#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Rod Monochromacy and the Coevolution of Cetacean Retinal Opsins


Cetaceans have a long history of commitment to a fully aquatic lifestyle that extends back to the Eocene. Extant species have evolved a spectacular array of adaptations in conjunction with their deployment into a diverse array of aquatic habitats. Sensory systems are among those that have experienced radical transformations in the evolutionary history of this clade. In the case of vision, previous studies have demonstrated important changes in the genes encoding rod opsin (RH1), short-wavelength sensitive opsin 1 (SWS1), and long-wavelength sensitive opsin (LWS) in selected cetaceans, but have not examined the full complement of opsin genes across the complete range of cetacean families. Here, we report protein-coding sequences for RH1 and both color opsin genes (SWS1, LWS) from representatives of all extant cetacean families. We examine competing hypotheses pertaining to the timing of blue shifts in RH1 relative to SWS1 inactivation in the early history of Cetacea, and we test the hypothesis that some cetaceans are rod monochomats. Molecular evolutionary analyses contradict the “coastal” hypothesis, wherein SWS1 was pseudogenized in the common ancestor of Cetacea, and instead suggest that RH1 was blue-shifted in the common ancestor of Cetacea before SWS1 was independently knocked out in baleen whales (Mysticeti) and in toothed whales (Odontoceti). Further, molecular evidence implies that LWS was inactivated convergently on at least five occasions in Cetacea: (1) Balaenidae (bowhead and right whales), (2) Balaenopteroidea (rorquals plus gray whale), (3) Mesoplodon bidens (Sowerby's beaked whale), (4) Physeter macrocephalus (giant sperm whale), and (5) Kogia breviceps (pygmy sperm whale). All of these cetaceans are known to dive to depths of at least 100 m where the underwater light field is dim and dominated by blue light. The knockout of both SWS1 and LWS in multiple cetacean lineages renders these taxa rod monochromats, a condition previously unknown among mammalian species.


Vyšlo v časopise: Rod Monochromacy and the Coevolution of Cetacean Retinal Opsins. PLoS Genet 9(4): e32767. doi:10.1371/journal.pgen.1003432
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003432

Souhrn

Cetaceans have a long history of commitment to a fully aquatic lifestyle that extends back to the Eocene. Extant species have evolved a spectacular array of adaptations in conjunction with their deployment into a diverse array of aquatic habitats. Sensory systems are among those that have experienced radical transformations in the evolutionary history of this clade. In the case of vision, previous studies have demonstrated important changes in the genes encoding rod opsin (RH1), short-wavelength sensitive opsin 1 (SWS1), and long-wavelength sensitive opsin (LWS) in selected cetaceans, but have not examined the full complement of opsin genes across the complete range of cetacean families. Here, we report protein-coding sequences for RH1 and both color opsin genes (SWS1, LWS) from representatives of all extant cetacean families. We examine competing hypotheses pertaining to the timing of blue shifts in RH1 relative to SWS1 inactivation in the early history of Cetacea, and we test the hypothesis that some cetaceans are rod monochomats. Molecular evolutionary analyses contradict the “coastal” hypothesis, wherein SWS1 was pseudogenized in the common ancestor of Cetacea, and instead suggest that RH1 was blue-shifted in the common ancestor of Cetacea before SWS1 was independently knocked out in baleen whales (Mysticeti) and in toothed whales (Odontoceti). Further, molecular evidence implies that LWS was inactivated convergently on at least five occasions in Cetacea: (1) Balaenidae (bowhead and right whales), (2) Balaenopteroidea (rorquals plus gray whale), (3) Mesoplodon bidens (Sowerby's beaked whale), (4) Physeter macrocephalus (giant sperm whale), and (5) Kogia breviceps (pygmy sperm whale). All of these cetaceans are known to dive to depths of at least 100 m where the underwater light field is dim and dominated by blue light. The knockout of both SWS1 and LWS in multiple cetacean lineages renders these taxa rod monochromats, a condition previously unknown among mammalian species.


Zdroje

1. ThewissenJGM, BajpaiS (2001) Whale origins as a poster child for macroevolution. BioScience 51: 1037–1049.

2. ThewissenJGM, CooperLN, GeorgeJC, BajpaiS (2009) From land to water: the origin of whales, dolphins, and porpoises. Evo Edu Outreach 2: 272–288.

3. UhenMD (2010) The origin(s) of whales. Annu Rev Earth Planet Sci 38: 189–219.

4. GatesyJ, GeislerJH, ChangJ, BuellC, BertaA, et al. (2013) A phylogenetic blueprint for a modern whale. Mol Phylogenet Evol 66: 479–506.

