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)Osorio Tafall, B. F. (1943)Breder, C. M. (1943)Breder, C. M. (1943)Breder, C. M. (1944)Alvarez, J. (1946)Breder, C. M. and Rasquin, P. (1947)Alvarez, J. (1947)Schlagel, S. R. and Breder, C. M. (1947)Breder, C. M. and Rasquin, P. (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)Stefanelli, A. (1954)Rasquin, P. and Rosenbloom, L. (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)Boucquey, C., Thines, G. and Van Der Borght, C. (1965)Thines, G., Wolff-Van Ermengem, F., Boucquey, C. and Soffie, M. (1965)Carmignani, M. P. A. (1966)Peters, N. and Peters, G. (1966)Cavicchioli, G. and Guarnieri, P. (1966)Reed, M. (1966)Thines, G., Soffie, M. and Vandenbussche, E. (1966)Sadoglu, P. (1967)Walters, V. and Liu, R. K. (1967)Schemmel, C. (1967)Pfeiffer, W. (1967)Pfeiffer, W. (1967)Popper, A. N. and Tavolga, W. N. (1967)Carmignani, M. P. A. (1968)Wilkens, H. (1968)Mattheij, J. A. (1968)Mattheij, J. A. (1968)Weiss, B. A. (1969)Sadoglu, P. and McKee, A. (1969)Mattheij, J. A. (1969)Mattheij, J. A. and Sprangers, J. A. P. (1969)Weiss, B. and Martini, J. (1970)Whitt, G. S. and Maeda, F. S. (1970)Wilkens, H. (1970)Wilkens, H. (1970)Wilkens, H. (1970)Popper, A. N. (1970)Mattheij, J. A. (1970)Mattheij, J. A. (1970)Gertychowa, R. (1970)Gertychowa, R. (1970)Gertychowa, R. (1971)Wiley, S. and Mitchell, R. W. (1971)Wiley, S. and Mitchell, R. W. (1971)Zaccone, G. (1971)Wilkens, H. (1971)Popper, A. N. (1971)Avise, J. C. and Selander, R. K. (1972)Zaccone, G. (1972)Wilkens, H. (1972)Wilkens, H. (1972)Wilkens, H. (1972)Wilkens, H. and Burns, R. J. (1972)Thines, G. and Wissocq, N. (1972)Voneida, T. J. (1973)Yasuda, K. (1973)Schemmel, C. (1973)Zeitlin, S. M. (1973)Zeitlin, S. M. and McDevitt, D. S. (1973)Durand, J. P. (1973)Thines, G. and LeGrain, J. M. (1973)Mitchell, R. W. (1973)Schemmel, C. (1974)Chakraborty, R. and Nei, M. (1974)Schemmel, C. (1974)Sligar, C. (1974)Omura, Y. (1975)Sadoglu, P. (1975)Peters, N., Scholl, A. and Wilkens, H. (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)Zaccone, G. (1977)Wilkens, H. (1977)Kirby, R. F., Thompson, K. W. and Hubbs, C. (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)Sadoglu, P. (1979)Durand, J. P. (1979)Weissert, R. (1980)Schemmel, C. (1980)Quinn, T. P. (1980)Wilkens, H. (1980)Wilkens, H. (1980)Campenhausen, C., Riess, I. and Weissert, R. (1981)Weissert, R. and Campenhausen, C. (1981)Herwig, H. J. (1981)Reddell, J. R. (1981)Jankowska, M. and Thines, G. (1982)Tabata, M. (1982)Erckens, W. and Martin, W. (1982)Lamprecht, G. and Weber, F. (1982)Erckens, W. and Martin, W. (1982)Rose, F. L. and Mitchell, R. W. (1982)Parzefall, J. (1983)Zilles, K., Tillmann, B. and Bennemann, R. (1983)Romero, A. (1983)Voneida, T. J. and Fish, S. E. (1984)Wilkens, H. (1984)Romero, A. (1984)Romero, A. (1984)Burchards, H., Dolle, A. and Parzefall, J. (1985)Teyke, T. (1985)Wilkens, H. (1985)Lamprecht, G. and Weber, F. (1985)Romero, A. (1985)Hassan, E. S. (1986)Parzefall, J. (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)Wilkens, H. (1986)Romero, A (1986)Wilkens, H. and Huppop, K. (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)Wilkens, H. (1988)Fricke, D. (1988)Hassan, E. S. (1989)Huppop, K. (1989)Teyke, T. (1989)Langecker, T. G. (1989)Fricke, D. and Parzefall, J. (1989)Fack, H. and Wilkens, H. (1989)Parzefall, J. and Fricke, D. (1990)Yokoyama, R. and Yokoyama, S. (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)Teyke, T. (1990)Klimpel, B. and Parzefall, J. (1990)Langecker, T. G. (1990)Langecker, T. G., Wilkens, H. and