A Novel Role for in the Parallel Evolution of Depigmentation in Independent Populations of the Cavefish


The evolution of degenerate characteristics remains a poorly understood phenomenon. Only recently has the identification of mutations underlying regressive phenotypes become accessible through the use of genetic analyses. Focusing on the Mexican cave tetra Astyanax mexicanus, we describe, here, an analysis of the brown mutation, which was first described in the literature nearly 40 years ago. This phenotype causes reduced melanin content, decreased melanophore number, and brownish eyes in convergent cave forms of A. mexicanus. Crosses demonstrate non-complementation of the brown phenotype in F2 individuals derived from two independent cave populations: Pachón and the linked Yerbaniz and Japonés caves, indicating the same locus is responsible for reduced pigmentation in these fish. While the brown mutant phenotype arose prior to the fixation of albinism in Pachón cave individuals, it is unclear whether the brown mutation arose before or after the fixation of albinism in the linked Yerbaniz/Japonés caves. Using a QTL approach combined with sequence and functional analyses, we have discovered that two distinct genetic alterations in the coding sequence of the gene Mc1r cause reduced pigmentation associated with the brown mutant phenotype in these caves. Our analysis identifies a novel role for Mc1r in the evolution of degenerative phenotypes in blind Mexican cavefish. Further, the brown phenotype has arisen independently in geographically separate caves, mediated through different mutations of the same gene. This example of parallelism indicates that certain genes are frequent targets of mutation in the repeated evolution of regressive phenotypes in cave-adapted species.


Vyšlo v časopise: A Novel Role for in the Parallel Evolution of Depigmentation in Independent Populations of the Cavefish. PLoS Genet 5(1): e32767. doi:10.1371/journal.pgen.1000326
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1000326

Souhrn

The evolution of degenerate characteristics remains a poorly understood phenomenon. Only recently has the identification of mutations underlying regressive phenotypes become accessible through the use of genetic analyses. Focusing on the Mexican cave tetra Astyanax mexicanus, we describe, here, an analysis of the brown mutation, which was first described in the literature nearly 40 years ago. This phenotype causes reduced melanin content, decreased melanophore number, and brownish eyes in convergent cave forms of A. mexicanus. Crosses demonstrate non-complementation of the brown phenotype in F2 individuals derived from two independent cave populations: Pachón and the linked Yerbaniz and Japonés caves, indicating the same locus is responsible for reduced pigmentation in these fish. While the brown mutant phenotype arose prior to the fixation of albinism in Pachón cave individuals, it is unclear whether the brown mutation arose before or after the fixation of albinism in the linked Yerbaniz/Japonés caves. Using a QTL approach combined with sequence and functional analyses, we have discovered that two distinct genetic alterations in the coding sequence of the gene Mc1r cause reduced pigmentation associated with the brown mutant phenotype in these caves. Our analysis identifies a novel role for Mc1r in the evolution of degenerative phenotypes in blind Mexican cavefish. Further, the brown phenotype has arisen independently in geographically separate caves, mediated through different mutations of the same gene. This example of parallelism indicates that certain genes are frequent targets of mutation in the repeated evolution of regressive phenotypes in cave-adapted species.


Zdroje

1. ProtasME

HerseyC

KochanekD

ZhouY

WilkensH

2006 Genetic analysis of cavefish reveals molecular convergence in the evolution of albinism. Nat Genet 38 107 111

2. ProtasM

TabanskyI

ConradM

GrossJB

VidalO

2008 Multi-trait evolution in a cave fish, Astyanax mexicanus. Evol Dev 10 196 209

3. BensouilahM

DenizotJ-P

1991 Taste buds and neuromasts of Astyanax jordani: Distribution and immunochemical demonstration of co-localized substance P and enkephalins. Eur J Neurosci 3 407 414

4. WilkensH

1988 Evolution and genetics of epigean and cave Astyanax fasciatus (Characidae, Pisces): Support for the neutral mutation theory.

