A timescale for the evolution of lice

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. GENBANK (June 2011) 68 spp. (15%) 18 Genera 1427 seq. +29 seq.* Anoplura 1 spp. (33%) 1 Genus 12 seq. +3 seq.* Rhynchophthirina 509 spp. (17%) 95 Genera 2264 seq. +285 seq.* Ischnocera 134 spp. (10%) 37 Genera 326 seq. +29 seq.* Amblycera 286 spp. 113 Genera 1218 seq. +478 seq.* *Change since Feb. 2010 http://phylota.net/ [ “Psocoptera”] Louse phylogeny (eight years on…) • 60+ phylogenies! (circa 25 in 2003) • One full genome (more coming) • 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.

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

4. P s o c o p t e r a • 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 • 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 R i c i n i d a e L a e m o b o t h r i i d a e B o o p i i d a e D e n n y u s - c o m p l e x A u s t r o m e n o p o n - c o m p l e x M e n a c a n t h u s / M e n o p o n - c o m p l e x C o l p o c e p h a l u m - c o m p l e x First fossil louse Wappler, Smith & Dalgleish Proc. R. Soc., 2004.

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

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. Character change Molecular dating • Build a tree

8. = time Molecular dating • Build a tree

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

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

11. Molecular dating • Build a tree • Test for molecular clock • Apply calibrations

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

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

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

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

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

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

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

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

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

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

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?