Y. 2012-2013

Submitted by:

Casey Jon VeaRuth Joy Relador

Section T

Submitted to:

Prof. Ma. Carmina C. Manuel

October 15, 2012

EVOLUTIONARY HISTORY OF THE FUNGAL FAMILY SERPULACEAE

To understand the evolution of any taxon, it is important to comprehend the

characteristics and the evolutionary history of the higher taxon that contains it, thus before we

delve deep into the evolution of the fungal family Serpulaceae, it will be helpful to review the

general characteristics of the Kingdom Fungi first and its evolution.

The Kingdom Fungi, although not very much appreciated by many due to the annoying

diseases some of its species may cause, plays various ecological, economical, and biomedical

roles. Fungi are more like the animals that they cannot synthesize their own food. They feed by

secreting chemicals to lyse off the tissues of their substrate or host and absorbing the nutrients

made available upon lysis. Many fungi are saprotrophic, which means they obtain their nutrition

from dead organic matter. Their mode of nutrition allows the recycling of inorganic compounds

from dead organisms to the environment. Other fungal species are important parasites, which can

cause harm or benefit to their plant or animal host. Interestingly, some species are found to

parasitize other fungal species (Thanukos, 2012).

To perpetuate, fungi produce spores that give rise to haploid filaments called the hyphae.

Some exceptions may be found, such as in yeasts that are unicellular and reproduce by fission or

by budding (Thanukos, 2012). Spores may be enclosed or anchored to fruiting bodies, also

known as sporocarps, and may be released through different mechanisms depending on the

species. Some species developed a mechanism of force expulsion of spores by accumulating

pressure inside the fruiting body, i.e. the puffball fungus. On the other hand, other fungal species,

i.e. those that are truffle-like, require mechanical or biological vectors for them to disperse off

their spores. An example of a mechanical vector is the wind that scatters the spores when it

blows. Biological vectors include animals, i.e. small mammals and birds, which feed upon some

edible fungal species (Lepp, Types of fungal fruiting bodies, 2011).

Figure 1. An example of a puffball fungus (left) and a truffle-like fungus (right)

Fungi are also a very important in the biomedical field. A lot of fungi are known to cause

diseases on animals, including humans. Some of the known diseases are athlete’s foot,

ringworm, and dandruff. Fungi debilitating to plants may cause rusts, smuts and rots and may

pose significant economic harm when they infect crops and other types of plants that supply

food. On the other hand, a few fungal species are known to have antibiotic properties, i.e.

Penicillin, while, some species, such as Saccharomyces sp., are very important laboratory

specimen for genetics and molecular biology studies (Thanukos, 2012).

Another economic and ecological role of the fungi that is worth mentioning is their

ability to form a symbiotic relationship with some plant species. In this type of relationship

called mycorrhiza, the fungi are found attached on the roots of plants, especially legumes. The

plants become a source of nutrition for the fungi, while the fungi gives back to the plants by

aiding in nitrogen fixation. Aside from its ability to form partnership with plants, some fungi are

also found to associate with algal species to form lichens. Lichens are significant bio-indicators.

The abundance of lichens on trees may indicate absence or minimal pollution, while absence of

lichens imply otherwise (Thanukos, 2012).

Figure 2. A mycorrhiza (left) and a lichen (right)

The Kindom Fungi is divided into seven divisions: Microsporidia, Chytridiomycota,

Blastocladiomycota, Neocallimastigomycota, Glomeromycota, Ascomycota, and Basidiomycota.

Fungal taxa are classified under each of the divisions according to the mode of sexual

reproduction and the morphology of their sporangia or the reproductive structure that produces

the spores is also greatly considered to categorize the fungal populations (Hibbett & Hibbett,

2007).

Just as the distribution of plants and animals is a result of ecological and evolutionary

events, the distribution of fungi is also widely influenced by these factors. Just like animals and

plants, fungi have a diverse type of distribution pattern depending on their requirements to

survive and reproduce. Fungi can either be cosmopolitan, endemic or disjunct in distribution.