HechtMK

WallaceB

Evolutionary biology New York Plenum Publishing Corporation 271 367

5. JefferyWR

2001 Cavefish as a model system in evolutionary developmental biology. Dev Biol 231 1 12

6. JefferyWR

2008 Emerging model systems in evo-devo: cavefish and microevolution of development. Evol Dev 10 265 272

7. Kosswig

C

1964 Problems of polymorphism in fishes. Copeia 1964 65 75

8. AviseJC

SelanderR

1971 Evolutionary genetics of cave-dwelling fishes of the genus Astyanax. Evolution 26 1 19

9. MitchellRW

RussellWH

ElliotWR

1977 Mexican eyeless characin fishes, genus Astyanax: Environment, distribution, and evolution. Spec Publ Mus Texas Tech Univ 12 1 89

10. Sadoglu

P

1979 A breeding method for blind Astyanax mexicanus based on annual spawning patterns. Copeia 1979 369 371

11. SadogluP

1957a A Mendelian gene for albinism in natural cave fish. Experientia 13 394

12. SadogluP

1957b Mendelian inheritance in the hybrids between the Mexican blind cave fish and their overground ancestor. Verh Deut Zool, Graz 1957 432 439

13. KosswigC

1963 Genetische Analyse konstruktiver und degenerativer Evolutionsprozesse. Zeit Zool Syst Evolut 1 290 309

14. SadogluP

1967 The selective value of eye and pigment loss in Mexican cave fish. Evolution 21 541 549

15. ProtasM

ConradM

GrossJB

TabinC

BorowskyR

2007 Regressive evolution in the Mexican cave tetra, Astyanax mexicanus. Curr Biol 17 452 454

16. WilkensH

StreckerU

2003 Convergent evolution of the cavefish Astyanax (Characidae, Teleostei): genetic evidence from reduced eye-size and pigmentation. Biol J Linn Soc 80 545 554

17. BrederCM

RasquinP

1947 Comparative studies in the light sensitivity of blind characins from a series of Mexican caves. Bull Amer Mus Natur Hist 89 323 351

18. SadogluP

McKeeA

1969 A second gene that affects eye and body color in Mexican blind cave fish. J Hered 60 10 14

19. WilkensH

2004 The Astyanax model (Teleostei): neutral mutations and directional selection. Mitt Hamb Zool Mus Inst 101 123 130

20. VassilatisDK

HohmannJG

ZengH

LiF

RanchalisJE

2003 The G protein-coupled receptor repertoires of human and mouse. Proc Natl Acad Sci U S A 100 4903 4908

21. ReesJL

2003 Genetics of hair and skin color. Annu Rev Genet 37 67 90

22. WidlundHR

FisherDE

2003 Microphthalmia-associated transcription factor: a critical regulator of pigment cell development and survival. Oncogene 22 3035 3041

23. RobbinsLS

NadeauJH

JohnsonKR

KellyMA

Roselli-RehfussL

1993 Pigmentation phenotypes of variant extension locus alleles result from point mutations that alter MSH receptor function. Cell 72 827 834

24. MundyNI

2005 A window on the genetics of evolution: MC1R and plumage colouration in birds. Proc Biol Sci 272 1633 1640

25. SchiöthHB

PhillipsSR

RudzishR

Birch-MachinMA

WikbergJE

1999 Loss of function mutations of the human melanocortin 1 receptor are common and are associated with red hair. Biochem Biophys Res Commun 260 488 491

26. FlanaganN

HealyE

RayA

PhilipsS

ToddC

2000 Pleiotropic effects of the melanocortin 1 receptor (MC1R) gene on human pigmentation. Hum Mol Genet 9 2531 2537

27. SturmRA

DuffyDL

BoxNF

NewtonRA

ShepherdAG

2003 Genetic association and cellular function of MC1R variant alleles in human pigmentation. Ann N Y Acad Sci 994 348 358

28. BeaumontKA

NewtonRA

SmitDJ

LeonardJH

StowJL

2005 Altered cell surface expression of human MC1R variant receptor alleles associated with red hair and skin cancer risk. Hum Mol Genet 14 2145 2154