5. LiY, LiuZ, ShiP, ZhangJ (2010) The hearing gene Prestin unites echolocating bats and whales. Curr Biol 20: R55–R56.

6. LiuY, RossiterS, HanX, CottonJ, ZhangS (2010) Cetaceans on a molecular fast track to ultrasonic hearing. Curr Biol 20: 1834–1839.

7. DaviesKTJ, CottonJA, KirwanJD, TeelingEC, RossiterSJ (2012) Parallel signatures of sequence evolution among hearing genes in echolocating mammals: an emerging model of genetic convergence. Heredity 108: 480–489.

8. McGowenMR, MontgomerySH, ClarkC, GatesyJ (2011) Phylogeny and adaptive evolution of the brain-development gene microcephalin (MCPH1) in cetaceans. BMC Evol Biol 11: 98.

9. XuS, ChenY, ChengY, YangD, ZhouX, et al. (2012) Positive selection at the ASPM gene coincides with brain size enlargements in cetaceans. Proc R Soc B 279: 4433–4440.

10. WangZ, YuanL, RossiterSJ, ZuoX, RuB, et al. (2009) Adaptive evolution of 5′HoxD genes in the origin and diversification of the cetacean flipper. Mol Biol Evol 26: 613–622.

11. KishidaT, KubotaS, ShirayamaY, FukamiH (2007) The olfactory receptor gene repertoires in secondary-adapted marine vertebrates: evidence for reduction of the functional proportions in cetaceans. Biol Lett 3: 428–430.

12. McGowenMR, ClarkC, GatesyJ (2008) The vestigial olfactory receptor subgenome of odontocete whales: phylogenetic congruence between gene-tree reconciliation and supermatrix methods. Syst Biol 57: 574–590.

13. HaydenS, BekaertM, CriderTA, MarianiS, MurphyWJ, et al. (2010) Ecological adaptation determines functional mammalian olfactory subgenomes. Genome Res 20: 1–9.

14. JiangP, JosueJ, LiX, GlaserD, LiW, et al. (2012) Major taste loss in carnivorous mammals. Proc Natl Acad Sci USA 109: 4956–4961.

15. DeméréTA, McGowenMR, BertaA, GatesyJ (2008) Morphological and molecular evidence for a stepwise evolutionary transition from teeth to baleen in mysticete whales. Syst Biol 57: 15–37.

16. MeredithRW, GatesyJ, MurphyWJ, RyderOA, SpringerMS (2009) Molecular decay of the tooth gene enamelin (ENAM) mirrors the loss of enamel in the fossil record of placental mammals. PLoS Genet 5: e1000634 doi:10.1371/journal.pgen.1000634.

17. MeredithRW, GatesJ, ChengJ, SpringerMS (2011) Pseudogenization of the tooth gene enamelysin (MMP20) in the common ancestor of extant baleen whales. Proc Roy Soc Lond B 278: 993–1002.

18. YuL, JinW, WangJ, ZhangX, ChenM, et al. (2010) 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 27: 1467–1477.

19. GriebelU, PeichlL (2003) Colour vision in aquatic mammals - facts and open questions. Aquat Mamm 29: 18–30.

20. McFarlandWN (1971) Cetacean visual pigments. Vision Res 11: 1065–1076.

21. FasickJI, BischoffN, BrennanS, VelasquezS, AndradeG (2011) Estimated absorbance spectra of the visual pigments of the North Atlantic right whale (Eubalaena glacialis). Mar Mamm Sci 27: E321–E331.

22. DaviesWIL, CollinSP, HuntDM (2012) Molecular ecology and adaptation of visual photopigments in craniates. Mol Ecol 21: 3121–3158.

23. LevensonDH, DizonA (2003) Genetic evidence for the ancestral loss of SWS cone pigments in mysticete and odontocete cetaceans. Proc Roy Soc London B 270: 673–679.

24. PeichlL (2005) Diversity of mammalian photoreceptor properties: adaptations to habitat and lifestyle. Anat Rec 287A: 1001–1012.

25. BischoffN, NickleB, CroninTW, VelasquezS, FasickJI (2012) Deep-sea and pelagic rod visual pigments identified in the mysticete whales. Vis Neurosci 29: 95–103.

26. PeichlL, BehrmannG, KrogerRHH (2001) For whales and seals the ocean is not blue: A visual pigment loss in marine mammals. Eur J Neurosci 13: 1520–1528.

