Journal Article

The population genomics of repeated evolution in the blind cavefish Astyanax mexicanus

Bradic, M., Teotonio, H. and Borowsky, R. L.

Record Number:
3001
Year:
2013
Journal:
Molecular Biology and Evolution
Pages:
2383-2400
Volume:
30
Abstract:
Distinct populations of Astyanax mexicanus cavefish offer striking examples of repeatable convergence or parallelism in their independent evolutions from surface to cave phenotypes. However, the extent to which the repeatability of evolution occurred at the genetic level remains poorly understood. To address this, we first characterized the genetic diversity of 518 single-nucleotide polymorphisms (SNPs), obtained through RAD tag sequencing and distributed throughout the genome, in seven cave and three groups of surface populations. The cave populations represented two distinct lineages (old and new). Thirty-one SNPs were significantly differentiated between surface and old cave populations, two SNPs were differentiated between surface and new cave populations, and 44 SNPs were significantly differentiated in both old and new cave populations. In addition, we determined whether these SNPs map to the same locations of previously described quantitative trait loci (QTL) between surface and cave populations. A total of 25 differentiated SNPs co-map with several QTL, such as one containing a fibroblast growth factor gene (Fgf8) involved in eye development and lens size. Further, the identity of many SNPs that co-mapped with QTL was the same in independently derived cave populations. These conclusions were further confirmed by haplotype analyses of SNPs within QTL regions. Our findings indicate that the repeatability of evolution at the genetic level is substantial, suggesting that ancestral standing genetic variation significantly contributed to the population genetic variability used in adaptation to the cave environment.
Times Cited:
1
Related Records:
Hubbs, C.L. and Innes, W.T. (1936)Bridges, W. (1940)Gresser, E. B. and Breder, C. M. (1940)Breder, C. M. and Gresser, E. B. (1941)Breder, C. M. and Gresser, E. B. (1941)Breder, C. M. and Gresser, E. B. (1941)Breder, C. M. (1942)Breder, C. M. (1943)Breder, C. M. (1943)Osorio Tafall, B. F. (1943)Breder, C. M. (1944)Alvarez, J. (1946)Breder, C. M. and Rasquin, P. (1947)Breder, C. M. and Rasquin, P. (1947)Schlagel, S. R. and Breder, C. M. (1947)Alvarez, J. (1947)Rasquin, P. (1949)Luling, K. H. (1953)Luling, K. H. (1953)Luling, K. H. (1953)Luling, K. H. (1954)Luling, K. H. (1954)Stefanelli, A. (1954)Rasquin, P. and Rosenbloom, L. (1954)Stefanelli, A. (1954)Thines, G. (1954)Luling, K. H. (1955)Luling, K. H. (1955)Sadoglu, P. (1956)Thines, G. and Kahling, J. (1957)Sadoglu, P. (1957)Sadoglu, P. (1957)Cahn, P. H. (1958)Grobbel, G. and Hahn, G. (1958)Kahling, J. (1961)Luling, K. H. (1962)Burgers, A. C. J., Bennink, P. J. H. and van Oordt, G. J. (1963)Franck, A. (1964)Thines, G., Wolff-Van Ermengem, F., Boucquey, C. and Soffie, M. (1965)Boucquey, C., Thines, G. and Van Der Borght, C. (1965)Carmignani, M. P. A. (1966)Cavicchioli, G. and Guarnieri, P. (1966)Reed, M. (1966)Thines, G., Soffie, M. and Vandenbussche, E. (1966)Peters, N. and Peters, G. (1966)Pfeiffer, W. (1967)Pfeiffer, W. (1967)Popper, A. N. and Tavolga, W. N. (1967)Sadoglu, P. (1967)Schemmel, C. (1967)Walters, V. and