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

2. …Niche Specialization
Head lice
Wing lice
Body lice

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

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

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

6. Louse Phylogeny Morphology Molecules
- 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)

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

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

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

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

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

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

13. Which hypothesis is best supported?
Molecules
Niche evolves late
(displaces within host lineages)
Character displacement
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. - phylogenetically speaking
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. Identifying co-varying characters?
Niche Constraint
Morphology
Repeat until no more
characters improve their fit
Enforce backbone constraint
Which characters fit the constraint tree better than the original?
Exclude characters with
increased RI
Heuristic search
9 cycles, 61 characters excluded
We need a better method - any suggestions?
Almost half the dataset removed!
Remaining characters very noisy

16. Is character displacement common?
Generic phylogeny of sucking lice
Genera are sister taxa!
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. Radiation of Anolis lizards on the Greater Antilles
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)
Niche / Microhabitat
Losos et al. Science

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

20. National Science Foundation
Acknowledgements
National Science Foundation