Molecular evolution tracks macroevolutionary transitions in Cetacea

Trends in Ecology and Evolution

Volumn 29, Issue 6, 2014, Pages 336-346

  McGowen, Michael R ^a   Gatesy, John ^b   Wildman, Derek E ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Aquatic adaptation; Convergence; Pseudogenes; Sensory genes; Whale

Indexed keywords

CETACEAN; CONVERGENCE; EVOLUTION; GENOMICS; MOLECULAR ANALYSIS; PHYSIOLOGY; VERTEBRATE;

CETACEA; PHOCOENIDAE; VERTEBRATA;

MYOGLOBIN;

ANIMAL; CETACEA; DIVING; EVOLUTION; GENETICS; MOLECULAR EVOLUTION; PHYLOGENY; PHYSIOLOGY; SENSATION;

ANIMALS; BIOLOGICAL EVOLUTION; CETACEA; DIVING; EVOLUTION, MOLECULAR; MYOGLOBIN; PHYLOGENY; SENSATION;

EID: 84901006925     PISSN: 01695347     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tree.2014.04.001     Document Type: Review

References (88)

1. Thewissen J.G.M., Bajpai S. Whale origins as a poster child for macroevolution. Bioscience 2001, 51:1037-1049.
2. Futuyma D.J. Evolution 2009, Sinauer Associates.
3. Zimmer C., Emlen D.J. Evolution: Making Sense of Life 2013, Roberts and Co.
4. Gatesy J., O'Leary M.A. Deciphering whale origins with molecules and fossils. Trends Ecol. Evol. 2001, 16:562-571.
5. Gatesy J., et al. A phylogenetic blueprint for a modern whale. Mol. Phylogenet. Evol. 2013, 66:479-506.
6. O'Leary M.A., et al. The placental mammal ancestor and the post-K-Pg radiation of placentals. Science 2013, 339:662-667.
7. Meredith R.W., et al. Impacts of the Cretaceous terrestrial revolution and KPg extinction on mammal diversification. Science 2011, 334:521-524.
8. Zhou X., et al. Phylogenomic analyses and improved resolution of Cetartiodactyla. Mol. Phylogenet. Evol. 2011, 61:255-264.
9. Oelschläger H.A. Development of the olfactory and terminalis systems in whales and dolphins. Chemical Signals in Verterbrates VI 1992, 141-147. Plenum Press. R.L. Doty, D. Müller-Schwarze (Eds.).
10. Oelschläger H.A., Oelschläger J.S. Brain. Encyclopedia of Marine Mammals 2008, 134-149. Academic Press. 2nd edn. W.F. Perrin (Ed.).
11. Deméré T.A., et al. Morphological and molecular evidence for a stepwise evolutionary transition from teeth to baleen in mysticete whales. Syst. Biol. 2008, 57:15-37.
12. Thewissen J.G.M., et al. Developmental basis for hind-limb loss in dolphins and origin of the cetacean bodyplan. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:8414-8418.
13. Nummela S., et al. Eocene evolution of whale hearing. Nature 2004, 430:776-778.
14. Thewissen J.G.M., et al. Fossil evidence for the origin of aquatic locomotion in archaeocete whales. Science 1994, 263:210-212.
15. Thewissen J.G.M., et al. Whales originated from aquatic artiodactyls in the Eocene epoch of India. Nature 2007, 450:1190-1191.
16. Gingerich P.D., et al. Origin of whales in epicontinental remnant seas: new evidence from the Early Eocene of Pakistan. Science 1983, 220:403-406.
17. Thewissen J.G.M., et al. Skeletons of terrestrial cetaceans and the relationship of whales to artiodactyls. Nature 2001, 413:277-281.
18. Uhen M.D. The origin(s) of whales. Annu. Rev. Earth Planet. Sci. 2010, 38:189-219.
19. Gingerich P.D., et al. Origin of whales from early artiodactyls: hands and feet of Eocene Protocetidae from Pakistan. Science 2001, 293:2239-2242.
20. Fitzgerald E.M.G. A bizarre new toothed mysticete (Cetacea) from Australia and the early evolution of baleen whales. Proc. R. Soc. B 2006, 273:2955-2963.
21. Lindblad-Toh K., et al. A high-resolution map of human evolutionary constraint using 29 mammals. Nature 2011, 478:476-482.
22. Zhou X., et al. Baiji genomes reveal low genetic variability and new insights into secondary aquatic adaptations. Nat. Commun. 2013, 4:2708.
23. Yim H-S., et al. Minke whale genome and aquatic adaptation in cetaceans. Nat. Genet. 2013, 46:88-92.
24. The genome sequence of taurine cattle: a window to ruminant biology and evolution. Science 2009, 324:522-528. The Bovine Genome Sequencing and Analysis Consortium.
25. Hayden S., et al. Ecological adaptation determines functional mammalian olfactory subgenomes. Genome Res. 2010, 20:1-9.
26. Jiang P., et al. Major taste loss in carnivorous mammals. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:4956-4961.
27. Meredith R.W., et al. Molecular decay of the tooth gene enamelin (ENAM) mirrors the loss of enamel in the fossil record of placental mammals. PLoS Genet. 2009, 5:e1000634.
