Journal Article

The evolution of gene expression underlying vision loss in cave animals

Stern, D.B and Crandall, K.A.

Record Number:
3930
Year:
2018
Journal:
Molecular Biology and Evolution
Pages:
yy
Volume:
xx
Abstract:
Dissecting the evolutionary genetic processes underlying eye reduction and vision loss in obligate cave-dwelling organisms has been a long-standing challenge in evolutionary biology. In dependent vision loss events in related subterranean organisms can provide critical insight into these processes as well as into the nature of convergent loss of complex traits. Advances in evolutionary developmental biology have illuminated the significant role of heritable gene expression variation in the evolution of new forms. Here we analyze gene expression variation in adult eye tissue across the freshwater crayfish, representing four independent vision-loss events in caves. Species and individual expression patterns cluster by eye function rather than phylogeny, suggesting convergence in transcriptome evolution in independently blind animals. However, this clustering is not greater than what is observed in surface species with conserved eye function after accounting for phylogenetic expectations. Modeling expression evolution suggests that there is a common increase in evolutionary rates in the blind lineages, consistent with a relaxation of selective constraint maintaining optimal expression levels. This is evidence for a repeated loss of expression constraint in the transcriptomes of blind animals and that convergence occurs via a similar trajectory through genetic drift.
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)Sadoglu, P. (1957)Thines, G. and Kahling, J. (1957)Sadoglu, P. (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)Peters, N. and Peters, G. (1966)Carmignani, M. P. A. (1966)Cavicchioli, G. and Guarnieri, P. (1966)Reed, M. (1966)Thines, G., Soffie, M. and Vandenbussche, E. (1966)Schemmel, C. (1967)Walters, V. and Liu, R. K. (1967)Pfeiffer, W. (1967)Pfeiffer, W. (1967)Popper, A. N. and Tavolga, W. N. (1967)Sadoglu, P. (1967)Carmignani, M. P. A. (1968)Mattheij, J. A. (1968)Mattheij, J. A. (1968)Wilkens, H. (1968)Sadoglu, P. and McKee, A. (1969)Weiss, B. A. (1969)Mattheij, J. A. (1969)Mattheij, J. A. and Sprangers, J. A. P. (1969)Weiss, B. and Martini, J. (1970)Popper, A. N. (1970)Whitt, G. S. and Maeda, F. S. (1970)Mattheij, J. A. (1970)Wilkens, H. (1970)Mattheij, J. A. (1970)Wilkens, H. (1970)Wilkens, H. (1970)Gertychowa, R. (1970)Gertychowa, R. (1970)Popper, A. N. (1971)Wiley, S. and Mitchell, R. W. (1971)Wiley, S. and Mitchell, R. W. (1971)Wilkens, H. (1971)Zaccone, G. (1971)Gertychowa, R. (1971)Thines, G. and Wissocq, N. (1972)Wilkens, H. and Burns, R. J. (1972)Avise, J. C. and Selander, R. K. (1972)Wilkens, H. (1972)Wilkens, H. (1972)Wilkens, H. (1972)Zaccone, G. (1972)Voneida, T. J. (1973)Schemmel, C. (1973)Yasuda, K. (1973)Durand, J. P. (1973)Mitchell, R. W. (1973)Zeitlin, S. M. (1973)Zeitlin, S. M. and McDevitt, D. S. (1973)Thines, G. and LeGrain, J. M. (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)Voneida, T. J. and Sligar, C. (1976)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)Yew, D. T. and Yoshihara, H. M. (1977)Kirby, R. F., Thompson, K. W. and Hubbs, C. (1977)Wilkens, H. (1977)Zaccone, G. (1977)Mitchell, R. W., Russell, W. H. and Elliott, W. R. (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)Schemmel, C. (1980)Weissert, R. (1980)Quinn, T. P. (1980)Wilkens, H. (1980)Wilkens, H. (1980)Herwig, H. J. (1981)Campenhausen, C., Riess, I. and Weissert, R. (1981)Weissert, R. and Campenhausen, C. (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)Romero, A. (1983)Zilles, K., Tillmann, B. and Bennemann, R. (1983)Parzefall, J. (1983)Voneida, T. J. and