The distribution of a fungal taxon generally is determined by the distribution of its host or

substrate, since some fungal groups are host specific and are not capable of surviving on other

host species. However, some fungal taxa are able to adapt and transfer to another host. On the

other hand, other less demanding groups when it comes to nutritional and environmental

requirements tend to be more widespread. Conversely, cosmopolitan taxa of fungi are thought to

have evolved during the existence of the supercontinent Pangaea. Long distance spore dispersal

before the Pangaea split allowed the spread of some fungal groups during that time. An example

of an cosmopolitan fungi is Schizophyllum commune, which survive on all continents aside from

Antartica and can grow on all types of wood (Lepp, Mycogeography, 2005). One fungal group

with an interesting distribution pattern is the Family Serpulaceae, which will be discussed in

detail later.

Due to the characteristic of the fungal body, it was quite challenging to trace the

evolution of this kingdom. Although some fungi may be hard as rock, members of the kingdom

in general lack hard parts that can easily be preserved as fossils. Another challenge is that most

fungal fossils are microscopic and it is very difficult to distinguish it from other microscopic

organisms with similar filamentous or unicellular structure unless the fossil found closely

resemble extant fungal species (Thanukos, 2012). Nevertheless, with the few fossils available

and dating the oldest fungal fossil, it was found that, just like the first plant and animal groups

that existed, the first fungal populations were probably aquatic. The oldest fungal fossil had a

filamentous habit with cross walls or septae, was capable of anastomosis and was determined to

be about 1.4 billion years old. It was also theorized that the Kingdom Fungi was able to colonize

the land first before land plants and colonization of land paved way to the diversification in

modes of nutrition, i.e. saprobism, parasitism, mycorrhization and lichenization (Taylor &

Berbee, 2006).

Kingdom Fungi became abundant in the Devonian period around 416-360 million years

ago. It also became more diverse during this time when the divisions Ascomycota and

Basidiomycota (the division over the Family Serpulaceae) started to diverge around 400 million

years ago. Consequently, the Kingdom Fungi radiated and not long after a hundred of million of

years during the Late Carboniferous period (~318 to 299MYA) all the extant classes of fungi

today had already evolved (Taylor & Berbee, 2006).

When putting the evolution of the Kingdom Fungi in fast-forward and then on pause at

about the Late Cretaceous approximately 64 million years ago, Skrede and his team (2011)

reported that it is around this time, that the Family Serpulaceae diverged from Family

Tapinellineae. Family Serpulaceae is a taxon of fungi under the Order Boletales, Class

Agaricomycetes, and Division Basidiomycota. It includes three genera, Serpula, Austropaxillus

and Gymnopaxillus. Family Serpulaceae morphology varies from resupinate or flat form

(Serpula), mushroom-like (Austropaxillus), to truffle-like forms (Gymnopaxillus). Its mode of

nutrition may either be saprotrophic (Serpula) or mycorrhiza-forming (Austropaxillus and

Gymnopaxillus). Due to its diverse morphology and modes of nutrition, it is difficult to identify

one physical diagnostic feature for the taxon. Hence, phylogenetic relationship among these

genera can only be established by molecular analysis (Skrede, Engh, Binder, Carlsen, Kauserud,

& Bendiksby, 2011).

Figure 3. Serpula lacrymans, Austropaxillus infundibuliformis, Gymnopaxillus sp.

Family Serpulaceae has a disjunct distribution pattern. Species under this family can be

found in western North America, eastern North America, western Eurasia, eastern Eurasia,

southern South America, Australia, New Zealand and Old World Tropical region. The

mycogeographical history of this family can be traced from their theorized origin in temperate

North America where their main host plant genus Pinus has evolved around 155 to 87 million

years ago during the Cretaceous. The evolution of Serpulaceae followed shortly after the

establishment of genus Pinus at approximately 94 to 74 million years ago. The initial dispersal of

Serpulaceae was greatly influenced by the dispersal of the genus Pinus. Fossil evidences that

prove the presence of members of Pinaceae in the high-altitude and high-latitude regions of

North America during the early Cenozoic era can support this idea (Skrede, Engh, Binder,

Carlsen, Kauserud, & Bendiksby, 2011).

Further diffusion of the members of the Family Serpulaceae was proposed to be resulted

from long distance dispersal although exact mechanism was not pointed out. Serpulacean genus

Austropaxillus can only be found in Gondwanalan areas, i.e. South America and Australia/New

Zealand. Skrede, et.al (2011) explained that disjunct distribution of Austropaxillus might be

caused by long distance dispersal during the time where in Gondwana had not separated into

smaller continents yet from its separation from Pangaea. More recent divergence of two

Austropaxillus species (A. macnabbi in New Zealand and A. muelleri in Tazmania) has been

associated with an equally recent dispersal of Austropaxillus host genus Nothofagus and another

fungal parasite of this genus, Cyttaria (Skrede, Engh, Binder, Carlsen, Kauserud, & Bendiksby,

2011).

