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Did dinosaurs have lice?
Vince Smith, Tom Ford, Kevin Johnson*, Paul Johnson & Rod Page University of Glasgow, Glasgow, UK *Illinois Natural History Survey, USA
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Fossil Lice 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 P s o c p t e r a M n h u / - m l x R i d L b B A D y C Wappler, Smith & Dalgleish, Proc.R.Soc., 2004.
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Approaches To Dating Test for molecular clock Compare ages
30 20 10 100 75 50 25 Bottom Up Top Down 35 ma 30 ma 30 20 10 Test for molecular clock Top down - cospeciation dates 100 75 50 25 Multiple approaches! Bottom up R8s (Sanderson, 2003) Apply rate smoothing Penalized likelihood Cross validation 100 75 50 25 Establish calibration points Crown group fossils
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18s rRNA COI (1st & 2nd pos.) ML (GTR+I+G) ML (TVM+I+G) Crustacea
Dictyoptera Hemiptera Psocoptera Lepidoptera Diptera Odonata Plecoptera Coleoptera Raphidiodea Megaloptera Neuroptera Hymenoptera Trichoptera Siphonaptera Mecoptera Diptera / Strepsiptera Thysanoptera ML (TVM+I+G) Phthiraptera Phthiraptera 0.1 0.1
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EF1-a Wingless ML (GTR+I+G) ML (GTR+I+G) Crustacea Odonata Hemiptera
Trichoptera Lepidoptera Siphonaptera Mecoptera Coleoptera Hymenoptera Diptera Hemiptera Thysanoptera Odonata Crustacea Phthiraptera Phthiraptera 0.1 0.1
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Insect Phylogeny (unsmoothed)
18s rRNA COI EF1-a Wingless Age Constraints 0.1 0.1 0.1 Ages Fixed 0.1
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Insect Phylogeny (rate smoothed)
18s rRNA COI EF1-a Wingless Odonata Hemiptera Bugs Thrips ~185 ma ~260 ma ~250 ma ~295 ma ( ma) ( ma) ( ma) ( ma) Bark Lice LICE Bugs LICE Hemiptera Thysanoptera LICE LICE Diptera Coleop. Coleoptera Beetles Hymenop. Neurop. Lepidoptera Flies Hymenop. Lepidoptera Mecop. Fleas Diptera Tric./Lep. Caddis Fleas/Mecop. Hymenoptera Lepidop. Flies Strepsip. 400 300 200 100 500 400 300 200 100 400 300 200 100 300 200 100
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Louse Phylogeny (unsmoothed)
Min. Age 44 ma Louse Fossil Primate-Louse Cospeciation Age Fixed 4.5 ma Dove-Louse Cospeciation Age Fixed 19.8 ma Rhea/Ostrich-Louse Cospeciation Age Fixed 60 ma Amblycera Ischnocera Anoplura Rhyn. Cospeciation Events Constraints Combined ML (18s, COI, EF1-a) 0.1
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Louse Phylogeny (rate smoothed)
Ricinus sp KT Laemobothrion atrum Amblycera Austromenopon elliotti Trinoton querquedulae Holomenopon sp Combined ML (18s, COI, EF1-a) Dennyus hirundinis Machaerilaemus sp Colimenopon urocolius Docophoroides brevis Fulicoffula longipila Bovicola sp Felicola subrostratus Neotrichodectes sp Geomydoecus sp Pectinopygus sulae Pectinopygus brevicornis Pectinopygus punctatus Pectinopygus varius Ischnocera Anatoecus icterodes Trichophilopterus babakotophilus Columbicola columbae Columbicola passerinae Struthioliperus nandu Struthiolipeurus struthionis Craspedorrhynchus sp Degeeriella fulva Austrophilopterus subsimilus Colilipeurus colius Campanulotes compar Result very sensitive to smoothing parameter used Goniodes sp Naubates sp Perineus nigrolimbatus Haematomyzus elephants Rhyn. Pediculus humanus var capitis Pediculus schaeffi Echinophthirius horridus b Polyplax spinulosa Haematopinus tuberculatus Anoplura Haematopinus suis ~190 ma Haematopinus pacochoeri Hoplopleura trispinosa Hoplopleura sp ( ma) Pterophthirus imitans Linognathoides marmotae Linognathoides marmotae b Neohaematopinus sciuri Neohaematopinus sciuri b 200 100
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Host Implications KT Modern birds much older - Gondwanic origin?
100 200 Paleocene Cretaceous Late Cretaceous Early Cretaceous Late Jurassic 157ma ± 146ma ± 97ma ± 65ma ± Modern Birds ‘Ratites’ and tinamous Neognathae Neornithes Archaeopteryx Paleognathae Tertiary ‘big bang’ model for modern bird evolution sensu Feduccia, 1995 Figure adapted from Feduccia, 1995 Modern birds much older - Gondwanic origin? Revised classic model sensu Cracraft, 2001 KT Modern Birds ‘Big bang’ followed by a ‘big switch’?
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Host Implications 2-300ma ? Figure adapted from ???, Science, ????
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Summary Caveats Lice are old (150-300ma)
Major radiation of lice before the KT (65ma) Modern birds & lice have a very long coevolutionary history Recent threopod dinosaurs probably had lice? Origin of lice associated with origin of feathers? Molecular clocks run fast at times of rapid radiation? Caveats
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Acknowledgements Wellcome Trust
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