Fish, S. E. (1984)Schuppa, M. (1984)Romero, A. (1984)Romero, A. (1984)Wilkens, H. (1984)Burchards, H., Dolle, A. and Parzefall, J. (1985)Teyke, T. (1985)Romero, A. (1985)Lamprecht, G. and Weber, F. (1985)Wilkens, H. (1985)Wilkens, H. and Huppop, K. (1986)Hassan, E. S. (1986)Huppop, K. (1986)De Fraipont, M. (1986)Fraipont, M. (1986)De Fraipont, M. and Thines, G. (1986)De Fraipont, M. and Thines, G. (1986)Romero, A. (1986)Wilkens, H. (1986)Parzefall, J. (1986)Huppop, K. (1987)De Fraipont, M. (1987)De Fraipont, M. (1987)Wilkens, H. (1987)Huppop, K. (1988)De Fraipont, M. (1988)Teyke, T. (1988)Fricke, D. (1988)Wilkens, H. (1988)Fack, H. and Wilkens, H. (1989)Hassan, E. S. (1989)Huppop, K. (1989)Teyke, T. (1989)Langecker, T. G. (1989)Fricke, D. and Parzefall, J. (1989)Parzefall, J. and Fricke, D. (1990)Peters, N., Schmidt, W. and Fricke, D. (1990)Abdel-Latif, H., Hassan, E. S. and von Campenhausen, C. (1990)Yokoyama, R. and Yokoyama, S. (1990)Yokoyama, R and Yokoyama, S (1990)Klimpel, B. and Parzefall, J. (1990)Teyke, T. (1990)Langecker, T. G. (1990)Langecker, T. G., Wilkens, H. and Junge, P. (1991)Parzefall, J. and Fricke, D. (1991)Campenhausen, C. (1991)Huppop, K. and Wilkens, H. (1991)Huppop, K. (1991)Riedel, G. and Krug, L. (1991)Wilkens, H. and Meyer, M. (1992)Hassan, E. S., Abdel-Latif, H. and Biebricher, R. (1992)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)Parzefall, J. (1993)Langecker, T. G., Schmale, H. and Wilkens, H. (1993)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)Borowsky, R. (1994)Teyke, T. and Schaerer, S. (1994)Langecker, T. G., Wilkens, H. and Schmale, H. (1995)Yokoyama, S., Meany, A., Wilkens, H. and Yokoyama, R. (1995)Langecker, T. G., Neumann, B., Hausberg, C. and Parzefall, J. (1995)Borowsky, R. (1996)Riedel, G. (1997)Behrens, M., Langecker, T.G., Wilkens, H. and Schmale, H. (1997)Riedel, G. and Krug, L. (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)Ford, D.C. (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)Krejca, J. (2002)Romero, A., Jeffery, W.R. and Yamamoto, Y. (2002)Berg, A. and Watson, G.M. (2002)Strickler, AG, Famuditimi, K and Jeffery, WR (2002)Dowling, TE, Martasian, DP and Jeffery, WR (2002)Borowsky, RL and Wilkens, H (2002)Porter, M.L. and Crandall, K.A. (2003)Sarma, SSS, Lopez-Romulo, A and Nandini, S (2003)Wilkens, H. and Strecker, U. (2003)Contreras-Balderas, S, Almada-Villela, P, Lozano-Vilano, M de L and Garcia-Ramirez, ME (2003)Strecker, U. (2003)Strecker, U., Bernatchez, L. and Wilkens, H. (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)Kowalko, J, Gross, JB, Protas, M, Borowsky, RL and Tabin, C (2009)Jeffery, WR (2009)Esquivel-Bobadilla, S (2011)Bradic, M, Beerli, P and Borowsky, RL (2011)Yamamoto, Y. and Jeffery, W.R. (2011)Kish, P.E., Bohnsack, B.L., Gallina, D., Kasprick, D.S. and Kahana, A. (2011)Kowalko, J, Rohner, N, Borowsky, RL and Tabin, C (2011)Protas, M. and Jeffery, W. R. (2012)Dufton, M, Hall, BK and Franz-Odendaal, T. (2012)Idda, M.L., Bertolucci, C., Vallone, D., Gothilf, Y., Sánchez-Vázquez, F.J. and Foulkes N.S. (2012)Gross, J.B. (2012)Bradic, M., Beerli, P., Garcia-de Leon, F. J., Esquivel-Bobadilla, S. and Borowsky, R. L. (2012)Jeffery, W.R. (2012)Wilkens, H. (2012)Trontelj, P. (2012)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)Atukorala, A. D. S., Hammer, C., Dufton, M. and Franz-Odendaal, T. A. (2013)Stahl, B. A. and Gross, J. B. (2013)Stahl, AL (2013)Elliott, William R. (2013)Bibliowicz, J., Alie, A., Espinasa, L., Yoshizawa, M., Blin, M., Hinaux, H., Legendre, L., Pere, S. and Retaux, S. (2013)Bradic, M., Teotonio, H. and Borowsky, R. L. (2013)Pazza, R (2013)Atukorallaya, D. and Franz-Odendaal, T. (2014)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)Atukorala, A. D. S. and Franz-Odendaal, T. A. (2014)Elliott, W.R. (2014)Gross, J.B., Krutzler, A.J. and Carlson, B.M. (2014)Moran, D., Softley, R. and