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)Gresser, E. B. and Breder, C. M. (1940)Bridges, W. (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)Stefanelli, A. (1954)Rasquin, P. and Rosenbloom, L. (1954)Stefanelli, A. (1954)Luling, K. H. (1954)Luling, K. H. (1954)Thines, G. (1954)Luling, K. H. (1955)Luling, K. H. (1955)Sadoglu, P. (1956)Sadoglu, P. (1957)Sadoglu, P. (1957)Thines, G. and Kahling, J. (1957)Grobbel, G. and Hahn, G. (1958)Cahn, P. H. (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)Reed, M. (1966)Peters, N. and Peters, G. (1966)Carmignani, M. P. A. (1966)Cavicchioli, G. and Guarnieri, P. (1966)Thines, G., Soffie, M. and Vandenbussche, E. (1966)Popper, A. N. and Tavolga, W. N. (1967)Walters, V. and Liu, R. K. (1967)Sadoglu, P. (1967)Schemmel, C. (1967)Pfeiffer, W. (1967)Pfeiffer, W. (1967)Wilkens, H. (1968)Carmignani, M. P. A. (1968)Mattheij, J. A. (1968)Mattheij, J. A. (1968)Mattheij, J. A. and Sprangers, J. A. P. (1969)Weiss, B. A. (1969)Sadoglu, P. and McKee, A. (1969)Mattheij, J. A. (1969)Mattheij, J. A. (1970)Mattheij, J. A. (1970)Weiss, B. and Martini, J. (1970)Whitt, G. S. and Maeda, F. S. (1970)Gertychowa, R. (1970)Wilkens, H. (1970)Gertychowa, R. (1970)Wilkens, H. (1970)Wilkens, H. (1970)Popper, A. N. (1970)Popper, A. N. (1971)Wiley, S. and Mitchell, R. W. (1971)Wiley, S. and Mitchell, R. W. (1971)Gertychowa, R. (1971)Wilkens, H. (1971)Zaccone, G. (1971)Thines, G. and Wissocq, N. (1972)Wilkens, H. and Burns, R. J. (1972)Wilkens, H. (1972)Wilkens, H. (1972)Wilkens, H. (1972)Zaccone, G. (1972)Avise, J. C. and Selander, R. K. (1972)Zeitlin, S. M. and McDevitt, D. S. (1973)Voneida, T. J. (1973)Durand, J. P. (1973)Mitchell, R. W. (1973)Yasuda, K. (1973)Schemmel, C. (1973)Thines, G. and LeGrain, J. M. (1973)Zeitlin, S. M. (1973)Sligar, C. (1974)Schemmel, C. (1974)Schemmel, C. (1974)Chakraborty, R. and Nei, M. (1974)Omura, Y. (1975)Sadoglu, P. (1975)Peters, N., Scholl, A. and Wilkens, H. (1975)Sligar, C. and Voneida, T. J. (1976)Voneida, T. J. and Sligar, C. (1976)Durand, J. P. (1976)Erckens, W. and Weber, F. (1976)Wilkens, H. (1976)Herwig, H. J. (1976)Herwig, H. J. (1976)Kirby, R. F., Thompson, K. W. and Hubbs, C. (1977)Mitchell, R. W., Russell, W. H. and Elliott, W. R. (1977)Wilkens, H. (1977)Yew, D. T. and Yoshihara, H. M. (1977)Zaccone, G. (1977)Durand, J. P. (1978)Thines, G. and Weyers, M. (1978)Wilkens, H., Peters, H. and Schemmel, C. (1979)Woodhead, A. D. and Achey, P. M. (1979)Durand, J. P. (1979)Sadoglu, P. (1979)Quinn, T. P. (1980)Weissert, R. (1980)Wilkens, H. (1980)Wilkens, H. (1980)Schemmel, C. (1980)Reddell, J. R. (1981)Weissert, R. and