microhabitat specialization in parasitic lice:lineage assortment or character displacement?
Illinois Natural History SurveyUniversity of Illinois Campus
Champaign, IllinoisUSA
Vincent S. Smith & Kevin P. Johnson
The evolution of
…Niche Specialization
Body lice
Head lice
Wing lice
Niche Specialization is Common
Opisthocomiformes Passeriformes
GalliformesTinamiformes
Charadriiformes
Anseriformes
Coraciiformes
Patterns of Niche Evolution
Niche conserved Niche convergent
Wing WWWHead HHHBody BBB
CI 1.00 CI 0.33
Process of Niche Evolution - consider hosts
Niche evolves early(niche assorts with host lineages)
Niche evolves late(niche displaces within host lineages)
?
GalliformesG G G AnseriformesA A A TinamouT T T
Louse Phylogeny
MoleculesMorphology
- 41 in-group taxa (~ 1/3rd ischnoceran genera)- mammal louse (trichodectid) outgroup
- in-group span basal ischnoceran diversity- representatives from 18 bird orders
- all but 4 bird orders host lice from 2 or more niches- include 8 ‘body’, 12 ‘head’, 10 ‘wing’ & 11 ‘generalist’ genera
- focus on avian Ischnocera (Philopteridae)
Louse Phylogeny
• 4 genes (12s, COI, EF1-a, wingless)• MrBayes (partitioned by gene)• 4 chains, 5 million generations
Molecules
Posterior Prob. > 0.95
Morphology
• 138 characters• PAUP*• Parsimony, TBR
Bootstrap > 0.85
Topologies Very Different!
Principal coordinate analysis of partition metric scores( subset of these taxa but including more genes)
Combined Tree
Mol. trees2 islands
morph. trees
Niche EvolutionMorphology Molecules
RI 0.31CI 0.1421 steps
RI 0.65CI 0.2512 steps
Randomization Tests - character fitMolecules
RI 0.65
12 stepsActual tree
Sig. (P < 0.001)
Niche shuffled across molecular phylogeny(1000 Randomizations, 17-22 steps, RI 0.08-0.469)
0
50
100
150
200
250
12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27
RI 0.31
21 stepsActual tree
Not Sig. (P = 0.19)
Host shuffled across molecular phylogeny(1000 Randomizations, 29-37 steps, RI 0.00-0.409)
0
50
100
150
200
250
300
350
26 27 28 29 30 31 32 33 34 35 36 37
RI 0.65
12 stepsActual tree
Sig. (P < 0.001)
Morphology
Freq
uenc
y
Niche shuffled across morphological phylogeny(1000 Randomizations, 17-27 steps, RI 0.08-0.469)
0
50
100
150
200
250
12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27
RI 0.31
30 stepsActual tree
Sig. (P=0.011)
Host shuffled across morphological phylogeny(1000 Randomizations, 29-37 steps, RI 0.00-0.309)
0
50
100
150
200
250
300
350
29 30 31 32 33 34 35 36 37
Randomization Tests
0
100
200
300
400
500
600
700
800
0 1 2 3 4 5 6 7 8 9
(sister taxa occupying a different niche)
No. of sister taxon pairs from the same host order occupying different ecological niches
(1000 Randomized trees)
Freq
uenc
y
Same Host Order
Diff. niche
# sister taxa pairs
Randomization Tests
0
100
200
300
400
500
600
700
800
0 1 2 3 4 5 6 7 8 9
(sister taxa occupying a different niche)
No. of sister taxon pairs from the same host order occupying different ecological niches
(1000 Randomized trees)
Freq
uenc
y
Molecular Phylogeny
Highly significant (P < 0.001)
Morphological Phylogeny
Not significant (P = 1.0)
Niche Evolution - RecapMorphology Molecules
Sig.better than randomNiche Not significant
Host Sig.better than random (just) Sig.better than random
Sister taxonniche pairs
Not significant Highly significant
Niche evolves early(niche assorts with host lineages)
Niche evolves late(niche displaces within host lineages)
?Morphology supports lineage
assortment
Moleculessupports characterdisplacement
Lineage assortment or character displacement?
Which hypothesis is best supported?
Molecules
Niche evolves late(displaces within host lineages)
Character displacement
• Mol. phylogeny well supported• Especially terminal clades• Mit. + nuclear genes agree
• Mol. data blind to niche• There are only a few host niches• We would expect to see strong selection
& morphological character convergence
What use is morphology?
Can we identify morphologicalcharacters that co-vary with niche?
If so, what are they, and can we extract them to build the ‘correct’ louse phylogeny
i.e. one that is topologically more similar to the molecular tree
- phylogenetically speaking
Identifying co-varying characters?MorphologyNiche Constraint
Enforce backbone constraint
Which characters fitthe constraint tree
better than theoriginal?