Warrant, E.J. (2014)Aspiras, A.C., Rohner, N., Martineau, B., Borowsky, R.L. and Tabin, C.J. (2015)Stahl, Bethany A. and Gross, Joshua B. (2015)Stahl, B. A., Ma, L and Gross, J. B. (2015)McGaugh, S. E. (2015)Dufton, Megan and Franz-Odendaal, Tamara A. (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)Stemmer, Manuel, Schuhmacher, Laura-Nadine, Foulkes, Nicholas S., Bertolucci, Cristiano and Wittbrodt, Joachim (2015)Devos, Lucie, Alie, A. and Retaux, S (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)Carlson, B.M., Onusko, S.W. and Gross, J.B. (2015)Silva, D. M. Z. A., Utsunomia, R., Pansonato-Alves, J.C., Oliveira, C. and Foresti, F. (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)Schmitter-Soto, JJ (2016)Gross, J.B., Stahl, B.A., Powers, A.K. and Carlson, B.M. (2016)O'Quin, Kelly and McGaugh, Suzanne E. (2016)Atukorala, A. D. S. and Franz-Odendaal, Tamara A. (2016)Yoshizawa, M., Settle, A., Macaspac, C., Fernandes, V. Yoshida, M. and Keene, A. (2016)Foulkes, N. S., Whitmore, D., Vallone, D and Bertolucci, C. (2016)Retaux, S., Alie, A., Blin, M., Devos, L., Elipot, Y. and Hinaux, H. (2016)Rohner, Nicolas (2016)Carlson, B.M. and Gross, J.B. (2016)Aspiras, A., Tabin, C. and Rohner, N. (2016)Casane, D. and Retaux, S. (2016)Beale, A., Whitmore, D. and Moran, D. (2016)Keene, A.C., Yoshizawa, M. and McGaugh, S.E. (2016)Lyon, A., Powers, A. K., Gross, J. B. and O'Quin, K. E. (2017)Gross, J. B. (2017)Kaplan, S.A., Powers, A.K. and Gross, J.B. (2017)Schmitter-Soto, JJ (2017)Jaggard, J. B., Robinson, B. G., Stahl, B, Oh, I, Masek, P, Yoshizawa, M and Keene, A. (2017)Stahl, B (2017)Yoshizawa, M (2017)Stahl, B.A. and Gross, J.B. (2017)Jaggard, J. B. (2017)Torres-Paz, J (2017)Hinaux, H, Recher, G, Alie, A., Legendre, L, Blin, M. and Retaux, S (2017)Krishnan, J and Rohner, N (2017)Alvarado, C.G. (2017)Wilkens, H. and Strecker, U. (2017)Fumey J, Hinaux H, Noirot C, Thermes C, Re´ taux S, Casane D. (2017)Retaux, S. (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., Jeffery, W., Retaux, S. and Rohner, N. (2018)Blin, M., Tine, E., Meister, L., Elipot, Y., Bibliowicz, J., Espinasa, L. and Rétaux, S. (2018)Gore, A.V., Rohner, N., Rétaux, S. and Jeffery, W.R. (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)Powers, A.K., Kaplan, S.A., Boggs, T.E. and Gross, J. (2018)Carlson, B.M. and Gross, J.B. (2018)Sears, C.R. and Gross, J.B. (2018)Stah, B.A., Sears, C.R., Ma, L., Perkins, M. and Gross, J.B. (2018)Powers, A.K., Boggs, T.E. and Gross, J.B. (2018)Gross, J.B., Weagley, J., Stahl, B.A., Ma, L., Espinasa, L. and McGaugh, S.E. (2018)Devi, A., Atukorala, S. and Franz-Odendaal, T.A. (2018)Yoshizawa, M., Settle, A., Hermosura, M.C., Tuttle, L.J., Cetraro, N., Passow, C.N. and McGaugh, S.E. (2018)Fernandes, V.F.L., Macaspac, C., Lu, L. and Yoshizawa, M. (2018)Jaggard, J.B., Stahl, B.A., Lloyd, E., Prober, D.A., Duboue, E.R. and Keene, A.C. (2018)Torres-Paz,J., Hyacinthe, C., Pierre, C., Retaux, S. (2018)Espinasa, L. (2018)Espinasa, L., Legendre, L., Fumey, J., Blin, M., Rétaux, S. and Espinasa, M. (2018)Alie, A., Devos, L., Torres-Paz, J., Prunier, L., Boulet, F., Blin, M., Elipot, Y. and Retaux, S. (2018)Mirande, J.M. (2018)Borowsky, R. (2018)Elliott, W.R. (2018)Carlson, B.M., Klingler, I.B., Meyer, B.J. and Gross, J.B. (2018)Tabin, J.A., Aspiras, A., Martineau, B., Riddle, M., Kowalko, J. Borowsky, R. Rohner, N. and Tabin, C.J. (2018)Devitsina, G.V. and Golovkina, T.V. (2018)Borowsky, R., Luk, A., He, X.J. and Kim, R.S. (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)Garita-Alvarado, C.A., Barluenga, M. and Ornelas-García, C.P. (2018)Fumey, J., Hinaux, H., Noirot, C., Thermes, C., Rétaux, S. and Casane, D. (2018)Pazza, R., Dergam, J.A. and Kavalco, K.F. (2018)Kopp, J., Avasthi, S. and Espinasa, L. (2018)Kling, J. (2018)Ojha, A. and Watve, M. (2018)