Campenhausen, C. (1981)Campenhausen, C., Riess, I. and Weissert, R. (1981)Herwig, H. J. (1981)Jankowska, M. and Thines, G. (1982)Lamprecht, G. and Weber, F. (1982)Erckens, W. and Martin, W. (1982)Erckens, W. and Martin, W. (1982)Rose, F. L. and Mitchell, R. W. (1982)Tabata, M. (1982)Zilles, K., Tillmann, B. and Bennemann, R. (1983)Romero, A. (1983)Parzefall, J. (1983)Voneida, T. J. and Fish, S. E. (1984)Romero, A. (1984)Romero, A. (1984)Schuppa, M. (1984)Wilkens, H. (1984)Lamprecht, G. and Weber, F. (1985)Romero, A. (1985)Burchards, H., Dolle, A. and Parzefall, J. (1985)Teyke, T. (1985)Wilkens, H. (1985)Wilkens, H. and Huppop, K. (1986)De Fraipont, M. and Thines, G. (1986)De Fraipont, M. and Thines, G. (1986)Romero, A. (1986)Hassan, E. S. (1986)Parzefall, J. (1986)Wilkens, H. (1986)Huppop, K. (1986)De Fraipont, M. (1986)Fraipont, M. (1986)De Fraipont, M. (1987)De Fraipont, M. (1987)Huppop, K. (1987)Wilkens, H. (1987)De Fraipont, M. (1988)Fricke, D. (1988)Teyke, T. (1988)Huppop, K. (1988)Wilkens, H. (1988)Langecker, T. G. (1989)Fricke, D. and Parzefall, J. (1989)Fack, H. and Wilkens, H. (1989)Hassan, E. S. (1989)Teyke, T. (1989)Huppop, K. (1989)Klimpel, B. and Parzefall, J. (1990)Langecker, T. G. (1990)Parzefall, J. and Fricke, D. (1990)Yokoyama, R. and Yokoyama, S. (1990)Teyke, T. (1990)Peters, N., Schmidt, W. and Fricke, D. (1990)Yokoyama, R and Yokoyama, S (1990)Abdel-Latif, H., Hassan, E. S. and von Campenhausen, C. (1990)Huppop, K. (1991)Riedel, G. and Krug, L. (1991)Langecker, T. G., Wilkens, H. and Junge, P. (1991)Campenhausen, C. (1991)Parzefall, J. and Fricke, D. (1991)Huppop, K. and Wilkens, H. (1991)Wilkens, H. and Meyer, M. (1992)De Fraipont, M. (1992)Lamprecht, G. and Weber, F. (1992)Langecker, T. G. and Longley, G. (1992)Parzefall, J. (1992)Hassan, E. S., Abdel-Latif, H. and Biebricher, R. (1992)Parzefall, J. (1992)Wilkens, H. (1992)Langecker, T. G. (1993)Langecker, T. G., Schmale, H. and Wilkens, H. (1993)Langecker, T. G., Schmale, H. and Wilkens, H. (1993)Parzefall, J. (1993)Hoffman, S. and Hausberg, C. (1993)Peters, N., Schacht, V., Schmidt, W. and Wilkens, H. (1993)Borowsky, R. (1994)Teyke, T. and Schaerer, S. (1994)Langecker, T. G., Neumann, B., Hausberg, C. and Parzefall, J. (1995)Langecker, T. G., Wilkens, H. and Schmale, H. (1995)Yokoyama, S., Meany, A., Wilkens, H. and Yokoyama, R. (1995)Borowsky, R. (1996)Behrens, M., Langecker, T.G., Wilkens, H. and Schmale, H. (1997)Riedel, G. (1997)Riedel, G. and Krug, L. (1997)Borowsky, R. and Espinasa, L. (1997)Behrens, M, Wilkens, H and Schmale, H (1998)Jeffery, WR and Martasian, DP (1998)Contreras-Balderas, S. and