Figure 4. Mycogeography of the Fungal Family Serpulaceae

Mainly because of the long standing perception that fungi are more or less free from

dispersal barriers and that fungi are primarily controlled by the distribution of their host and

environment (Skrede et. al. 2011), the studies related to the distributions of fungi in an

evolutionary context is very rare and is considered relatively new.

In order to study the evolution of the family Serpulaceae the group of Skrede (2011)

gathered data of DNA sequence from 41 species under the genera Serpula, Austropaxillus and

Gymnopaxillus. Also, in order to study the phylogenetic of these extant species with other

groups of fungi, the group of Skrede gathered samples from their relative under order Boletales

and their sister group Atheliales.

So in order to generate DNA sequences, small amounts of fungal tissues were

homogenized from each of the species gathered, and using DNA sequencing methods, they

generated three separate datasets, namely Datasets 1, 2 and 3. These datasets were used to study

and analyze the Phylogenetic relationships, historical biogeography and, one of their traits, the

transitions of their mode of nutrition.

In analyzing the molecular phylogenetics of the family Serpulaceae the group of Skrede

(2011) two methods, the Maximum Parsimony (MP) and the Bayesian Inference (BI)

phylogenetics methods, were employed to Datasets 1 and 2 while Dataset 3 was only analyzed

using MP.

The Maximum Parsimony method identifies the most probable course of cladogenesis.

Which in order to do so, the method requires the investigation of the simplest explanation that is

consistent with the facts. According to Campbell and Reece (2009), the method “shaves away”

the unnecessary complications thus in the case of phylogenetic trees based on morphology it

Figure 1. Serpulaceae phylogeny

selects the parsimonious trees that requires the least evolutionary events measured by derived

morphological characters or the trees that have fewest base change if based on DNA.

Meanwhile the Bayesian Inference is used in studying phylogeny mainly because of its

advances in computational machinery. It has a number of uses in molecular phylogenetics. For

one, it can be used of the estimation of species phylogeny and species divergences times. Also,

the method generates a posterior distribution for a parameter, made from a phylogenetic tree and

a model of evolution based on the likelihood of the data. This data is generated by a multiple

alignment. In the case of the experiment done by Skrede, et. al. (2011) the data was generated by

alignment of nuclear regions of the Datasets.

Their results from the BI and MP analyses were largely congruent. Their results further

showed, as seen in Figure 1, that Serpulaceae is monophyletic with Tapinellineae as

phylogenetic sister. Both groups consist of members of brown rot species except for the

Austropaxillus clade. Furthermore, species under the Coniophoraceae also exhibit brown rot

characteristics and appear to be a monophyletic group that is separated from the

Serpulaceae/Tapinellineae clade. Moreover, as seen in the figure, the saprotrophic Serpula

himantioides and S. lacrymans appear as sister taxa in the phylogeny and together form a

monophyletic group. Austropaxillus forms a monophyletic sister to the S. lacrymans/S.

himantioides group that makes Serpula paraphyletic as currently circumscribed.

Meanwhile, the MP analysis of Dataset 3 reveals that Gymnopaxillus become

paraphyletic with the clade of Austropaxillus. Before, Serpula was considered to be a member of

Coniophoraceae, but results of Skrede and his group (2011) shows that Serpulaceae is a distant

relative of Coniophora.

Figure 2. Molecular Dating Analysis

Due to the scarcity of fungal fossils or the absence of it and the diverse morphology and

modes of nutrition, the divergence of the group is also rarely given emphasis. But several studies

have attempted to date evolutionary splits using various calibration strategies. Aside from the

sparsely of fossil records found in fungi, the documented between-lineage rate homogeneity in

fungi also complicates the reconstruction of fungal evolutionary divergence. However, many

methods have been developed to account for this factor that impedes the process.

For that reason, the group of Skrede (2011) used the computer program Bayesian

Evolutionary Analysis Sampling Trees (BEAST). This technology estimates the posterior

probability distribution of divergence times in Serpulaceae. The group used this method on

Dataset 2.