27. NewmanLA, RobinsonPR (2005) Cone visual pigments of aquatic mammals. Vis Neurosci 22: 873–879.

28. ZhaoH, RuB, TeelingEC, FaulkesCG, ZhangS, et al. (2009) Rhodopsin molecular evolution in mammals inhabiting low light environments. PLoS ONE 4: e8326 doi:10.1371/journal.pone.0008326.

29. GeislerJH, TheodorJM (2009) Hippopotamus and whale phylogeny. Nature 458: E1–E4.

30. SpauldingM, O'LearyMA, GatesyJ (2009) Relationships of Cetacea (Artiodactyla) among mammals: increased taxon sampling alters interpretations of key fossils and character evolution. PLoS ONE 4: e7062 doi:10.1371/journal.pone.0007062.

31. GatesyJ, HayashiC, CroninA, ArctanderP (1996) Evidence from milk casein genes that cetaceans are close relatives of hippopotamid artiodactyls. Mol Biol Evol 13: 954–963.

32. GatesyJ (1997) More DNA support for a Cetacea/Hippopotamidae clade: the blood-clotting protein gene gamma-fibrinogen. Mol Biol Evol 14: 537–543.

33. GingerichPD, HaqMU, ZalmoutIS, KhanIH, MalakaniMS (2001) Origin of whales from early artiodactyls: hands and feet of Eocene Protocetidae from Pakistan. Science 293: 2239–2242.

34. ThewissenJGM, WilliamsEM, RoeLJ, HussaiST (2001) Skeletons of terrestrial cetaceans and the relationship of whales to artiodactyls. Nature 413: 277–281.

35. ThewissenJGM, CooperLN, ClementzMT, BajpaiS, TiwariBN (2007) Whales originated from aquatic artiodactyls in the Eocene epoch of India. Nature 450: 1190–1194.

36. YokoyamaS (2008) Evolution of dim-light and color vision pigments. Annu Rev Genomics Hum Genet 9: 259–282.

37. GeislerJH, McGowenRM, YangG, GatesyJ (2011) A supermatrix analysis of genomic, morphological, and paleontological data from crown Cetacea. BMC Evol Biol 11: 112.

38. Reuter T, Peichl L (2008) Structure and function of the retina in aquatic tetrapods. In: Thewissen JGM, Nummela S, eds. Sensory evolution on the threshold: adaptations in secondarily aquatic vertebrates. Berkeley and Los Angeles, California: Univ California Press. pp 149–174.

39. BloodworthBE, OdellDK (2008) Kogia breviceps (Cetacea: Kogiidae). Mamm Species 819: 1–12.

40. FordyceRE (1994) Waipatia maerewhenua, new genus and new species (Waipatiidae, new family), an archaic late Oligocene dolphin (Cetacea: Odontoceti: Platanistoidea) from New Zealand. Proc San Diego Soc Nat Hist 29: 147–176.

41. GeislerJH, SandersAE (2003) Morphological evidence for the phylogeny of Cetacea. J Mammal Evol 10: 23–129.

42. McGowenMR, SpauldingM, GatesyJ (2009) Divergence date estimation and a comprehensive molecular tree of extant cetaceans. Mol Phylogenet Evol 53: 891–906.

43. SteemanME, HebsgaardMB, FordyceRE, HoSYW, RaboskyDL, et al. (2009) Radiation of extant cetaceans driven by restructuring of the oceans. Syst Biol 58: 573–585.

44. NozawaM, SuzukiY, NeiM (2009) Reliabilities of identifying positive selection by the branch-site and the site-prediction methods. Proc Natl Acad Sci USA 106: 6700–6705.

45. YangZ (2007) PAML 4: a program package for phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: 1586–1591.

46. YangZ, WongWSW, NielsenR (2005) Bayes empirical Bayes inference of amino acid sites under positive selection. Mol Biol Evol 22: 1107–1118.

47. ZhangJ, NielsenR, YangZ (2005) Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol Biol Evol 22: 2472–2479.

48. YangZ, NielsenR, GoldmanN (2009) In defense of statistical methods for detecting positive selection. Proc Natl Acad Sci USA 106: E95.

49. SugawaraT, ImaiH, NikaidoM, ImamotoY, OkadaN (2010) Vertebrate rhodopsin adaptation to dim light via rapid meta-II intermediate formation. Mol Biol Evol 27: 506–519.

50. RaderAJ, AndersonG, IsinB, KhoranaHG, BaharI, et al. (2004) Identification of core amino acids stabilizing rhodopsin. Proc Natl Acad Sci USA 101: 7246–7251.