Lozano-Vilano, M.D.L. (1998)Wilkens, H. (1998)Baker, CF and Montgomery, J (1999)Kullander, S. O. (1999)Jeffery, W. R., Strickler, A.G., Guiney, S., Heyser, D.G. and Tomarev, S.I. (2000)Yamamoto, Y. and Jeffery, W. R. (2000)Espinasa, L. and Borowsky, R. (2000)Ford, D.C. (2000)Jeffery, W. R. (2001)Boudriot, F and Reutter, K (2001)Montgomery, J.C., Coombs, S. and Baker, C.F. (2001)Espinasa, L. and Borowsky, R. (2001)Strickler, A.G., Yamamoto, Y. and Jeffery, W. R. (2001)Berg, A. and Watson, G.M. (2002)Dowling, TE, Martasian, DP and Jeffery, WR (2002)Krejca, J. (2002)Borowsky, RL and Wilkens, H (2002)Strickler, AG, Famuditimi, K and Jeffery, WR (2002)Romero, A., Jeffery, W.R. and Yamamoto, Y. (2002)Wilkens, H. and Strecker, U. (2003)Porter, M.L. and Crandall, K.A. (2003)Strecker, U. (2003)Strecker, U., Bernatchez, L. and Wilkens, H. (2003)Sarma, SSS, Lopez-Romulo, A and Nandini, S (2003)Contreras-Balderas, S, Almada-Villela, P, Lozano-Vilano, M de L and Garcia-Ramirez, ME (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, J.B., Tabin, C. and Borowsky, R.L. (2007)Protas, M, Tabansky, I, Conrad, M, Gross, JB, Vidal, O, Tabin, C and Borowsky, RL (2008)Gross, J.B., Protas, M., Conrad, M., Scheid, P.E., Vidal, O., Jeffery, W.R., Tabin, C. and others (2008)Salin, K, Voituron, Y, Colson, C and Hervant, F (2008)Kowalko, J, Gross, JB, Protas, M, Borowsky, RL and Tabin, C (2009)Jeffery, WR (2009)Salin, K., Voituron, Y., Mourin, J. and Hervant, F. (2010)Yamamoto, Y. and Jeffery, W.R. (2011)Kowalko, J, Rohner, N, Borowsky, RL and Tabin, C (2011)Kish, P.E., Bohnsack, B.L., Gallina, D., Kasprick, D.S. and Kahana, A. (2011)Esquivel-Bobadilla, S (2011)Bradic, M, Beerli, P and Borowsky, RL (2011)Salin, K, Voituron, Y, Mourin, J and Hervant, F (2011)Trontelj, P. (2012)Jeffery, W.R. (2012)Idda, M.L., Bertolucci, C., Vallone, D., Gothilf, Y., Sánchez-Vázquez, F.J. and Foulkes N.S. (2012)Dufton, M, Hall, BK and Franz-Odendaal, T. (2012)Protas, M. and 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)Hervant, F. (2012)Wilkens, H. (2012)Atukorala, A. D. S., Hammer, C., Dufton, M. and Franz-Odendaal, T. A. (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 S.B., Warren, W.C., Borowsky, R., Tabin, C.J., Jeffery, W.R. and Yoshizawa M. (2013)Gross, J.B., Furterer, A., Carlson, B.M. and Stahl, B.A. (2013)Elliott, William R. (2013)Stahl, B. A. and Gross, J. B. (2013)Stahl, AL (2013)Beale, A., Guibal, C., Tamai, T. K., Klotz, L., Cowen, S., Peyric, E., Reynoso, V. H., Yamamoto, Y. and Whitmore, D. (2013)Beale, A. (2013)Bradic, M., Teotonio, H. and Borowsky, R. L. (2013)Bibliowicz, J., Alie, A., Espinasa, L., Yoshizawa, M., Blin, M., Hinaux, H., Legendre, L., Pere, S. and