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Convergent evolution of the genomes of marine mammals. Gregg Thomas Indiana University SMBE 2014. Convergent evolution is observed at the phenotypic level. Porcupine ( Rodentia ). Echidna ( Monotremata ). Hedgehog ( Erinaceomorpha ). Predictable Evolution.
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Convergent evolution of the genomes of marine mammals Gregg Thomas Indiana University SMBE 2014
Convergent evolution is observed at the phenotypic level Porcupine (Rodentia) Echidna (Monotremata) Hedgehog (Erinaceomorpha)
Predictable Evolution • If phenotypic convergence can be attributed to specific molecular changes, it would suggest that evolution is to some extent predictable • We have very few examples…
Phenotypic convergence can be attributed to molecular convergence Lysozyme (Kornegay et al, 1994) Foregut fermenters Prestin(Parker et al 2013, Li et al 2010, Liu et al 2010) COCH (Parker et al 2013) Echolocation
Marine mammals provide a chance to study molecular convergence
Convergent phenotypes of marine mammals • Hydrodynamic body structure with reduced neck length • Sensory adaptations • Sight in low light environments • Changes in ear structure to accommodate hearing in high pressure • Changes in respiratory and cardiac patterns depending on how long and deep the animal dives • Variations in bone density based on dive depth • Insulating blubber layer
Marine mammal genome sequencing • 16,878 orthologous protein coding genes between the four marine mammals and ten other mammals • 5,900 orthologs which are present in all 4 marine mammals and their sister land mammals (cow, dog, elephant)
Detecting molecular convergence • Ancestral reconstruction implemented in PAML v4.7 • Controlled for CpG sites • Various cutoffs for confidence in ancestral sites
Convergent substitutions X Y Y X Y X
Simulations suggest excess convergence Alpaca Cow Dolphin Killer Whale Dog Walrus 44 convergent substitutions Elephant Manatee
Adaptive convergent genes are related to convergent phenotypes
Molecular convergence has been demonstrated Phenotypic convergence can be inferred on a genome wide scale at the molecular level But another comparison can be made…
Marine mammal convergence Alpaca Cow Dolphin Killer Whale Dog Walrus Elephant Manatee
Land mammal convergence Alpaca Cow Dolphin Killer Whale Dog Walrus Elephant Manatee
Expectations for molecular convergence in land mammals • Any molecular convergence observed should be due to chance • There should be less convergence than we found for marine mammals
Convergent substitutions in land mammals Alpaca Cow Dolphin Killer Whale Dog Walrus 93 convergent substitutions Elephant Manatee
Simulations suggest excess convergence even among land mammals Alpaca Cow Dolphin Killer Whale Dog Walrus 93 convergent substitutions Elephant Manatee
Land mammals have more convergence than marine mammals Alpaca Cow Dolphin Killer Whale Dog Walrus Elephant Manatee
Positive selection comparable between marine and land mammals Marine Mammals Land Mammals
Genes can have more than one convergent site = convergent substitution
Genes with multiple convergent sites are more prevalent in land mammals
What we have learned from marine mammals • Some intriguing genes linking molecular and phenotypic convergence • Surprisingly, just as much molecular convergence among land mammals • Simulations do not fully account for background convergence
What we have learned from marine mammals • Some intriguing genes linking molecular and phenotypic convergence • Surprisingly, just as much molecular convergence among land mammals • Simulations do not fully account for background convergence
Simulations do not provide an adequate null model Manatee Elephant Walrus Dog Cow Killer Whale Dolphin Difference between observed and simulated numbers of convergent substitutions Value = (% observed - % simulated) Alpaca Rat Mouse Marmoset Baboon Macaque Human Rat Cow Dog Mouse Walrus Human Alpaca Baboon Dolphin Elephant Macaque Manatee Marmoset Killer Whale
Simulations do not provide an adequate null model Manatee Elephant Walrus Dog Cow Killer Whale Dolphin Alpaca Rat Mouse Marmoset Baboon Macaque Human Rat Cow Dog Mouse Walrus Human Alpaca Baboon Dolphin Elephant Macaque Manatee Marmoset Killer Whale
Molecular convergence of echolocation Echolocating Echolocating
Molecular convergence of echolocation Non-echolocating Echolocating Echolocating
Convergence and echolocation genes 2525 Prestin OTOF COCH
Convergence and echolocation genes Prestin OTOF COCH
Conclusions Phenotypic convergence can be attributed to molecular convergence, but this is rare Simulations do not provide an adequate null model for convergence Our results suggest that evolution is not easily predictable
Acknowledgements • Matt Hahn Collaborators: • Andy Foote • Kim Worley • Tomas Vinar Colleagues: • James Pease • Simo Zhang • Fabio Mendes • Rafael Guerrero • Melissa Toups • Jeff Adrion • Genome Assembly • Yue Liu • JixinDeng • Carson Qu • Sequencing Project Managers • Vandita Joshi • Shannon Dugan • Sequencing • Ziad Khan • Christie Kovar • Sandra Lee • Donna Muzny • RNAseq analysis • Xiang Qin • Tissue Samples for Dolphin • AnnalauraMancia • Manatee Sequencing • Kerstin Lindblad-Toh • Jessica Alföldi • Tissue samples for walrus and killer whale • Nils van Elk • Multi-genome alignment • Brian J. Raney • Bioinformatics and statistical support • Rasmus Nielsen • Nagarjun Vijay • Jochen Wolf • Principal Investigators • Richard Gibbs • Thomas Gilbert Images: P:Yellowstone Digital Slide File, E: australiazoo.com, H: instagram.com/biddythehedgehog, H: amazonwiki.org, E: asu.edu, D: jlhweb.net/BOSS/AKCstandard.html, B: John Gould from The Zoology of the Voyage of H.M.S. Beagle