29. LoganDW

BurnSF

JacksonIJ

2006 Regulation of pigmentation in zebrafish melanophores. Pigment Cell Res 19 206 213

30. StemshornKC

NolteAW

TautzD

2005 A genetic map of Cottus gobio (Pisces, Teleostei) based on microsatellites can be linked to the physical map of Tetraodon nigroviridis. J Evol Biol 18 1619 1624

31. RoseTM

HenikoffJG

HenikoffS

2003 CODEHOP (COnsensus-DEgenerate Hybrid Oligonucleotide Primer) PCR primer design. Nucl Acids Res 31 3763 3766

32. KimmelCB

BallardWW

KimmelSR

UllmannB

SchillingTF

1995 Stages of embryonic development of the zebrafish. Dev Dyn 203 253 310

33. FinkSV

FinkWL

1996 Interrelationships of ostariophysan fishes (Teleostei).

StiassnyMLJ

ParentiLR

JohnsonGD

Interrelationships of fishes New York Academic Press 209 249

34. ReesJL

Birch-MachinM

FlanaganN

HealyE

PhillipsS

1999 Genetic studies of the human melanocortin-1 receptor. Ann N Y Acad Sci 885 134 142

35. JohnPR

RamsayM

2002 Four novel variants in MC1R in red-haired South African individuals of European descent: S83P, Y152X, A171D, P256S. Hum Mutat 19 461 462

36. NaysmithL

WaterstonK

HaT

FlanaganN

BissetY

2004 Quantitative measures of the effect of the melanocortin 1 receptor on human pigmentary status. J Invest Derm 122 423 428

37. Sánchez-LaordenBL

Sánchez-MásJS

Martínez-AlonsoE

Martínez-MenárguezA

García-BorrónJC

2006 Dimerization of the human melanocortin 1 receptor: Functional consequences and dominant-negative effects. J Invest Derm 126 172 181

38. BeaumontKA

ShekarSL

NewtonRA

JamesMR

StowJL

2007 Receptor function, dominant negative activity and phenotype correlations for MC1R variant alleles. Hum Mol Genet 16 2249 2260

39. SteíngrimssonE

CopelandNG

JenkinsNA

2006 Mouse coat color mutations: From fancy mice to functional genomics. Dev Dyn 235 2401 2411

40. KadekaroAL

KantoH

KavanaghR

Abdel-MalekZA

2003 Significance of melanocortin 1 receptor in regulating human melanocyte pigmentation, proliferation, and survival. Ann N Y Acad Sci 994 359 365

41. JacksonIJ

KeighrenM

BuddP

da SilvaN

LoganD

2004 The molecular genetics of MC1R in humans, mice and fish. Pigment Cell Res 17 572

42. MarklundL

JohnanssonMollerM

SandbergK

AnderssonL

1996 A missense mutation in the gene for melanocyte-stimulating hormone receptor (MC1R) is associated with chestnut coat color in horses. Mamm Genome 7 895 899

43. KijasJMH

WalesR

TörnstenA

ChardonP

MollerM

1998 Melanocortin receptor 1 (MC1R) mutations and coat color in pigs. Genetics 150 1177 1185

44. NewtonJM

WilkieAL

HeL

JordanSA

MetallinosDL

2000 Melanocortin 1 receptor variation in domestic dog. Mamm Genome 11 24 30

45. Gutiérrez-GilB

WienerP

WilliamsJL

2007 Genetic effects on coat colour in cattle: dilution of eumelanin and phaeomelanin pigments in an F2 -backcross Charolais×Holstein population. BMC Genet 8 56

46. HoekstraHE

NachmanMW

2003 Different genes underlie adaptive melanism in different populations of rock pocket mice. Mol Ecol 12 1185 1194

47. MundyNI

BadcockNS

HartT

ScribnerK

JanssenK

2004 Conserved genetic basis of a quantitative plumage trait involved in mate choice. Science 303 1870 1873

48. RosenblumEB

HoekstraHE

NachmanMW

2004 Adaptive reptile color variation and the evolution of the MC1R gene. Evolution 58 1794 1808

49. HoekstraHE

HirschmannRJ

BundeyRA

InselPA

CrosslandJP

2006 A single amino acid mutation contributes to adaptive beach mouse color pattern. Science 313 101 104

50. BaiãoPC

SchreiberEA

ParkerPG

2007 The genetic basis of the plumage polymorphism in red-footed boobies (Sula sula): A melanocortin-1 receptor (MC1R) analysis. J Hered 98 287 292

51. BastiaensMT

ter HuurneJ

KielichC

GruisNA

WestendorpRG

2001 Melanocortin-1 receptor gene variants determine the risk of nonmelanoma skin cancer independently of fair skin and red hair. Am J Hum Genet 68 884 894

52. KennedyC

ter HuurneJ

BerkhoutM

GruisN

BastiaensM

2001 Melanocortin 1 receptor (MC1R) gene variants are associated with an increased risk for cutaneous melanoma which is largely independent of skin type and hair color. J Invest Dermatol 117 294 300

53. SturmRA

2002 Skin colour and skin cancer-MC1r, the genetic link. Melanoma Res 12 405 416

54. MogilJS

RitchieJ

SmithSB

StrasburgK

KaplanL

2005 Melanocortin-1 receptor gene variants affect pain and μ-opiod analgesia in mice and humans. J Med Genet 42 583 587

55. BeaumontKA

ShekarSN

CookAL

DuffyDL

SturmRA

2008 Red hair is a null phenotype of MC1R. Hum Mutat 29 E88 E94

56. BorowskyR

WilkensH

2002 Mapping a cave fish genome: Polygenic systems and regressive evolution. J Hered 93 19 21

57. PorterML

CrandallKA

2003 Lost along the way: The significance of evolution in reverse. Trends Ecol Evol 18 541 547

58. McCauleyDW

HixonE

JefferyWR

2004 Evolution of pigment cell regression in the cavefish Astyanax: A late step in melanogenesis. Evol Dev 6 209 218

59. JefferyWR

2005 Adaptive evolution of eye degeneration in the Mexican blind cavefish. J Hered 96 185 96

60. PfeifferW

1966 Uber die vererbung der Schreckreaktion bei Astyanax (Characidae, Pisces). Z Vererbungsl 98 97 105

61. MetzJR

PetersJJM

FlikG

2006 Molecular biology and physiology of the melanocortin system in fish: A review. Gen Comp Endocrinol 148 150 162

62. TakahashiA

KawauchiH

2006 Evolution of melanocortin systems in fish. Gen Comp Endocrinol 148 85 94

63. LoganDW

Bryson-RichardsonRJ

PagánKE

TaylorMS

CurriePD

2003a The structure and evolution of the melanocortin and MCH receptors in fish and mammals. Genomics 81 184 191

64. LoganDW

Bryson-RichardsonRJ

TaylorMS

CurrieP

JacksonIJ

2003b Sequence characterization of teleost fish melanocortin receptors. Ann N Y Acad Sci 994 319 330

65. BoswellT

TakeuchiS

2005 Recent developments in our understanding of the avian melanocortin system: Its involvement in the regulation of pigmentation and energy homeostasis. Peptides 26 1733 1743

66. SelzY

BraaschI

HoffmannC

SchmidtC

SchultheisC

2007 Evolution of melanocortin receptors in teleost fish: the melanocortin type 1 receptor. Gene 401 114 122

67. DongS

LeungKKH

PellingAL

LeePYT

TangASP

2002 Circling, deafness, and yellow coat displayed by yellow submarine (ysb) and light coat and circling (lcc) mice with mutations on chromosome 3. Genomics 79 777 784

68. Abdel-MalekZ

ScottMC

SuzukiI

TadaA

ImS

2000 The melanocortin-1 receptor is a key regulator of human cutaneous pigmentation. Pigment Cell Res 13 156 162

69. BagnaraJT

1998 Comparative anatomy and physiology of pigment cells in nonmammalian tissues.

NordlundJJ

BoissyRE

HearingVJ

KingRA

OrtonneJP

The pigmentary system: Physiology and pathophysiology New York Oxford University Press 9 40