Retaux, S. (2013)Pennisi, E. (2013)Pazza, R (2013)Moran, D., Softley, R. and Warrant, E.J. (2014)Espinasa, L., Bartolo, N.D. and Newkirk, C.E. (2014)Atukorallaya, D. and Franz-Odendaal, T. (2014)Gross, J.B., Krutzler, A.J. and Carlson, B.M. (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)Atukorala, A. D. S. and Franz-Odendaal, T. A. (2014)Elliott, W.R. (2014)Silva, D. M. Z. A., Utsunomia, R., Pansonato-Alves, J.C., Oliveira, C. and Foresti, F. (2015)Stemmer, M., Schuhmacher, L.-N., Foulkes, N.S., Bertolucci, C. and Wittbrodt, J. (2015)Moran, D., Softley, R. and Warrant, E.J. (2015)Hinaux, H., Blin, M., Fumey, J., Legendre, L., Heuze, A., Casane, D. and Retaux, S. (2015)Fumey, J. (2015)Carlson, B.M., Onusko, S.W. and Gross, J.B. (2015)McGaugh, S. E. (2015)Dufton, Megan and Franz-Odendaal, Tamara A. (2015)Stahl, Bethany A. and Gross, Joshua B. (2015)Stahl, B. A., Ma, L and Gross, J. B. (2015)Caballero-Hernandez, O., Hernandez-Patricio, M., Sigala-Regalado, I., Morales-Malacara, J. B. and Miranda-Anaya, M. (2015)Aspiras, A.C., Rohner, N., Martineau, B., Borowsky, R.L. and Tabin, C.J. (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)Bradic, M, Rohner, N, Tabin, C and Borowsky, R. (2015)Jaggard, J. B. (2015)Rohner, N (2015)Riddle, M and Tobin, C. J. (2015)Devos, Lucie, Alie, A. and Retaux, S (2015)Keene, A.C., Yoshizawa, M. and McGaugh, S.E. (2016)Casane, D. and Retaux, S. (2016)Foulkes, N. S., Whitmore, D., Vallone, D and Bertolucci, C. (2016)Beale, A., Whitmore, D. and Moran, D. (2016)Carlson, B.M. and Gross, J.B. (2016)O'Quin, Kelly and McGaugh, Suzanne E. (2016)Atukorala, A. D. S. and Franz-Odendaal, Tamara A. (2016)Beale, A. D. and Whitmore, D. (2016)Gross, J.B., Stahl, B.A., Powers, A.K. and Carlson, B.M. (2016)Rohner, Nicolas (2016)Aspiras, A., Tabin, C. and Rohner, N. (2016)Retaux, S., Alie, A., Blin, M., Devos, L., Elipot, Y. and Hinaux, H. (2016)Pennisi, E. (2016)Schmitter-Soto, JJ (2016)Pennisi, E (2016)Yoshizawa, M., Settle, A., Macaspac, C., Fernandes, V. Yoshida, M. and Keene, A. (2016)Yoshizawa, M (2017)Riddle, M. R.; Tabin, C. J (2017)Wilkens, H. and Strecker, U. (2017)Riddle, M (2017)Fumey J, Hinaux H, Noirot C, Thermes C, Re´ taux S, Casane D. (2017)Torres-Paz, J (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)Lyon, A., Powers, A. K., Gross, J. B. and O'Quin, K. E. (2017)Gross, J. B. (2017)Riddle, M (2017)Jaggard, J. B. (2017)Kaplan, S.A., Powers, A.K. and Gross, J.B. (2017)Krishnan, J and Rohner, N (2017)Alvarado, C.G. (2017)Hinaux, H, Recher, G, Alie, A., Legendre, L, Blin, M. and Retaux, S (2017)Schmitter-Soto, JJ (2017)Elliott, W.R. (2018)Kopp, J., Avasthi, S. and Espinasa, L. (2018)Devitsina, G.V. and Golovkina, T.V. (2018)Yoshizawa, M., Settle, A., Hermosura, M.C., Tuttle, L.J., Cetraro, N., Passow, C.N. and McGaugh, S.E. (2018)Riddle, M.R., Boesmans, W., Caballero, O, Kazwiny, Y. and Tabin,C.J. (2018)Ojha, A. and Watve, M. (2018)Fernandes, V.F.L., Macaspac, C., Lu, L. and Yoshizawa, M. (2018)Riddle, M., Martineau, B., Peavey, M. and Tabin, C. (2018)Kling, J. (2018)Gore, A., Jeffery, W., Retaux, S. and Rohner, N. (2018)Chin, J.S.R., Gassant, C.E., Amaral, P.M., Lloyd, E., Stahl, B.A., Jaggard, J.B., Keene, A.C. and Duboue, E.R. (2018)Gore, A.V., Rohner, N., Rétaux, S. and Jeffery, W.R. (2018)Fumey, J., Hinaux, H., Noirot, C., Thermes, C., Rétaux, S. and Casane, D. (2018)Stern, D.B and Crandall, K.A. (2018)Ma, L., Strickler, A.G., Parkhurst, A., Yoshizawa, M., Shi, J. and Jeffery, W.R. (2018)Xiong, S., Krishnan, J., Peuß, F. and Rohner, N. (2018)Ren, X.Y., Hamilton, N., Müller, F. and Yamamoto, Y. (2018)Torres-Paz,J., Hyacinthe, C., Pierre, C., Retaux, S. (2018)Carlson, B.M., Klingler, I.B., Meyer, B.J. and Gross, J.B. (2018)Gross, J.B., Weagley, J., Stahl, B.A., Ma, L., Espinasa, L. and McGaugh, S.E. (2018)Klaassen, H., Wang, Y., Adamski, K., Rohner, N. and Kowalko, J.E. (2018)Rohner, N. (2018)Frøland Steindal, I.V., Beale, A.D., Yamamoto, Y. and Whitmore, D. (2018)Devi, A., Atukorala, S. and Franz-Odendaal, T.A. (2018)Retaux, S. (2018)Blin, M., Tine, E., Meister, L., Elipot, Y., Bibliowicz, J., Espinasa, L. and Rétaux, S. (2018)Espinasa, L. (2018)Espinasa, L., Legendre, L., Fumey, J., Blin, M., Rétaux, S. and Espinasa, M. (2018)Mirande, J.M. (2018)Ornelas-García, P,. Pajares, S., Sosa-Jiménez, V.M., Rétaux, S. and Miranda-Gamboa, R.A. (2018)Borowsky, R. (2018)Jaggard, J.B., Stahl, B.A., Lloyd, E., Prober, D.A., Duboue, E.R. and Keene, A.C. (2018)Powers, A.K., Kaplan, S.A., Boggs, T.E. and Gross, J. (2018)Sovrano, V.A., Potrich, D., Foà, A. and Bertolucci, C. (2018)Tabin, J.A., Aspiras, A., Martineau, B., Riddle, M., Kowalko, J. Borowsky, R. Rohner, N. and Tabin, C.J. (2018)Carlson, B.M. and Gross, J.B. (2018)Borowsky, R., Luk, A., He, X.J. and Kim, R.S. (2018)Sears, C.R. and Gross, J.B. (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)Stah, B.A., Sears, C.R., Ma, L., Perkins, M. and Gross, J.B. (2018)Rohner, N. (2018)Garita-Alvarado, C.A., Barluenga, M. and Ornelas-García, C.P. (2018)Alie, A., Devos, L., Torres-Paz, J., Prunier, L., Boulet, F., Blin, M., Elipot, Y. and Retaux, S. (2018)Powers, A.K., Boggs, T.E. and Gross, J.B. (2018)Pazza, R., Dergam, J.A. and Kavalco, K.F. (2018)Pennisi, E. (2019)