28. Meredith R.W., et al. Pseudogenization of the tooth gene enamelysin (MMP20) in the common ancestor of extant baleen whales. Proc. R. Soc. B 2011, 278:993-1002.
29. Davies K.T.J., et al. Parallel signatures of sequence evolution among hearing genes in echolocating mammals: an emerging model of genetic convergence. Heredity 2012, 108:480-489.
30. Meredith R.W., et al. Rod monochromacy and the coevolution of cetacean retinal opsins. PLoS Genet. 2013, 9:e1003432.
31. Mirceta S., et al. Evolution of mammalian diving capacity traced by myoglobin net surface charge. Science 2013, 340:1234192.
32. Parker J., et al. Genome-wide signatures of convergent evolution in echolocating mammals. Nature 2013, 502:228-231.
33. Berta A., et al. Marine Mammals: Evolutionary Biology 2005, Academic Press. 2nd edn.
34. Christin P.A., et al. Causes and evolutionary significance of genetic convergence. Trends Genet. 2010, 26:400-405.
35. Zakon H.H., et al. Sodium channel genes and the evolution of diversity in communication signals of electric fishes: convergent molecular evolution. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:2675-2680.
36. Hubbard J.K., et al. Vertebrate pigmentation: from underlying genes to adaptive function. Trends Genet. 2010, 26:231-239.
37. Stewart C.B., et al. Adaptive evolution in the stomach lysozymes of foregut fermenters. Nature 1987, 330:401-404.
38. Kornegay J.R., et al. Molecular adaptation of a leaf-eating bird: stomach lysozyme of the hoatzin. Mol. Biol. Evol. 1994, 11:921-928.
39. Zhang J. Parallel adaptive origins of digestive RNases in Asian and African leaf monkeys. Nat. Genet. 2006, 38:819-823.
40. Christin P.A., et al. C4 Photosynthesis evolved in grasses via parallel adaptive genetic changes. Curr. Biol. 2007, 17:1241-1247.
41. Castoe T.A., et al. Evidence for an ancient adaptive episode of convergent molecular evolution. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:8986-8991.
42. Chen C-H.C. Evolution of diverse antifreeze proteins. Curr. Opin. Genet. Dev. 1998, 8:715-720.
43. Gatesy J., et al. Extreme diversity, conservation, and convergence of spider silk fibroin sequences. Science 2001, 291:2603-2605.
44. Kooyman G.L., Ponganis P.J. The physiological basis of diving to depth: birds and mammals. Annu. Rev. Physiol. 1998, 60:19-32.
45. Tyack P.L., et al. Extreme diving of beaked whales. J. Exp. Biol. 2006, 209:4238-4253.
46. Nery M.F., et al. Accelerated evolutionary rate of the myoglobin gene in long-diving whales. J. Mol. Evol. 2013, 76:380-387.
47. Dasmeh P., et al. Positively selected sites in cetacean myoglobins contribute to protein stability. PLoS Comput. Biol. 2013, 9:e1002929.
48. Li Y., et al. The hearing gene prestin unites echolocating bats and whales. Curr. Biol. 2010, 20:R55-R56.
49. Liu Y., et al. Convergent sequence evolution between echolocating bats and dolphins. Curr. Biol. 2010, 20:R53-R54.
50. Liu Y., et al. Cetaceans on a molecular fast track to ultrasonic hearing. Curr. Biol. 2010, 20:1834-1839.
51. Shen Y.Y., et al. Parallel evolution of auditory genes for echolocation in bats and toothed whales. PLoS Genet. 2012, 8:e1002788.
52. Vater M., Kossl M. The ears of whales and bats. Echolocation in Bats and Dolphins 2004, 89-99. University of Chicago Press. J.T. Thomas (Ed.).
53. Cranford T.W., et al. Functional morphology and homology in the odontocete nasal complex: implications for sound generation. J. Morphol. 1996, 228:223-285.
54. Ketten D.R. The marine mammal ear: specializations for aquatic audition and echolocation. The Evolutionary Biology of Hearing 1992, 717-750. Springer-Verlag. D.B. Webster (Ed.).
55. Fleischer G. Hearing in extinct cetaceans as determined by cochlear structure. J. Paleontol. 1976, 50:133-152.
56. Griebel U., Peichl L. Colour vision in aquatic mammals: facts and open questions. Aquat. Mamm. 2003, 29:18-30.
57. Peichl L. Diversity of mammalian photoreceptor properties: adaptations to habitat and lifestyle?. Anat. Rec. A: Discov. Mol. Cell. Evol. Biol. 2005, 287:1001-1012.
58. Levenson D.H., Dizon A. Genetic evidence for the ancestral loss of short-wavelength-sensitive cone pigments in mysticete and odontocete cetaceans. Proc. Biol. Sci. 2003, 270:673-679.
59. Fasick J.I., Robinson P.R. Spectral-tuning mechanisms of marine mammal rhodopsins and correlations with foraging depth. Vis. Neurosci. 2000, 17:781-788.