Junge, P. (1991)Campenhausen, C. (1991)Parzefall, J. and Fricke, D. (1991)Huppop, K. and Wilkens, H. (1991)Huppop, K. (1991)Riedel, G. and Krug, L. (1991)Wilkens, H. and Meyer, M. (1992)Parzefall, J. (1992)Hassan, E. S., Abdel-Latif, H. and Biebricher, R. (1992)Parzefall, J. (1992)De Fraipont, M. (1992)Lamprecht, G. and Weber, F. (1992)Wilkens, H. (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)Parzefall, J. (1993)Hoffman, S. and Hausberg, C. (1993)Peters, N., Schacht, V., Schmidt, W. and Wilkens, H. (1993)Langecker, T. G. (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)Borowsky, R. and Espinasa, L. (1997)Riedel, G. and Krug, L. (1997)Contreras-Balderas, S. and Lozano-Vilano, M.D.L. (1998)Behrens, M, Wilkens, H and Schmale, H (1998)Jeffery, WR and Martasian, DP (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)Strickler, A.G., Yamamoto, Y. and Jeffery, W. R. (2001)Jeffery, W. R. (2001)Boudriot, F and Reutter, K (2001)Espinasa, L. and Borowsky, R. (2001)Montgomery, J.C., Coombs, S. and Baker, C.F. (2001)Romero, A, Jeffery, WR and Yamamoto, Y (2002)Krejca, J. (2002)Berg, A and Watson, GM (2002)Strickler, AG, Famuditimi, K and Jeffery, WR (2002)Dowling, TE, Martasian, DP and Jeffery, WR (2002)Borowsky, RL and Wilkens, H (2002)Wilkens, H. and Strecker, U. (2003)Porter, M.L. and Crandall, K.A. (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)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, 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)Kowalko, J, Rohner, N, Borowsky, RL and Tabin, C (2011)Esquivel-Bobadilla, S (2011)Jeffery, W.R. (2012)Protas, M. and Jeffery, W. R. (2012)Pazza, R (2013)Bibliowicz, J., Alie, A., Espinasa, L., Yoshizawa, M., Blin, M., Hinaux, H., Legendre, L., Pere, S. and Retaux, S. (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)Gross, J.B., Furterer, A., Carlson, B.M. and Stahl, B.A. (2013)Stahl, B. A. and Gross, J. B. (2013)Stahl, AL (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)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)McGaugh, S. E. (2015)Silva, D. M. Z. A., Utsunomia, R., Pansonato-Alves, J.C., Oliveira, C. and Foresti, F. (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)Rohner, N (2015)Aspiras, Ariel C., Rohner, Nicolas, Martineau, Brian, Borowsky, Richard L. and Tabin, Clifford J. (2015)Bradic, M, Rohner, N, Tabin, C and Borowsky, R. (2015)Stahl, Bethany A. and Gross, Joshua B. (2015)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 (2016)O'Quin, Kelly and McGaugh, Suzanne E. (2016)Casane, D and Retaux, S (2016)Beale, A., Whitmore, D and Moran, D (2016)Rohner, Nicolas (2016)Aspiras, A., Tabin, C. and Rohner, N. (2016)Jaggard, J. B., Robinson, B. G., Stahl, B, Oh, I, Masek, P, Yoshizawa, M and Keene, A. (2017)Wilkens, H. and Strecker, U. (2017)Stahl, B (2017)Stahl, B.A. and Gross, J.B. (2017)Jaggard, J. B. (2017)Hinaux, H, Recher, G, Alie, A., Legendre, L, Blin, M. and Retaux, S (2017)Schmitter-Soto, JJ (2017)Fumey J, Hinaux H, Noirot C, Thermes C, Re´ taux S, Casane D. (2017)Krishnan, J and Rohner, N (2017)Pazza, R., Dergam, J.A. and Kavalco, K.F. (2018)Kling, J. (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)Jaggard, J.B., Stahl, B.A., Lloyd, E., Prober, D.A., Duboue, E.R. and Keene, A.C. (2018)Alie, A., Devos, L., Torres-Paz, J., Prunier, L., Boulet, F., Blin, M., Elipot, Y. and Retaux, S. (2018)Gross, J.B., Weagley, J., Stahl, B.A., Ma, L., Espinasa, L. and McGaugh, S.E. (2018)Elliott, W.R. (2018)Fumey, J., Hinaux, H., Noirot, C., Thermes, C., Rétaux, S. and Casane, D. (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)