51. GetherU, LinS, GhanouniP, BallesterosJA, WeinsteinH, et al. (1997) Agonists induce conformational changes in transmembrane domains III an VI of the β2 adrenoceptor. EMBO J 16: 6737–6747.

52. Walls GL (1942) The vertebrate eye and its adaptive radiation. Bloomfield Hills, Michigan: Cranbrook Institute of Science.

53. WoollardHH (1927) The differentiation of the retina in the primates. Proc Zool Soc Lond 97: 1–18.

54. WoollardHH, BeattieJ (1927) The comparative anatomy of the lateral geniculate body. J Anat 61: 414–423.

55. DetwilerSR (1941a) The eye of the owl monkey (Nyctipithecus). Anat Rec 80: 233–241.

56. DetwilerSR (1941b) Some biological aspects of vision. Sigma Xi Quart 29: 112–129.

57. DetwilerSR (1956) The eye and its structural adaptations. Am Sci 44: 45–72.

58. NagaoK, TakenakaN, HiraiM, KawamuraS (2005) Coupling and decoupling of evolutionary mode between X- and Y-Chromosomal red-green opsin genes in owl monkeys. Gene 352: 32–91.

59. TanY, YoderAD, YamashitaN, LiW-H (2005) Evidence from opsin genes rejects nocturnality in ancestral primates. Proc Natl Acad Sci USA 102: 14712–14716.

60. MüllerB, GoodmanSM, PeichlL (2007) Cone photoreceptor diversity in the retinas of fruit bats (Megachiroptera). Brain Behav Evol 70: 90–104.

61. BowmakerJK (2008) Evolution of vertebrate visual pigments. Vision Res 48: 2022–2041.

62. KimEB, FangX, FushanAA, HuangZ, LobanovAB, et al. (2011) Genome sequencing reveals insights into physiology and longevity of the naked mole rat. Nature 479: 223–227.

63. JacobsGH, DeeganDFII (1992) Cone photopigments in nocturnal and diurnal procyonids. J Comp Physiol A 171: 351–358.

64. JacobsGH, DeeganDFII, NeitzJ, CrognaleMA, NeitzM (1993) Photopigments and color vision in the nocturnal monkey, Aotus. Vision Res 33: 1773–1783.

65. JacobsGH, NeitzM, NeitzJ (1996) Mutations in S-cone pigment genes and the absence of colour vision in two species of nocturnal primate. Proc Royal Soc London B 263: 705–710.

66. DeeganDFII, JacobsGH (1996) Spectral sensitivity and photopigments of a nocturnal prosimian, the bushbaby (Otolemur crassicaudatus). Am J Primatol 40: 55–66.

67. PeichlL, MoutairouK (1998) Absence of short-wavelength sensitive cones in the retinae of seals (Carnivora) and African giant rats (Rodentia). Eur J Neurosci 10: 2586–2594.

68. CrognaleMA, LevensonDH, PonganisPJ, DeeganJF, JacobsGH (1998) Cone spectral sensitivity in the harbor seal (Phoca vitulina) and implications for color vision. Can J Zool 76: 2114–2118.

69. KawamuraS, KuboteraN (2004) Ancestral loss of short wave-sensitive cone visual pigment in Lorisiform prosimians, contrasting with its strict conservation in other prosimians. J Mol Evol 58: 314–321.

70. CarvalhoLPS, CowinJA, WilkieSE, BowmakerJK, HuntDM (2006) Shortwave visual sensitivity in tree and flying squirrels reflects changes in life style. Curr Biol 16: R81–R83.

71. JacobsGH (2009) Evolution of colour vision in mammals. Phil Trans R Soc B 364: 2957–2967.

72. GriebelU, SchmidA (2002) Spectral sensitivity and color vision in the bottlenose dolphin (Tursiops truncatus). Mar Fresh Behav Physiol 35: 129–137.

73. PartridgeJC, ShandJ, ArcherSN, LythgoeJN, van Groningen-LuybenWAHM (1989) Interspecific variation in the visual pigments of deep-sea fishes. J Comp Physiol A 164: 513–529.

74. RippsH, DowlingJE (1991) Structural features and adaptive properties of photoreceptors in the skate retina. J Exp Zool Suppl 5: 46–54.

75. DouglasRH, PartridgeJC, HopeAJ (1995) Visual and lenticular pigments in the eyes of demersal deep-sea fishes. J Comp Physiol A 177: 111–122.