Liu, R. K. (1967)Wilkens, H. (1968)Mattheij, J. A. (1968)Mattheij, J. A. (1968)Carmignani, M. P. A. (1968)Weiss, B. A. (1969)Mattheij, J. A. (1969)Mattheij, J. A. and Sprangers, J. A. P. (1969)Sadoglu, P. and McKee, A. (1969)Weiss, B. and Martini, J. (1970)Whitt, G. S. and Maeda, F. S. (1970)Popper, A. N. (1970)Wilkens, H. (1970)Wilkens, H. (1970)Wilkens, H. (1970)Mattheij, J. A. (1970)Mattheij, J. A. (1970)Gertychowa, R. (1970)Gertychowa, R. (1970)Wiley, S. and Mitchell, R. W. (1971)Wiley, S. and Mitchell, R. W. (1971)Popper, A. N. (1971)Wilkens, H. (1971)Gertychowa, R. (1971)Zaccone, G. (1971)Wilkens, H. (1972)Wilkens, H. (1972)Wilkens, H. (1972)Avise, J. C. and Selander, R. K. (1972)Thines, G. and Wissocq, N. (1972)Wilkens, H. and Burns, R. J. (1972)Zaccone, G. (1972)Zeitlin, S. M. (1973)Zeitlin, S. M. and McDevitt, D. S. (1973)Mitchell, R. W. (1973)Durand, J. P. (1973)Thines, G. and LeGrain, J. M. (1973)Yasuda, K. (1973)Voneida, T. J. (1973)Schemmel, C. (1973)Schemmel, C. (1974)Schemmel, C. (1974)Sligar, C. (1974)Chakraborty, R. and Nei, M. (1974)Peters, N., Scholl, A. and Wilkens, H. (1975)Omura, Y. (1975)Sadoglu, P. (1975)Herwig, H. J. (1976)Herwig, H. J. (1976)Sligar, C. and Voneida, T. J. (1976)Wilkens, H. (1976)Durand, J. P. (1976)Erckens, W. and Weber, F. (1976)Voneida, T. J. and Sligar, C. (1976)Zaccone, G. (1977)Kirby, R. F., Thompson, K. W. and Hubbs, C. (1977)Wilkens, H. (1977)Mitchell, R. W., Russell, W. H. and Elliott, W. R. (1977)Yew, D. T. and Yoshihara, H. M. (1977)Durand, J. P. (1978)Thines, G. and Weyers, M. (1978)Durand, J. P. (1979)Sadoglu, P. (1979)Wilkens, H., Peters, H. and Schemmel, C. (1979)Woodhead, A. D. and Achey, P. M. (1979)Weissert, R. (1980)Schemmel, C. (1980)Quinn, T. P. (1980)Wilkens, H. (1980)Wilkens, H. (1980)Herwig, H. J. (1981)Weissert, R. and Campenhausen, C. (1981)Campenhausen, C., Riess, I. and Weissert, R. (1981)Reddell, J. R. (1981)Jankowska, M. and Thines, G. (1982)Tabata, M. (1982)Lamprecht, G. and Weber, F. (1982)Rose, F. L. and Mitchell, R. W. (1982)Erckens, W. and Martin, W. (1982)Erckens, W. and Martin, W. (1982)Zilles, K., Tillmann, B. and Bennemann, R. (1983)Romero, A. (1983)Parzefall, J. (1983)Schuppa, M. (1984)Romero, A. (1984)Romero, A. (1984)Wilkens, H. (1984)Voneida, T. J. and Fish, S. E. (1984)Burchards, H., Dolle, A. and Parzefall, J. (1985)Teyke, T. (1985)Romero, A. (1985)Lamprecht, G. and Weber, F. (1985)Wilkens, H. (1985)Huppop, K. (1986)De Fraipont, M. (1986)Fraipont, M. (1986)De Fraipont, M. and Thines, G. (1986)Romero, A (1986)De Fraipont, M. and Thines, G. (1986)Wilkens, H. (1986)Parzefall, J. (1986)Wilkens, H. and Huppop, K. (1986)Hassan, E. S. (1986)Huppop, K. (1987)De Fraipont, M. (1987)De Fraipont, M. (1987)Wilkens, H. (1987)Huppop, K. (1988)Teyke, T. (1988)De Fraipont, M. (1988)Fricke, D. (1988)Wilkens, H. (1988)Fack, H. and Wilkens, H. (1989)Huppop, K. (1989)Teyke, T. (1989)Langecker, T. G. (1989)Fricke, D. and Parzefall, J. (1989)Hassan, E. S. (1989)Peters, N., Schmidt, W. and Fricke, D. (1990)Abdel-Latif, H., Hassan, E. S. and von Campenhausen, C. (1990)Klimpel, B. and Parzefall, J. (1990)Teyke, T. (1990)Langecker, T. G. (1990)Yokoyama, R. and Yokoyama, S. (1990)Yokoyama, R and Yokoyama, S (1990)Parzefall, J. and Fricke, D. (1990)Campenhausen, C. (1991)Huppop, K. and Wilkens, H. (1991)Huppop, K. (1991)Riedel, G. and