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 medicínaČlánok vyšiel v časopise
PLOS Genetics
2009 Číslo 1
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- A -Acting Diversification Activator Both Necessary and Sufficient for AID-Mediated Hypermutation
- Order and Disorder during Divergence
- Mouse Genome-Wide Association Mapping Needs Linkage Analysis to Avoid False-Positive Loci
- Why Is the Correlation between Gene Importance and Gene Evolutionary Rate So Weak?