70. KelshRN

2004 Genetics and evolution of pigment patterns in fish. Pigment Cell Res 17 326 336

71. JacksonIJ

1997 Homologous pigmentation mutations in human, mouse and other model organisms. Hum Mol Genet 6 1613 1624

72. DarwinC

1859 On the origin of species by means of natural selection, or, The preservation of favoured races in the struggle for life London John Murray 502

73. BarrT

1968 Cave ecology and the evolution of troglobites. Evol Biol 2 35 102

74. CulverDC

1982 Cave life: Evolution and ecology Cambridge Harvard University Press 189

75. DoucetSM

ShawkeyMD

RathburnMK

MaysHLJr

MontgomerieR

2004 Concordant evolution of plumage colour, feather microstructure and a melanocortin receptor gene between mainland and island populations of a fairy-wren. Proc R Soc Lond B Biol Sci 271 1663 1670

76. AokiK

2002 Sexual selection as a cause of human skin colour variation: Darwin's hypothesis revisited. Ann Hum Biol 29 589 608

77. HardingRM

HealyE

RayAJ

EllisNS

FlanaganN

2000 Evidence for variable selective pressures at MC1R. Am J Hum Genet 66 1351 1361

78. BamshadM

WoodingSP

2003 Signatures of natural selection in the human genome. Nat Rev Genet 4 99 111

79. SabetiPC

SchaffnerSF

FryB

LohmuellerJ

VarillyP

2006 Positive natural selection in the human lineage. Science 312 1614 1620

80. SchwartzGG

RosenblumLA

1981 Allometry of primate hair density and the evolution of human hairlessness. Amer J Phy Anthropol 55 9 12

81. KelshRN

BrandM

JiangYJ

HeisenbergCP

LinS

1996 Zebrafish pigmentation mutations and the processes of neural crest development. Development 123 369 389

82. ParichyDM

JohnsonSL

2001 Zebrafish hybrids suggest genetic mechanisms for pigment pattern diversification in Danio. Dev Genes Evol 211 319 328

83. FukamachiS

SugimotoM

MitaniH

ShimaA

2004 Somatolactin selectively regulates proliferation and morphogenesis of neural-crest derived pigment cells in medaka. Proc Natl Acad Sci U S A 101 10661 10666

84. KlovinsJ

HaitinaT

FridmanisD

KilianovaZ

KapaI

2003 The melanocortin system in Fugu: determination of POMC/AGRP/MCR gene repertoire and synteny, as well as pharmacology and anatomical distribution of the MCRs. Mol Biol Evol 21 563 579

85. MillerCT

BelezaS

PollenAA

SchluterD

KittlesRA

2007 cis-Regulatory changes in Kit ligand expression and parallel evolution of pigmentation in sticklebacks and humans. Cell 131 1179 1189

86. BoughmanJW

2007 Sticklebacks and humans walk hand in fin to lighter skin. Cell 131 1041 1043

87. LamasonRL

MohideenMA

MestJR

WongAC

NortonHL

2005 SLC24A5, a putative cation exchanger, affects pigmentation in zebrafish and humans. Science 310 1782 1786

88. EspinasaL

BorowskyRB

2000 Eyed cave fish in a karst window. J Cave Karst Studies 62 180 183

89. EspinasaL

BorowskyRB

2001 Origins and relationship of cave populations of the blind Mexican tetra, Astyanax fasciatus, in the Sierra de el Abra. Environ Biol Fishes 62 233 237

90. PanaramK

BorowskyR

2005 Gene flow and genetic variability in cave and surface populations of the Mexican tetra, Astyanax mexicanus (Teleostei: Characidae). Copeia 2005 409 416

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2009 Číslo 1
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Eozinofilní granulomatóza s polyangiitidou
nový kurz
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