Krug, L. (1991)Langecker, T. G., Wilkens, H. and Junge, P. (1991)Parzefall, J. and Fricke, D. (1991)De Fraipont, M. (1992)Lamprecht, G. and Weber, F. (1992)Langecker, T. G. and Longley, G. (1992)Wilkens, H. (1992)Parzefall, J. (1992)Parzefall, J. (1992)Wilkens, H. and Meyer, M. (1992)Hassan, E. S., Abdel-Latif, H. and Biebricher, R. (1992)Peters, N., Schacht, V., Schmidt, W. and Wilkens, H. (1993)Hoffman, S. and Hausberg, C. (1993)Langecker, T. G. (1993)Langecker, T. G., Schmale, H. and Wilkens, H. (1993)Parzefall, J. (1993)Langecker, T. G., Schmale, H. and Wilkens, H. (1993)Teyke, T. and Schaerer, S. (1994)Borowsky, R. (1994)Langecker, T. G., Neumann, B., Hausberg, C. and Parzefall, J. (1995)Yokoyama, S., Meany, A., Wilkens, H. and Yokoyama, R. (1995)Langecker, T. G., Wilkens, H. and Schmale, H. (1995)Borowsky, R. (1996)Riedel, G. (1997)Riedel, G. and Krug, L. (1997)Behrens, M., Langecker, T. G., Wilkens, H. and Schmale, H. (1997)Borowsky, R. and Espinasa, L. (1997)Contreras-Balderas, S. and Lozano-Vilano, M.D.L. (1998)Jeffery, WR and Martasian, DP (1998)Behrens, M, Wilkens, H and Schmale, H (1998)Wilkens, H. (1998)Baker, CF and Montgomery, J (1999)Kullander, S. O. (1999)Yamamoto, Y. and Jeffery, W. R. (2000)Jeffery, W. R., Strickler, A.G., Guiney, S., Heyser, D.G. and Tomarev, S.I. (2000)Espinasa, L. and Borowsky, R. (2000)Jeffery, W. R. (2001)Strickler, A.G., Yamamoto, Y. and Jeffery, W. R. (2001)Montgomery, J.C., Coombs, S. and Baker, C.F. (2001)Boudriot, F and Reutter, K (2001)Espinasa, L. and Borowsky, R. (2001)Strickler, AG, Famuditimi, K and Jeffery, WR (2002)Berg, A and Watson, GM (2002)Dowling, TE, Martasian, DP and Jeffery, WR (2002)Romero, A, Jeffery, WR and Yamamoto, Y (2002)Borowsky, RL and Wilkens, H (2002)Krejca, J. (2002)Strecker, U. (2003)Strecker, U., Bernatchez, L. and Wilkens, H. (2003)Contreras-Balderas, S, Almada-Villela, P, Lozano-Vilano, M de L and Garcia-Ramirez, ME (2003)Porter, M.L. and Crandall, K.A. (2003)Sarma, SSS, Lopez-Romulo, A and Nandini, S (2003)Wilkens, H. and Strecker, U. (2003)McCauley, DW, Hixon, E and Jeffery, WR (2004)Protas ME, Hersey C, Kochanek D, Zhou Y, Wilkens H, Jeffery WR, Zon LI, Borowsky R, Tabin CJ. (2006)Protas, M, Conrad, M, Gross, JB, Tabin, C and Borowsky, RL (2007)Protas, M, Tabansky, I, Conrad, M, Gross, JB, Vidal, O, Tabin, C and Borowsky, RL (2008)Gross, JB, Protas, M, Conrad, M, Scheid, PE, Vidal, O and others (2008)Jeffery, WR (2009)Kowalko, J, Gross, JB, Protas, M, Borowsky, RL and Tabin, C (2009)Esquivel-Bobadilla, S (2011)Kowalko, J, Rohner, N, Borowsky, RL and Tabin, C (2011)Bradic, M, Beerli, P and Borowsky, RL (2011)Jeffery, W.R. (2012)Gross, J.B. (2012)Bradic, M., Beerli, P., Garcia-de Leon, F. J., Esquivel-Bobadilla, S. and Borowsky, R. L. (2012)Protas, M. and Jeffery, W. R. (2012)Elliott, William R. (2013)Kowalko, J. E., Rohner, N., Rompani, S. B., Peterson, B. K., Linden, T. A., Yoshizawa, M., Kay, E. H., Weber, J., Hoekstra, H. E., Jeffery, W. R., Borowsky, R. and Tabin, C. J. (2013)Rohner, N., Jarosz, D. F., Kowalko, J. E., Yoshizawa, M., Jeffery, W. R., Borowsky, R. L., Lindquist, S. and Tabin, C. J. (2013)Rohner, N (2013)Kowalko, J., Rohner, N., Linden, T.A., Rompani SB, Warren, W.C., Borowsky, R, Tabin, C.J., Jeffery, W.R. and Yoshizawa M. (2013)Bradic, M., Teotonio, H. and