1. A timescale for the evolution of lice Vincent S. Smith with Tom Ford, Kevin Johnson, Paul Johnson, Kazunori Yoshizawa, and Jessica E. Light

2. Louse phylogeny (eight years on…) 60+ phylogenies! (circa 25 in 2003) Now cover 90% of louse genera Mix of molecules & morphology Beginning to reconcile differences Very unusual mit. & nuclear genome New questions emerging via next gen. One full genome (more coming) Amblycera Ischnocera Rhynchophthirina Anoplura [ Psocoptera ] 68 spp. (15%) 18 Genera 1427 seq. +29 seq.* 1 spp. (33%) 1 Genus 12 seq. +3 seq.* 509 spp. (17%) 95 Genera 2264 seq. +285 seq.* 134 spp. (10%) 37 Genera 326 seq. +29 seq.* 286 spp. 113 Genera 1218 seq. +478 seq.* GENBANK (June 2011) *Change since Feb. 2010 http://phylota.net/

3. Why deep branch louse phylogeny is important? Permanent obligate parasites Has ecological replicates Opportunity to identify ancestral host Tied to origin of feathers and hair Model for cospeciation studies at different scales Need to date the origin of lice

4. Psocoptera Menacanthus / Menopon -complex Ricinidae Laemobothriidae Boopiidae Austromenopon -complex Dennyus -complex Colpocephalum -complex Collected Eckfeld maar near Eifel, Germany Middle Eocene (Middle Lutetian, 44.3±0.4 Ma) First fossil louse Completes ordinal representation of fossil insects Excellent preservation Phylogenetic affinities with modern feather lice Parasite of Anseriformes or Charadriiformes Crown group position Suggests lice are very old Points to a long coevolutionary history with birds Useful molecular calibration point Wappler, Smith & Dalgleish First fossil louse Proc. R. Soc., 2004.

5. Not fossil lice! Amblyceropsis indica Kumar (2004) considered a mite by Dalgleish, Palma, Price, & Smith 2006 fused head and thorax (cephalothorax) Anopluropsis khatamaensis Kumar (2004) considered an orbatid mite by Dalgleish, Palma, Price, & Smith 2006

6. Not fossil lice! Saurodectes vrsanski Rasnitsyn & Zherikhin (1999) insect of uncertain ordinal affinities by Grimaldi and Engel 2005 & Dalgleish, Palma, Price, & Smith 2006 pterosaur louse !

7. Molecular dating i.Build a tree Character change

8. Molecular dating i.Build a tree = time

9. Molecular dating i.Build a tree ii.Test for molecular clock Now Age of lice

10. Molecular dating i.Build a tree ii.Test for molecular clock Rates of evolution vary Now Age of lice

11. Molecular dating i.Build a tree ii.Test for molecular clock iii.Apply calibrations

12. Molecular dating i.Build a tree ii.Test for molecular clock iii.Apply calibrations iv.Smooth rates across the tree -R8s with Penalized Likelihood (Sanderson, 2003) -Multidivtime (Thorne et al, 1998) Now Age of lice -BEAST (Drummond et al, 2006)

13. Louse phylogeny Amblycera Ischnocera Anoplura Rhynchophthirina 3 Genes (COI, EF1, 18s) No molecular clock Bayesian Analysis (MrBayes) - 4 chains, 10 million generations Recovers classical louse phlogeny Eight calibration points (Grimaldi & Engel 2006) 100 Ma min. Fossil Liposcelid booklouse 19.8 Ma min. Base of the Columbidae (fossil) (Benton 1993) Oldest fossil Diomedeidae- 37 - 53.25 Ma Oldest fossil Procellariform (Benton 1993) 49 Ma min. Oldest Pelicaniform fossil (Mayr 2002) 20 - 25 Ma Old World Monkeys & apes (Reed et al 2004) 5-7 Ma Chimpanzees & humans (Reed et al 2004) 4.75 - 30 Ma Last extant gopher fossil - (Russel 1968) gophers split from relatives 44 Ma min. (Wrappler et al 2004) Fossil Megamenopon louse

14. Louse phylogeny (Wappler et al 2004) 44 Myr Fossil louse, Megamenopon Fossil Louse

15. Louse phylogeny (Benton 1993) 19.8 Myr Base of the Columbidae (fossil) Dove-Louse Cospeciation

16. Louse phylogeny (Benton ed. 1993) 37 - 53 Ma Range for Diomedeidae based on fossils Albatross-Louse Cospeciation Hosts: Albatrosses Parasites: Feather Lice

17. Louse phylogeny (Reed et al 2004) 5-7 Ma Fossil & Molecular data Chimpanzee-human louse cospeciation

18. Louse phylogeny (Reed et al 2004) 20-25 Ma Fossil & Molecular data Old World Monkeys - Apes cospeciation

19. Louse phylogeny Amblycera 79 Ma (57-102 Ma) Ischnocera 98 Ma (74-125 Ma) Anoplura 74 Ma (53-98 Ma) Rhynchophthirina 0 100 Myr KT 105 161 130 Myr (Grimaldi & Engel 2006) 100 Ma min. Fossil Liposcelid booklouse 19.8 Ma min. Base of the Columbidae (fossil) (Benton 1993) Oldest fossil Diomedeidae- 37 - 53.25 Ma Oldest fossil Procellariform (Benton 1993) 49 Ma min. Oldest Pelicaniform fossil (Mayr 2002) 20 - 25 Ma Old World Monkeys & apes (Reed et al 2004) 5-7 Ma Chimpanzees & humans (Reed et al 2004) 4.75 - 30 Ma Last extant gopher fossil - (Russel 1968) gophers split from relatives 44 Ma min. (Wrappler et al 2004) Fossil Megamenopon louse

20. Lice and hosts must have a long shared history Louse phylogeny Three main clades of lice parasitizing mammals Lice are approx. 130 Ma - 161 - 105 Ma, 95% conf. intervals Major louse radiation before the KT boundary Amblycera 79 Ma (57-102 Ma) Ischnocera 98 Ma (74-125 Ma) Anoplura 74 Ma (53-98 Ma) Rhynchophthirina 0 100 Myr KT 105 161 130 Myr

21. Host implications Lice radiated on birds first Mammal lice are young These groups colonized mammals Placental Mammals Marsupials Birds What were the first louse hosts? Did lice radiate with feathers? feathers hair

22. Summary Just one fossil louse, but.. Many other calibration points Lice are approx. 130 Ma old Radiated before dinosaurs when extinct First radiated on the lineage leading to birds Either modern birds are older than we think, or… Perhaps the bird-like Theropod dinosaurs had lice? Radiated in response to the evolution of feathers?

23. Press Smith et al 2011. Multiple lineages of lice pass through the K–Pg boundary. Biology Letters doi:10.1098/rsbl.2011.0105

24. Questions?