According to Figure 2 the estimated divergence times using BEAST, Serpulaceae

diverged from the Tapinellineae during late Cretaceaous and the crown-group age of

Serpulaceae believed to be at about 64 Million Years Before Present (MyBP). Moreover, even

though the direct mechanism of the evolution of the family is not directly pointed out, their

results showed that extant Serpulacea have a Late Cretaceous origin at between 94 and 74 MyBP

and was said to be at Temperate North America.

One of the identified evidence of this claim is the presence of the Gymnosperm genus

Pinus which is believed to be a substrate of the evolution of the Family Serpulaceae in the

Northern Hemisphere. According to evidences, the estimated age of the evolution of Pinus

woods during the Cretaceous, which is between 155 and 87 MyBP, corresponds well with the

timing of the evolution of Serpulaceae. Moreover, due to the presence of fossil records of the

Pinaceae in high-altitude and high-latitide lands of North America during the ealy Cenozoic

further strengthens the claim. The presence of the wood family supports the research that as the

main host of the Serpulaceae Family, it is very posible that evolution of the fungal family starts

also at that era (Skrede, Engh, Binder, Carlsen, Kauserud, & Bendiksby, 2011).

The divergence and the origin of the extant species of the family are still debatable. But

as long as researches go, there are two widely accepted hypothesis about the distribution patterns

of existing groups. They are vicariance and long distance dispersal hypothesis

As we all know, vicariance is an event that influence distribution mainly due to the

appearance of barrier that splits the range of species even though no individuals have dispersed

to new areas. This event can even account for the disjunct distribution of a species. One

evidences that supports this is the differentiation of Serpula lacrymans var. lacrymans from

Serpula lacrymans var.shastensis. Research found out that S. lacrymans differentiated into its

two varieties after it distributed from western North American to eastern Eurasia. This event is

an indicative of trans-Beringian (Beringia is somewhere in Russia) distribution and the

differentiation is due to Beringan vicariance. This claim is also supported by a comparison of a

permafrost-preserved fungal DNA from north-eastern Siberia to modern tundra macrofungi that

indicates a shift in fungal diversity following the last ice age (Lydolp et. al., 2005).

Another reason for the dispersal of the family Serpulacea, even though the mechanism is

not detailed, is believed to be the Long-distance dispersal. The members of the genus

Austropaxillus can only be found in places comprising the Gondwana like South America and

New Zealand. Skrede, et. al. (2011) further explained that the long distance dispersal happened

during the time when Gondwana is still whole and through the separation of the landmass into

smaller pieces lead to the disjunction of the genus Austropaxillus. Moreover, the divergence of

A. macnabbi from New Zealand and A. muelleri from Tazmania has been directly associated

with the dispersal also of both Austropaxillus host and parasite, the genus Nothofagus and the

genus Cyttaria respectively Cyttaria (Skrede, Engh, Binder, Carlsen, Kauserud, & Bendiksby,

2011).

Maybe one of the most important and major change through the course of evolution of

the Family Serpulaceae is their shift of mode of nutrition from saprotrophic to ectomycorrhizal.

This kind of transition in mode of nutrition is a common ecological transition (Tedersoo, et. al.,

2010). According to Skrede, et. al. (2011) this transition only happened once in Serpulacea

leading to Austropaxillus.

To sustain a aprotrophic nutrition, the environment of the fungi should be abundant with

water and mild temperature conditions but due to the change in climate towards the end of the

Eocene period, where the temperature decline and the climate gets drier, forced the transition.

Using this new type of adaptation in the new climate, the family Serpulaceae was able to

colonize barren lands and resist diseases brought by the drought. It is also reported by Skrede, et.

al. (2011) that the mychorrhizal group diverged from the saprotrophic group about 50 (66-35)

MyBP and that the radiation of the extant species happened about 22 MyBP.

The fungal family Serpulaceae comprises several saprotrophic and ectomycchorizal

species members. Its monophyletic nature gave rise to many unique and interesting features that

enable them to survive in the changing environment. One of which is the transition of some

species from aprotrophic to ectomycchorizal. With the combination of long distance dispersal

and for the southern hemisphere and the vicariance for the northern hemisphere is used to

explain the diversity and distribution of the family that enables its members to colonize vast

lands.. All in all, what is important here is that we must realize that whatever affects the plants

and animals also affects the fungi. Whatever geographic barrier that limits plant and animal

dispersal also limits the spread of fungi.

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