76. O'BrienJ, RippsH, Al-UbaidiMR (1997) Molecular cloning of a rod opsin cDNA from the skate retina. Gene 193: 141–150.

77. BozzanoA, MurgiaR, Vallerga, HiranoJ, ArcherS (2001) The photoreceptor system in the retinae of two dogfishes, Scyliorhinus canicula and Galeus melastomus: possible relationship with depth distribution and predatory lifestyle. J Fish Biol 59: 1258–1278.

78. BozzanoA (2004) Retinal specialisations in the dogfish Centroscymnus coelolepis from the Mediterranean deep-sea. Scientia Marina 68 (Suppl 3) 185–195.

79. HartNS, TheissSM, HarahushBK, CollinSP (2011) Microspectrophotometric evidence for cone monochromacy in sharks. Naturwissenschaften 98: 193–201.

80. LisneyTJ, TheissSM, CollinsSP, HartNS (2012) Vision in elasmobranchs and their relatives: 21st century advances. J Fish Biol 80: 2024–2054.

81. SchieberNL, CollinS, HartNS (2012) Comparative retinal anatomy in four species of elasmobranch. J Morphol 273: 423–440.

82. MohunSM, DaviesWL, BowmakerJK, PisaniD, HimstedtW, et al. (2010) Identification and characterization of visual pigments in caecilians (Amphibia: Gymnophiona), an order of limbless vertebrates with rudimentary eyes. J Exp Biol 213: 3586–3592.

83. KosM, BulogB, SzélA, RöhlichP (2001) Immunocytochemical demonstration of visual pigments in the degenerate retinal and pineal photoreceptors of the blind cave salamander (Proteus anguinus). Cell Tissue Res 303: 15–25.

84. SchreerJF, KovacsKM (1997) Allometry of diving capacity in air-breathing vertebrates. Can J Zool 75: 339–358.

85. PanigadaS, ZanardelliM, CaneseS, JahodaM (1999) How deep can baleen whales dive? Mar Ecol Prog Ser 187: 309–311.

86. AmanoM, YoshiokaM (2003) Sperm whale diving behavior monitored using a suction-cup-attached TDR tag. Mar Ecol Prog Ser 258: 291–295.

87. CrollDA, MarinovicB, BensonS, ChavezFP, BlackN, et al. (2005) From wind to whales: trophic links in a coastal upwelling system. Mar Ecol Prog Ser 289: 117–130.

88. WatwoodSL, MillerPJO, JohnsonM, MadsenPT, TyackPL (2006) Deep-diving foraging behavior of sperm whales (Physeter macrocephalus). J Anim Ecol 75: 814–825.

89. Jerlov NG (1968) Optical oceanography. Amsterdam, The Netherlands: Elsevier Sci Publ Co.

90. WarrantEJ, LocketNA (2004) Vision in the deep sea. Biol Rev 79: 671–712.

91. FuY, KefalovV, LuoD-G, XueT, YauK-W (2008) Quantal noise from human red cone pigment. Nature Neurosci 11: 565–571.

92. LindbergDR, PyensonND (2007) Things that go bump in the night: evolutionary interactions between cephalopods and cetaceans in the tertiary. Lethaia 40: 335–343.

93. WareC, FriedlaenderAS, NowacekDP (2010) Shallow and deep lunge feeding of humpback whales in fjords of the West Antarctic Peninsula. Mar Mamm Sci 27: 587–605.

94. GoldbogenJA (2011) Mechanics, hydrodynamics and energetics of blue whale lunge feeding: efficiency dependence on krill density. J Exp Biol 214: 131–146.

95. Rambaut A (1996) Se-Al: sequence alignment editor, version 2.0a11. Available: http://tree.bio.ed.ac.uk/software/seal/.

96. StamatakisA (2006) RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688–2690.

97. Gatesy J (2009) Whales and even-toed ungulates (Cetartiodactyla). In: Hedges SB, Kumar S, eds. The timetree of life. Oxford, UK: Oxford Univ Press. pp 511–515.

98. Maddison WP, Maddison DR (2010) Mesquite: a modular system for evolutionary analysis, version 2.73. Available: http://mesquiteproject.org.

99. FasickJI, RobinsonPR (1998) Mechanism of spectral tuning in the dolphin visual pigments. Biochemistry 37: 433–438.

100. YangZ, dos ReisM (2011) Statistical properties of the branch-site test of positive selection. Mol Biol Evol 28: 1217–1228.

101. MeredithRW, JanečkaJE, GatesyJ, RyderOA, FisherCA, et al. (2011) Impacts of the Cretaceous terrestrial revolution and KPg extinction on mammal diversification. Science 334: 521–524.

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2013 Číslo 4
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#