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)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)Schlagel, S. R. and Breder, C. M. (1947)Alvarez, J. (1947)Breder, C. M. and Rasquin, P. (1947)Breder, C. M. and Rasquin, P. (1947)Rasquin, P. (1949)Luling, K. H. (1953)Luling, K. H. (1953)Luling, K. H. (1953)Thines, G. (1954)Luling, K. H. (1954)Luling, K. H. (1954)Stefanelli, A. (1954)Rasquin, P. and Rosenbloom, L. (1954)Stefanelli, A. (1954)Luling, K. H. (1955)Luling, K. H. (1955)Sadoglu, P. (1956)Thines, G. and Kahling, J. (1957)Sadoglu, P. (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)Carmignani, M. P. A. (1966)Peters, N. and Peters, G. (1966)Cavicchioli, G. and Guarnieri, P. (1966)Thines, G., Soffie, M. and Vandenbussche, E. (1966)Reed, M. (1966)Schemmel, C. (1967)Pfeiffer, W. (1967)Pfeiffer, W. (1967)Popper, A. N. and Tavolga, W. N. (1967)Walters, V. and Liu, R. K. (1967)Sadoglu, P. (1967)Carmignani, M. P. A. (1968)Mattheij, J. A. (1968)Mattheij, J. A. (1968)Wilkens, H. (1968)Mattheij, J. A. (1969)Weiss, B. A. (1969)Mattheij, J. A. and Sprangers, J. A. P. (1969)Sadoglu, P. and McKee, A. (1969)Popper, A. N. (1970)Mattheij, J. A. (1970)Weiss, B. and Martini, J. (1970)Mattheij, J. A. (1970)Whitt, G. S. and Maeda, F. S. (1970)Wilkens, H. (1970)Wilkens, H. (1970)Wilkens, H. (1970)Gertychowa, R. (1970)Gertychowa, R. (1970)Gertychowa, R. (1971)Popper, A. N. (1971)Wiley, S. and Mitchell, R. W. (1971)Wiley, S. and Mitchell, R. W. (1971)Zaccone, G. (1971)Wilkens, H. (1971)Avise, J. C. and Selander, R. K. (1972)Wilkens, H. and Burns, R. J. (1972)Thines, G. and Wissocq, N. (1972)Zaccone, G. (1972)Wilkens, H. (1972)Wilkens, H. (1972)Wilkens, H. (1972)Schemmel, C. (1973)Thines, G. and LeGrain, J. M. (1973)Voneida, T. J. (1973)Durand, J. P. (1973)Yasuda, K. (1973)Mitchell, R. W. (1973)Zeitlin, S. M. (1973)Zeitlin, S. M. and McDevitt, D. S. (1973)Schemmel, C. (1974)Schemmel, C. (1974)Chakraborty, R. and Nei, M. (1974)Sligar, C. (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)Voneida, T. J. and Sligar, C. (1976)Durand, J. P. (1976)Erckens, W. and Weber, F. (1976)Wilkens, H. (1976)Wilkens, H. (1977)Yew, D. T. and Yoshihara, H. M. (1977)Mitchell, R. W., Russell, W. H. and Elliott, W. R. (1977)Kirby, R. F., Thompson, K. W. and Hubbs, C. (1977)Zaccone, G. (1977)Thines, G. and Weyers, M. (1978)Durand, J. P. (1978)Wilkens, H., Peters, H. and Schemmel, C. (1979)Woodhead, A. D. and Achey, P. M. (1979)Durand, J. P. (1979)Sadoglu, P. (1979)Wilkens, H. (1980)Wilkens, H. (1980)Schemmel, C. (1980)Quinn, T. P. (1980)Weissert, R. (1980)Campenhausen, C., Riess, I. and Weissert, R. (1981)Herwig, H. J. (1981)Reddell, J. R. (1981)Weissert, R. and Campenhausen, C. (1981)Jankowska, M. and Thines, G. (1982)Erckens, W. and Martin, W. (1982)Erckens, W. and Martin, W. (1982)Rose, F. L. and Mitchell, R. W. (1982)Lamprecht, G. and Weber, F. (1982)Tabata, M. (1982)Romero, A. (1983)Parzefall, J. (1983)Zilles, K., Tillmann, B. and Bennemann, R. (1983)Wilkens, H. (1984)Schuppa, M. (1984)Voneida, T. J. and Fish, S. E. (1984)Romero, A. (1984)Romero, A. (1984)Teyke, T. (1985)Wilkens, H. (1985)Romero, A. (1985)Lamprecht, G. and Weber, F. (1985)Burchards, H., Dolle, A. and Parzefall, J. (1985)Hassan, E. S. (1986)Wilkens, H. (1986)De Fraipont, M. (1986)Fraipont, M. (1986)Wilkens, H. and Huppop, K. (1986)Huppop, K. (1986)De Fraipont, M. and Thines, G. (1986)De Fraipont, M. and Thines, G. (1986)Romero, A. (1986)Parzefall, J. (1986)Wilkens, H. (1987)De Fraipont, M. (1987)De Fraipont, M. (1987)Huppop, K. (1987)Teyke, T. (1988)Wilkens, H. (1988)De Fraipont, M. (1988)Huppop, K. (1988)Fricke, D. (1988)Teyke, T. (1989)Hassan, E. S. (1989)Huppop, K. (1989)Fack, H. and Wilkens, H. (1989)Langecker, T. G. (1989)Fricke, D. and Parzefall, J. (1989)Peters, N., Schmidt, W. and