60. Sugawara T., et al. Vertebrate rhodopsin adaptation to dim light via rapid Meta-II intermediate formation. Mol. Biol. Evol. 2010, 27:506-519.
61. Bischoff N., et al. Deep-sea and pelagic rod visual pigments identified in the mysticete whales. Vis. Neurosci. 2012, 29:95-103.
62. Nei M., et al. The evolution of animal chemosensory receptor gene repertoires: roles of chance and necessity. Nat. Rev. Genet. 2008, 9:951-963.
63. Cave A.J.E. Note on olfactory activity in mysticetes. J. Zool. 1988, 214:307-311.
64. Thewissen J.G.M., et al. Olfaction and brain size in the bowhead whale (Balaena mysticetus). Mar. Mamm. Sci. 2011, 27:282-294.
65. Rouquier S., et al. The olfactory receptor gene repertoire in primates and mouse: evidence for reduction of the functional fraction in primates. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:2870-2874.
66. Freitag J., et al. Olfactory receptors in aquatic and terrestrial vertebrates. J. Comp. Physiol. A 1998, 183:635-650.
67. Kishida T., et al. The olfactory receptor gene repertoires in secondary-adapted marine vertebrates: evidence for reduction of the functional proportions in cetaceans. Biol. Lett. 2007, 3:428-430.
68. McGowen M.R., et al. The vestigial olfactory receptor subgenome of odontocete whales: phylogenetic congruence between gene-tree reconciliation and supermatrix methods. Syst. Biol. 2008, 57:574-590.
69. Pihlström H. Comparative anatomy and physiology of chemical senses in aquatic mammals. Sensory Evolution on the Threshold: Adaptations in Secondarily Aquatic Vertebrates 2008, 95-109. University of California Press. J.G.M. Thewissen, S. Nummela (Eds.).
70. Young J.M., et al. Extreme variability among mammalian V1R gene families. Genome Res. 2010, 20:10-18.
71. Liman E.R., et al. TRP2: a candidate transduction channel for mammalian pheromone sensory signaling. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:5791-5796.
72. Yu L., et al. Characterization of TRPC2, an essential genetic component of VNS chemoreception, provides insights into the evolution of pheromonal olfaction in secondary-adapted marine mammals. Mol. Biol. Evol. 2010, 27:1467-1477.
73. Chandrashekar J., et al. The receptors and cells for mammalian taste. Nature 2006, 444:288-294.
74. Slijper E.J. Whales 1962, Basic Books.
75. Kraus P., et al. Some distal limb structures develop in mice lacking Sonic hedgehog signaling. Mech. Dev. 2001, 100:45-58.
76. Cooper L.N., et al. Evolution of hyperphalangy and digit reduction in the cetacean manus. Anat. Rec. (Hoboken) 2007, 290:654-672.
77. Wang Z., et al. Adaptive evolution of 5'HoxD genes in the origin and diversification of the cetacean flipper. Mol. Biol. Evol. 2009, 26:613-622.
78. Johnson K.R., et al. A new spontaneous mouse mutation of Hoxd13 with a polyalanine expansion and phenotype similar to human synpolydactyly. Hum. Mol. Genet. 1998, 7:1033-1038.
79. Foot N.J., et al. Positive selection in the N-terminal extramembrane domain of lung surfactant protein C (SP-C) in marine mammals. J. Mol. Evol. 2007, 65:12-22.
80. McGowen M.R., et al. Dolphin genome provides evidence for adaptive evolution of nervous system genes and a molecular rate slowdown. Proc. Biol. Sci. 2012, 279:3643-3651.
81. Nery M.F., et al. How to make a dolphin: molecular signature of positive selection in cetacean genome. PLoS ONE 2013, 8:e65491.
82. Shen Y.Y., et al. Genome-wide scan for bats and dolphin to detect their genetic basis for new locomotive styles. PLoS ONE 2012, 7:e46455.
83. Sun Y.B., et al. Genome-wide scans for candidate genes involved in the aquatic adaptation of dolphins. Genome Biol. Evol. 2013, 5:130-139.
84. Xu S.X., et al. Positive selection at the ASPM gene coincides with brain size enlargements in cetaceans. Proc. Biol. Sci. 2012, 279:4433-4440.
85. Montgomery S.H., et al. ASPM and mammalian brain evolution: a case study in the difficulty in making macroevolutionary inferences about gene-phenotype associations. Proc. R. Soc. B 2014, 281:20131743.
86. Chen Z., et al. Characterization of hairless (Hr) and FGF5 genes provides insights into the molecular basis of hair loss in cetaceans. BMC Evol. Biol. 2013, 13:34.
87. Kishida T., Thewissen J.G.M. Evolutionary changes of the importance of olfaction in cetaceans based on the olfactory marker protein gene. Gene 2012, 492:349-353.
88. McGowen M.R., et al. Phylogeny and adaptive evolution of the brain-development gene microcephalin (MCPH1) in cetaceans. BMC Evol. Biol. 2011, 11:98.