Abstract
The genetic basis of vertebrate morphological evolution has traditionally been very difficult to examine in naturally occurring populations. Here we describe the generation of a genome-wide linkage map to allow quantitative trait analysis of evolutionarily derived morphologies in the Mexican cave tetra, a species that has, in a series of independent caves, repeatedly evolved specialized characteristics adapted to a unique and well-studied ecological environment. We focused on the trait of albinism and discovered that it is linked to Oca2, a known pigmentation gene, in two cave populations. We found different deletions in Oca2 in each population and, using a cell-based assay, showed that both cause loss of function of the corresponding protein, OCA2. Thus, the two cave populations evolved albinism independently, through similar mutational events.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Rent or buy this article
Prices vary by article type
from$1.95
to$39.95
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Culver, D.C. Cave Life (Harvard University, Cambridge, 1982).
Romero, A. & Paulson, K.M. It's a wonderful hypogean life: a guide to the troglomorphic fishes of the world. Environ. Biol. Fishes 62, 13–41 (2001).
Espinasa, L., Rivas-Manzano, P. & Perez, H. A new blind cave fish population of genus Astyanax: geography, morphology and behavior. Environ. Biol. Fishes 62, 339–344 (2001).
Wilkens, H. Evolution and genetics of epigean and cave Astyanax (Characidae, Pisces). Evol. Biol. 23, 271–367 (1988).
Yamamoto, Y., Espinasa, L., Stock, D.W. & Jeffery, W.R. Development and evolution of craniofacial patterning is mediated by eye-dependent and -independent processes in the cavefish Astyanax. Evol. Dev. 5, 435–446 (2003).
Dowling, T.E., Martasian, D.P. & Jeffery, W.R. Evidence for multiple genetic forms with similar eyeless phenotypes in the blind cavefish, Astyanax mexicanus. Mol. Biol. Evol. 19, 446–455 (2002).
Strecker, U., Bernatchez, L. & Wilkens, H. Genetic divergence between cave and surface populations of Astyanax in Mexico (Characidae, Teleostei). Mol. Ecol. 12, 699–710 (2003).
Strecker, U., Faundez, V.H. & Wilkens, H. Phylogeography of surface and cave Astyanax (Teleostei) from Central and North America based on cytochrome b sequence data. Mol. Phylogenet. Evol. 33, 469–481 (2004).
Borowsky, R. & Wilkens, H. Mapping a cave fish genome: polygenic systems and regressive evolution. J. Hered. 93, 19–21 (2002).
Sadoglu, P. & McKee, A. A second gene that effects eye and body color in Mexican blind cave fish. J. Hered. 60, 10–14 (1969).
Oetting, W.S., Garrett, S.S., Brott, M. & King, R.A. P gene mutations associated with oculocutaneous albinism type II (OCA2). Hum. Mutat. 25, 323 (2005).
Fukamachi, S. et al. Conserved function of medaka pink-eyed dilution in melanin synthesis and its divergent transcriptional regulation in gonads among vertebrates. Genetics 168, 1519–1527 (2004).
Rinchik, E.M. et al. A gene for the mouse pink-eyed dilution locus and for human type II oculocutaneous albinism. Nature 361, 72–76 (1993).
Sviderskaya, E.V. et al. Complementation of hypopigmentation in p-mutant (pink-eyed dilution) mouse melanocytes by normal human P cDNA, and defective complementation by OCA2 mutant sequences. J. Invest. Dermatol. 108, 30–34 (1997).
Jeffery, W.R. Adaptive evolution of eye degeneration in the Mexican blind cavefish. J. Hered. 96, 185–196 (2005).
Page-McCaw, P.S. et al. Retinal network adaptation to bright light requires tyrosinase. Nat. Neurosci. 7, 1329–1336 (2004).
Yi, Z. et al. A 122.5-kilobase deletion of the P gene underlies the high prevalence of oculocutaneous albinism type 2 in the Navajo population. Am. J. Hum. Genet. 72, 62–72 (2003).
Colosimo, P.F. et al. Widespread parallel evolution in sticklebacks by repeated fixation of Ectodysplasin alleles. Science 307, 1928–1933 (2005).
Shapiro, M.D. et al. Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks. Nature 428, 717–723 (2004).
Sucena, E., Delon, I., Jones, I., Payre, F. & Stern, D.L. Regulatory evolution of shavenbaby/ovo underlies multiple cases of morphological parallelism. Nature 424, 935–938 (2003).
Majerus, M.E. & Mundy, N.I. Mammalian melanism: natural selection in black and white. Trends Genet. 19, 585–588 (2003).
Mundy, N.I. A window on the genetics of evolution: MC1R and plumage colouration in birds. Proc. Biol. Sci. 272, 1633–1640 (2005).
Gompel, N., Prud'homme, B., Wittkopp, P.J., Kassner, V.A. & Carroll, S.B. Chance caught on the wing: cis-regulatory evolution and the origin of pigment patterns in Drosophila. Nature 433, 481–487 (2005).
Van Laere, A.S. et al. A regulatory mutation in IGF2 causes a major QTL effect on muscle growth in the pig. Nature 425, 832–836 (2003).
Peichel, C.L. et al. The genetic architecture of divergence between three spine stickleback species. Nature 414, 901–905 (2001).
Matsuda, T. & Cepko, C.L. Electroporation and RNA interference in the rodent retina in vivo and in vitro. Proc. Natl. Acad. Sci. USA 101, 16–22 (2004).
Acknowledgements
This work was supported by US National Science Foundation grant IBN0217178 to R. Borowsky and C.J. Tabin. The authors thank L. Mekios for phenotyping and fish maintenance, the Bennett group for the use of the melan-p cell line, T. Matsuda for the pUB-GFP construct, R.C. Albertson for critical reading of the manuscript, and C. Peichel, R.V. Pearse II, J.L. Galloway and J. Rivera-Feliciano for help and advice.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Supplementary Fig. 1
Amino acid sequence of Oca2 from surface, Molino, and Pachón populations. (PDF 1747 kb)
Supplementary Fig. 2
Missing exons in Pachón and Molino Oca2 coding sequence are genomic deletions and not splice variants. (PDF 554 kb)
Supplementary Table 1
Microsatellite markers and primer sequences. (PDF 53 kb)
Supplementary Table 2
Polymorphisms in the Japonés, Pachón, and Molino populations. (PDF 27 kb)
Rights and permissions
About this article
Cite this article
Protas, M., Hersey, C., Kochanek, D. et al. Genetic analysis of cavefish reveals molecular convergence in the evolution of albinism. Nat Genet 38, 107–111 (2006). https://doi.org/10.1038/ng1700
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/ng1700
This article is cited by
-
Lack of genetic differentiation between two sympatric lacustrine morpho-species within the Astyanax (Characidae: Teleostei) genus, Mexico
Ichthyological Research (2024)
-
Selection-driven trait loss in independently evolved cavefish populations
Nature Communications (2023)
-
Pattern of color inheritance in African catfish (Clarias gariepinus): an expression of a Mendelian law
Fish Physiology and Biochemistry (2023)
-
Identifying Targets of Selection in Laboratory Evolution Experiments
Journal of Molecular Evolution (2023)
-
Fish genomics and its impact on fundamental and applied research of vertebrate biology
Reviews in Fish Biology and Fisheries (2022)