Fricke, D. (1990)Teyke, T. (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)Langecker, T. G. (1990)Parzefall, J. and Fricke, D. (1990)Parzefall, J. and Fricke, D. (1991)Langecker, T. G., Wilkens, H. and Junge, P. (1991)Huppop, K. and Wilkens, H. (1991)Huppop, K. (1991)Riedel, G. and Krug, L. (1991)Campenhausen, C. (1991)Hassan, E. S., Abdel-Latif, H. and Biebricher, R. (1992)Wilkens, H. (1992)De Fraipont, M. (1992)Wilkens, H. and Meyer, M. (1992)Lamprecht, G. and Weber, F. (1992)Parzefall, J. (1992)Parzefall, J. (1992)Langecker, T. G. and Longley, G. (1992)Langecker, T. G., Schmale, H. and Wilkens, H. (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)Parzefall, J. (1993)Langecker, T. G. (1993)Teyke, T. and Schaerer, S. (1994)Borowsky, R. (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)Wilkens, H. (1998)Behrens, M, Wilkens, H and Schmale, H (1998)Jeffery, WR and Martasian, DP (1998)Contreras-Balderas, S. and Lozano-Vilano, M.D.L. (1998)Baker, CF and Montgomery, J (1999)Kullander, S. O. (1999)Yamamoto, Y. and Jeffery, W. R. (2000)Ford, D.C. (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)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)Romero, A., Jeffery, W.R. and Yamamoto, Y. (2002)Borowsky, RL and Wilkens, H (2002)Krejca, J. (2002)Strickler, AG, Famuditimi, K and Jeffery, WR (2002)Contreras-Balderas, S, Almada-Villela, P, Lozano-Vilano, M de L and Garcia-Ramirez, ME (2003)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)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)Salin, K, Voituron, Y, Colson, C and Hervant, F (2008)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)Salin, K., Voituron, Y., Mourin, J. and Hervant, F. (2010)Kowalko, J, Rohner, N, Borowsky, RL and Tabin, C (2011)Salin, K, Voituron, Y, Mourin, J and Hervant, F (2011)Bradic, M, Beerli, P and Borowsky, RL (2011)Yamamoto, Y. and Jeffery, W.R. (2011)Esquivel-Bobadilla, S (2011)Kish, P.E., Bohnsack, B.L., Gallina, D., Kasprick, D.S. and Kahana, A. (2011)Gross, J.B. (2012)Hervant, F. (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)Idda, M.L., Bertolucci, C., Vallone, D., Gothilf, Y., Sánchez-Vázquez, F.J. and Foulkes N.S. (2012)Wilkens, H. (2012)Trontelj, P. (2012)Dufton, M, Hall, BK and Franz-Odendaal, T. (2012)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 S.B., 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)Pennisi, E. (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)Atukorala, A. D. S., Hammer, C., Dufton, M. and Franz-Odendaal, T. A. (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)Moran, D., Softley, R. and Warrant, E.J. (2014)Elliott, W.R. (2014)Gross, J.B., Krutzler, A.J. and Carlson, B.M. (2014)Holzman, R., Perkol-Finkel, S. and Zilman, G. (2014)Atukorallaya, D. and Franz-Odendaal, T. (2014)Espinasa, L., Bartolo, N.D. and Newkirk, C.E. (2014)Atukorala, A. D. S. and Franz-Odendaal, T. A. (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, E.J. (2015)Hinaux, H., Blin, M., Fumey, J., Legendre, L., Heuze, A., Casane, D. and Retaux, S. (2015)Fumey, J. (2015)Caballero-Hernandez, O., Hernandez-Patricio, M., Sigala-Regalado, I., Morales-Malacara, J. B. and Miranda-Anaya, M. (2015)Riddle, M and Tobin, C. J. (2015)Aspiras, A.C., Rohner, N., Martineau, B., Borowsky, R.L. and Tabin, C.J. (2015)Bradic, M, Rohner, N, Tabin, C and Borowsky, R. (2015)Stahl, Bethany A. and Gross, Joshua B. (2015)Rohner, N (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)Stemmer, M., Schuhmacher, L.