Borowsky, R. L. (2013)Gross, J.B., Furterer, A., Carlson, B.M. and Stahl, B.A. (2013)Stahl, B. A. and Gross, J. B. (2013)Stahl, AL (2013)Pazza, R (2013)Bibliowicz, J., Alie, A., Espinasa, L., Yoshizawa, M., Blin, M., Hinaux, H., Legendre, L., Pere, S. and Retaux, S. (2013)Espinasa, L., Bartolo, N.D. and Newkirk, C.E. (2014)McGaugh, S.E., Gross, J.B., Aken, B., Blin, M., Borowsky, R., Chalopin, D., Hinaux, H., Jeffery, W.R., Keene, A., Ma, L., Minx, P., Murphy, D., O'Quin, K.E., Retaux, S., Rohner, N., Searl, S.M., Stahl, B.A., Tabin, C., Volff, J.N., Yoshizawa M, Warren WC. (2014)Moran, D, Softley, R and Warrant, EJ (2014)Elliott, W.R. (2014)Silva, D. M. Z. A., Utsunomia, R., Pansonato-Alves, J.C., Oliveira, C. and Foresti, F. (2015)McGaugh, S. E. (2015)Hinaux, Helene, Blin, Maryline, Fumey, Julien, Legendre, Laurent, Heuze, Aurelie, Casane, Didier and Retaux, Sylvie (2015)Moran, D, Softley, R and Warrant, EJ (2015)Fumey, J. (2015)Aspiras, Ariel C., Rohner, Nicolas, Martineau, Brian, Borowsky, Richard L. and Tabin, Clifford J. (2015)Caballero-Hernandez, O., Hernandez-Patricio, M., Sigala-Regalado, I., Morales-Malacara, J. B. and Miranda-Anaya, M. (2015)Bradic, M, Rohner, N, Tabin, C and Borowsky, R. (2015)Rohner, N (2015)Stahl, Bethany A. and Gross, Joshua B. (2015)Stahl, B. A., Ma, L and Gross, J. B. (2015)Yoshizawa, Masato, Robinson, Beatriz G., Duboue, Erik R., Masek, Pavel, Jaggard, James B., O'Quin, Kelly E., Borowsky, Richard L., Jeffery, William R. and Keene, Alex C. (2015)Jaggard, J. B. (2015)Devos, Lucie, Alie, A. and Retaux, S (2015)Casane, D and Retaux, S (2016)O'Quin, Kelly and McGaugh, Suzanne E. (2016)Schmitter-Soto, JJ (2016)Beale, A., Whitmore, D and Moran, D (2016)Rohner, Nicolas (2016)Aspiras, A., Tabin, C. and Rohner, N. (2016)Gross, J.B., Stahl, B.A., Powers, A.K. and Carlson, B.M. (2016)Keene, A.C., Yoshizawa, M. and McGaugh, S.E. (2016)Retaux, Sylvie, Alie, Alexandre, Blin, Maryline, Devos, Lucie, Elipot, Yannick and Hinaux, Helene (2016)Schmitter-Soto, JJ (2017)Fumey J, Hinaux H, Noirot C, Thermes C, Re´ taux S, Casane D. (2017)Krishnan, J and Rohner, N (2017)Jaggard, J. B., Robinson, B. G., Stahl, B, Oh, I, Masek, P, Yoshizawa, M and Keene, A. (2017)Stahl, B (2017)Stahl, B.A. and Gross, J.B. (2017)Jaggard, J. B. (2017)Wilkens, H. and Strecker, U. (2017)Hinaux, H, Recher, G, Alie, A., Legendre, L, Blin, M. and Retaux, S (2017)Elliott, W.R. (2018)Fumey, J., Hinaux, H., Noirot, C., Thermes, C., Rétaux, S. and Casane, D. (2018)Gross, J.B., Weagley, J., Stahl, B.A., Ma, L., Espinasa, L. and McGaugh, S.E. (2018)Espinasa, L. (2018)Espinasa, L., Legendre, L., Fumey, J., Blin, M., Rétaux, S. and Espinasa, M. (2018)Mirande, J.M. (2018)Riddle, M.R., Aspiras, A.C., Gaudenz, K., Peuß, R., Sung, J.Y., Martineau, B., Peavey, M., Box, A.C., Tabin, J.A., McGaugh, S., Borowsky, R., Tabin, C.J. and Rohner, N. (2018)Rohner, N. (2018)Pazza, R., Dergam, J.A. and Kavalco, K.F. (2018)Kling, J. (2018)Jaggard, J.B., Stahl, B.A., Lloyd, E., Prober, D.A., Duboue, E.R. and Keene, A.C. (2018)Chin, J.S.R., Gassant, C.E., Amaral, P.M., Lloyd, E., Stahl, B.A., Jaggarda, J.B., Keenea, A.C. and Duboue, E.R. (2018)Stern, D.B and Crandall, K.A. (2018)Xiong, S., Krishnan, J., Peuß, F. and Rohner, N. (2018)Alie, A., Devos, L., Torres-Paz, J., Prunier, L., Boulet, F., Blin, M., Elipot, Y. and Retaux, S. (2018)