Exclude characters withincreased RI
Heuristic search
Repeat until no morecharacters improve their fit
• 9 cycles, 61 characters excluded• Almost half the dataset removed!• Remaining characters very noisy
• We need a better method- any suggestions?
Is character displacement common?
• Common mammal lice
• Traditionally considered unrelated
• Morphologically very different
• Occupy different host niches
• Placed in different families
Haematomyzus elephantisHaematomyzus hopkinsiHaematomyzus porciAntarctophthirus callorhiniAntarctophthirus microchirLepidophthirus macrorhiniEchinophthirius horridusLatagophthirus rauschiProechinophthirus fluctusProechinophthirus zumptiMicrothoracius cameliNeolinognathus elephantuliLinognathus aepycerusLinognathus africanusLinognathus setosusProlinognathus aethiopicusProlinognathus ferrisiSolenopotes muntiacusRatemia squamulataAtopophthirus emersoniMicrophthirus uncinatusEnderleinellus osborniWerneckia nigeriensisPhthirunculus sumatranusAncistroplax crociduraeHoplopleura acanthopusHoplopleura irritansHoplopleura pacificaPterophthirus audaxPterophthirus splendidaParadoxophthirus emarginataSchizophthirus graphiuriSchizophthirus pleurophaeusTyphlomyophthirus bifoliatusHaematopinoides squamosusLemurphthirus galagusLemurphthirus stigmosusSathrax durusNeohaematopinus callosciuriNeohaematopinus inornatusPolyplax abyssinicaPolyplax spinulosaAbrocomaphthirus chilensisCtenophthirus cercomydisJohnsonpthirus chlorotalpaeJohnsonpthirus heliosciuriLinognathoides laeviusculusProenderleinellus calvaDocophthirus acinetusLagidiophthirus parvusEulinognathus denticulatusFahrenholzia ferrisiFahrenholzia pinnataHaemodipsus leporisHaemodipsus lyriocephalusGaleophthirus caviaePhthirpediculus brygooiScipio aulacodiScipio tripedatusHamophthirius galeopitheciPecaroecus javaliiPedicinus ferrisiPedicinus patasPediculus humanusPediculus humanus var. americanusPediculus mjobergiPediculus schaeffiPthirus gorillaePthirus pubisHaematopinus asiniHaematopinus suisHybophthirus notophallus
Generic phylogeny of sucking lice
• Genera are sister taxa!
Is character displacement common?
Haematomyzus elephantisHaematomyzus hopkinsiHaematomyzus porciAntarctophthirus callorhiniAntarctophthirus microchirLepidophthirus macrorhiniEchinophthirius horridusLatagophthirus rauschiProechinophthirus fluctusProechinophthirus zumptiMicrothoracius cameliNeolinognathus elephantuliLinognathus aepycerusLinognathus africanusLinognathus setosusProlinognathus aethiopicusProlinognathus ferrisiSolenopotes muntiacusRatemia squamulataAtopophthirus emersoniMicrophthirus uncinatusEnderleinellus osborniWerneckia nigeriensisPhthirunculus sumatranusAncistroplax crociduraeHoplopleura acanthopusHoplopleura irritansHoplopleura pacificaPterophthirus audaxPterophthirus splendidaParadoxophthirus emarginataSchizophthirus graphiuriSchizophthirus pleurophaeusTyphlomyophthirus bifoliatusHaematopinoides squamosusLemurphthirus galagusLemurphthirus stigmosusSathrax durusNeohaematopinus callosciuriNeohaematopinus inornatusPolyplax abyssinicaPolyplax spinulosaAbrocomaphthirus chilensisCtenophthirus cercomydisJohnsonpthirus chlorotalpaeJohnsonpthirus heliosciuriLinognathoides laeviusculusProenderleinellus calvaDocophthirus acinetusLagidiophthirus parvusEulinognathus denticulatusFahrenholzia ferrisiFahrenholzia pinnataHaemodipsus leporisHaemodipsus lyriocephalusGaleophthirus caviaePhthirpediculus brygooiScipio aulacodiScipio tripedatusHamophthirius galeopitheciPecaroecus javaliiPedicinus ferrisiPedicinus patasPediculus humanusPediculus humanus var. americanusPediculus mjobergiPediculus schaeffiPthirus gorillaePthirus pubisHaematopinus asiniHaematopinus suisHybophthirus notophallus
Generic phylogeny of sucking lice
Human head louse Human pubic louse
Character displacement - a general mechanism producing phenotypic diversity
Radiation of Anolis lizards on the Greater Antilles
UPGMA Morphology(clusters phenotype)
Molecular Phylogeny(phenotype transitionscommon)
Niche /Microhabitat Losos et al. Science 279. 2115-2118
Character displacement - a general mechanism producing phenotypic diversity
Fig waspsWeiblen & Bush Mol. Ecol. 11. 1573-1578
Non pollinatingFig wasp parasites
FigPlant hosts
Shared host use by waspsister taxa promotes
character displacement
Acknowledgements
National ScienceFoundation