-N., Foulkes, N.S., Bertolucci, C. and Wittbrodt, J. (2015)Jaggard, J. B. (2015)O'Quin, Kelly E., Doshi, Pooja, Lyon, Anastasia, Hoenemeyer, Emma, Yoshizawa, Masato and Jeffery, William R. (2015)Devos, Lucie, Alie, A. and Retaux, S (2015)Carlson, B.M., Onusko, S.W. and Gross, J.B. (2015)Dufton, Megan and Franz-Odendaal, Tamara A. (2015)Silva, D. M. Z. A., Utsunomia, R., Pansonato-Alves, J.C., Oliveira, C. and Foresti, F. (2015)McGaugh, S. E. (2015)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)Beale, A., Whitmore, D. and Moran, D. (2016)Schmitter-Soto, JJ (2016)Pennisi, E. (2016)Pennisi, E (2016)Rohner, Nicolas (2016)Yoshizawa, M., Settle, A., Macaspac, C., Fernandes, V. Yoshida, M. and Keene, A. (2016)Gross, J.B., Stahl, B.A., Powers, A.K. and Carlson, B.M. (2016)Aspiras, A., Tabin, C. and Rohner, N. (2016)Foulkes, N. S., Whitmore, D., Vallone, D and Bertolucci, C. (2016)Keene, A.C., Yoshizawa, M. and McGaugh, S.E. (2016)Lyon, A., Krutzler, A.J., Gross, J.B. and O'Quin, K.E. (2016)O'Quin, K.E., Doshi, P., Lyon, A., Hoenemeyer, E., Yoshizawa, M. and Jeffery, W.R. (2016)Retaux, S., Alie, A., Blin, M., Devos, L., Elipot, Y. and Hinaux, H. (2016)Carlson, B.M. and Gross, J.B. (2016)Casane, D. and Retaux, S. (2016)Fumey J, Hinaux H, Noirot C, Thermes C, Re´ taux S, Casane D. (2017)Lyon, A., Powers, A. K., Gross, J. B. and O'Quin, K. E. (2017)Gross, J. B. (2017)Riddle, M (2017)Kaplan, S.A., Powers, A.K. and Gross, J.B. (2017)Schmitter-Soto, JJ (2017)Yoshizawa, M (2017)Riddle, M. R.; Tabin, C. J (2017)Jaggard, J. B., Robinson, B. G., Stahl, B, Oh, I, Masek, P, Yoshizawa, M and Keene, A. (2017)Krishnan, J and Rohner, N (2017)Stahl, B (2017)Alvarado, C.G. (2017)Stahl, B.A. and Gross, J.B. (2017)Jaggard, J. B. (2017)Wilkens, H. and Strecker, U. (2017)Torres-Paz, J (2017)Hinaux, H, Recher, G, Alie, A., Legendre, L, Blin, M. and Retaux, S (2017)Riddle, M (2017)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)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)Ornelas-García, P,. Pajares, S., Sosa-Jiménez, V.M., Rétaux, S. and Miranda-Gamboa, R.A. (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)Carlson, B.M. and Gross, J.B. (2018)Espinasa, L. (2018)Sears, C.R. and Gross, J.B. (2018)Espinasa, L., Legendre, L., Fumey, J., Blin, M., Rétaux, S. and Espinasa, M. (2018)Stah, B.A., Sears, C.R., Ma, L., Perkins, M. and Gross, J.B. (2018)Mirande, J.M. (2018)Powers, A.K., Boggs, T.E. and Gross, J.B. (2018)Borowsky, R. (2018)Tabin, J.A., Aspiras, A., Martineau, B., Riddle, M., Kowalko, J. Borowsky, R. Rohner, N. and Tabin, C.J. (2018)Borowsky, R., Luk, A., He, X.J. and Kim, R.S. (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)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)Fernandes, V.F.L., Macaspac, C., Lu, L. and Yoshizawa, M. (2018)Riddle, M., Martineau, B., Peavey, M. and Tabin, C. (2018)Rohner, N. (2018)Garita-Alvarado, C.A., Barluenga, M. and Ornelas-García, C.P. (2018)Lloyd, E., Olive, C., Stahl, B.A., Jaggarda, J.B., Amaral, P., Dubouéa, E.R and Keene, A.C. (2018)Pazza, R., Dergam, J.A. and Kavalco, K.F. (2018)Jaggard, J.B., Stahl, B.A., Lloyd, E., Prober, D.A., Duboue, E.R. and Keene, A.C. (2018)Kopp, J., Avasthi, S. and Espinasa, L. (2018)Kling, J. (2018)Ojha, A. and Watve, M. (2018)Torres-Paz,J., Hyacinthe, C., Pierre, C., 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)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)Carlson, B.M., Klingler, I.B., Meyer, B.J. and Gross, J.B. (2018)Alie, A., Devos, L., Torres-Paz, J., Prunier, L., Boulet, F., Blin, M., Elipot, Y. and Retaux, S. (2018)Xiong, S., Krishnan, J., Peuß, F. and Rohner, N. (2018)Ren, X.Y., Hamilton, N., Müller, F. and Yamamoto, Y. (2018)Klaassen, H., Wang, Y., Adamski, K., Rohner, N. and Kowalko, J.E. (2018)Elliott, W.R. (2018)Rohner, N. (2018)Devitsina, G.V. and Golovkina, T.V. (2018)Pennisi, E. (2019)Stahl, B.A., Peuß, R., McDole, B., Kenzior, A., Jaggard, J.B., Gaudenz, K., Krishnan, J., McGaugh, S.E., Duboue, E.R., Keene, A.C and Rohner, N. (2019)Kindl, G.H. and O’Quin, K.E. (2019)Blin, M. and Retaux, S. (2019)