microhabitat specialization in parasitic lice :

1. microhabitat specialization in parasitic lice: The evolution of lineage assortment or character displacement? Vincent S. Smith & Kevin P. Johnson Illinois Natural History Survey University of Illinois Campus Champaign, Illinois USA

2. Head lice Wing lice Body lice …Niche Specialization

3. Charadriiformes Passeriformes Opisthocomiformes Anseriformes Galliformes Tinamiformes Coraciiformes Niche Specialization is Common

4. Wing Head Body B H W B H W B H W Patterns of Niche Evolution CI 1.00 CI 0.33 Niche conserved Niche convergent

5. A G T G T G T Galliformes Tinamou A A Anseriformes ? Process of Niche Evolution - consider hosts Niche evolves early Niche evolves late (niche assorts with host lineages) (niche displaces within host lineages)

6. Molecules Morphology - focus on avian Ischnocera (Philopteridae) - mammal louse (trichodectid) outgroup - 41 in-group taxa (~ 1/3rd ischnoceran genera) - 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 Louse Phylogeny

7. Topologies Very Different! Combined Tree 2 islands morph. trees Mol. trees Principal coordinate analysis of partition metric scores ( subset of these taxa but including more genes) Posterior Prob. > 0.95 • 138 characters • 4 genes (12s, COI, EF1-a, wingless) • PAUP* • MrBayes (partitioned by gene) • Parsimony, TBR • 4 chains, 5 million generations Louse Phylogeny Morphology Molecules Bootstrap > 0.85

8. 21 steps 12 steps CI 0.14 CI 0.25 RI 0.31 RI 0.65 Niche Evolution Morphology Molecules

9. Actual tree Actual tree 250 250 21 steps 12 steps RI 0.31 RI 0.65 200 200 150 150 Sig. (P < 0.001) Not Sig. (P = 0.19) Frequency 100 100 50 50 0 0 12 12 13 13 14 14 15 15 16 16 17 17 18 18 19 19 20 20 21 21 22 22 23 24 23 25 24 26 25 27 26 27 Niche shuffled across morphological phylogeny Niche shuffled across molecular phylogeny (1000 Randomizations, 17-27 steps, RI 0.08-0.469) (1000 Randomizations, 17-22 steps, RI 0.08-0.469) Actual tree Actual tree 350 12 steps 350 30 steps 300 300 RI 0.65 RI 0.31 250 250 Sig. (P < 0.001) 200 200 Sig. (P=0.011) 150 150 100 100 50 50 0 0 29 30 31 32 33 34 35 36 37 26 27 28 29 30 31 32 33 34 35 36 37 Host shuffled across molecular phylogeny Host shuffled across morphological phylogeny (1000 Randomizations, 29-37 steps, RI 0.00-0.409) (1000 Randomizations, 29-37 steps, RI 0.00-0.309) Randomization Tests - character fit Morphology Molecules

10. Same Host Order Morphological Phylogeny Not significant (P = 1.0) Diff. niche Frequency Molecular Phylogeny # sister taxa pairs Highly significant (P < 0.001) No. of sister taxon pairs from the same host order occupying different ecological niches (1000 Randomized trees) Randomization Tests (sister taxa occupying a different niche) 800 700 600 500 400 300 200 100 0 0 1 2 3 4 5 6 7 8 9

11. Niche Sig.better than random Not significant Host Sig.better than random (just) Sig.better than random Not significant Highly significant Sister taxon niche pairs Niche Evolution - Recap Morphology Molecules

12. ? Lineage assortment or character displacement? Morphology supports lineage assortment Molecules supports character displacement Niche evolves early Niche evolves late (niche assorts with host lineages) (niche displaces within host lineages)

13. Molecules Niche evolves late (displaces within host lineages) Character displacement Which hypothesis is best supported? • Mol. phylogeny well supported • Mol. data blind to niche • Especially terminal clades • There are only a few host niches • Mit. + nuclear genes agree • We would expect to see strong selection & morphological character convergence

14. What use is morphology? - phylogenetically speaking Can we identify morphological characters 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

15. Enforce backbone constraint Which characters fit the constraint tree better than the original? Exclude characters with increased RI Heuristic search Identifying co-varying characters? Niche Constraint Morphology Repeat until no more characters improve their fit • 9 cycles, 61 characters excluded • We need a better method - any suggestions? • Almost half the dataset removed! • Remaining characters very noisy

16. Generic phylogeny of sucking lice • Genera are sister taxa! Is character displacement common? • Common mammal lice • Traditionally considered unrelated • Placed in different families • Morphologically very different • Occupy different host niches

17. Is character displacement common? Generic phylogeny of sucking lice Human head louse Human pubic louse

18. Niche / Microhabitat Character displacement -a general mechanism producing phenotypic diversity Radiation of Anolis lizards on the Greater Antilles UPGMA Morphology (clusters phenotype) Molecular Phylogeny (phenotype transitions common) Losos et al. Science 279. 2115-2118

19. Fig Plant hosts Non pollinating Fig wasp parasites Character displacement -a general mechanism producing phenotypic diversity Fig wasps Weiblen & Bush Mol. Ecol. 11. 1573-1578 Shared host use by wasp sister taxa promotes character displacement

20. National Science Foundation Acknowledgements