Journal Article

Maternal genetic effects in Astyanax cavefish development

Ma, L., Strickler, A.G., Parkhurst, A., Yoshizawa, M., Shi, J. and Jeffery, W.R.

Record Number:
4122
Year:
2018
Journal:
Developmental Biology
Pages:
209-220
Volume:
441
Abstract:
The role of maternal factors in the evolution of development is poorly understood. Here we describe the use of reciprocal hybridization between the surface dwelling (surface fish, SF) and cave dwelling (cavefish, CF) morphs of the teleost Astyanax mexicanus to investigate the roles of maternal genetic effects in cavefish development. Reciprocal hybridization, a procedure in which F1 hybrids are generated by fertilizing SF eggs with CF sperm (SF × CF hybrids) and CF eggs with SF sperm (CF × SF hybrids), revealed that the CF degenerative eye phenotype showed maternal genetic effects. The eyes of CF × SF hybrids resembled the degenerate eyes of CF in showing ventral reduction of the retina and corresponding displacement of the lens within the optic cup, a smaller lens and eyeball, more lens apoptosis, a smaller cartilaginous sclera, and lens-specific gene expression characteristics compared to SF × CF hybrids, which showed eye and lens gene expression phenotypes resembling SF. In contrast, reciprocal hybridization failed to support roles for maternal genetic effects in the CF regressive pigmentation phenotype or in CF constructive changes related to enhanced jaw development. Maternal transcripts encoded by the pou2f1b, runx2b, and axin1 genes, which are involved in determining ventral embryonic fates, were increased in unfertilized CF eggs. In contrast, maternal mRNAs encoded by the ßcatenin and syntabulin genes, which control dorsal embryonic fates, showed similar expression levels in unfertilized SF and CF eggs. Furthermore, maternal transcripts of a sonic hedgehog gene were detected in SF and CF eggs and early cleaving embryos. This study reveals that CF eye degeneration is controlled by changes in maternal factors produced during oogenesis and introduces A. mexicanus as a model system for studying the role of maternal changes in the evolution of development.
Times Cited:
1
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(1964)Thines, G., Wolff-Van Ermengem, F., Boucquey, C. and Soffie, M. (1965)Boucquey, C., Thines, G. and Van Der Borght, C. (1965)Thines, G., Soffie, M. and Vandenbussche, E. (1966)Peters, N. and Peters, G. (1966)Carmignani, M. P. A. (1966)Cavicchioli, G. and Guarnieri, P. (1966)Reed, M. (1966)Sadoglu, P. (1967)Schemmel, C. (1967)Walters, V. and Liu, R. K. (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)Mattheij, J. A. and Sprangers, J. A. P. (1969)Sadoglu, P. and McKee, A. (1969)Weiss, B. A. (1969)Mattheij, J. A. (1969)Mattheij, J. A. (1970)Mattheij, J. A. (1970)Weiss, B. and Martini, J. (1970)Gertychowa, R. (1970)Whitt, G. S. and Maeda, F. S. (1970)Gertychowa, R. (1970)Popper, A. N. (1970)Wilkens, H. (1970)Wilkens, H. (1970)Wilkens, H. (1970)Wiley, S. and Mitchell, R. W. (1971)Gertychowa, R. (1971)Popper, A. N. (1971)Wiley, S. and Mitchell, R. W. (1971)Wilkens, H. (1971)Zaccone, G. (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)Zaccone, G. (1972)Wilkens, H. (1972)Thines, G. and LeGrain, J. M. (1973)Voneida, T. J. (1973)Schemmel, C. (1973)Yasuda, K. (1973)Zeitlin, S. M. (1973)Durand, J. P. (1973)Zeitlin, S. M. and McDevitt, D. S. (1973)Mitchell, R. W. (1973)Schemmel, C. (1974)Schemmel, C. (1974)Chakraborty, R. and Nei, M. (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)Sligar, C. and Voneida, T. J. (1976)Herwig, H. J. (1976)Herwig, H. J. (1976)Wilkens, H. (1976)Durand, J. P. (1976)Erckens, W. and Weber, F. (1976)Kirby, R. F., Thompson, K. W. and Hubbs, C. (1977)Yew, D. T. and Yoshihara, H. M. (1977)Zaccone, G. (1977)Wilkens, H. (1977)Mitchell, R. W., Russell, W. H. and Elliott, W. R. (1977)Thines, G. and Weyers, M. (1978)Durand, J. P. (1978)Sadoglu, P. (1979)Wilkens, H., Peters, H. and Schemmel, C. (1979)Woodhead, A. D. and Achey, P. M. (1979)Durand, J. P. (1979)Schemmel, C. (1980)Weissert, R. (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)Reddell, J. R. (1981)Herwig, H. J. (1981)Jankowska, M. and Thines, G. (1982)Lamprecht, G. and Weber, F. (1982)Tabata, M. (1982)Erckens, W. and Martin, W. (1982)Erckens, W. and Martin, W. (1982)Rose, F. L. and Mitchell, R. W. (1982)Parzefall, J. (1983)Romero, A. (1983)Zilles, K., Tillmann, B. and Bennemann, R. (1983)Schuppa, M. (1984)Voneida, T. J. and Fish, S. E. (1984)Romero, A. (1984)Romero, A. (1984)Wilkens, H. (1984)Burchards, H., Dolle, A. and Parzefall, J. (1985)Lamprecht, G. and Weber, F. (1985)Teyke, T. (1985)Romero, A. (1985)Wilkens, H. (1985)Parzefall, J. (1986)Wilkens, H. and Huppop, K. (1986)De Fraipont, M. (1986)Fraipont, M. (1986)Hassan, E. S. (1986)De Fraipont, M. and Thines, G. (1986)De Fraipont, M. and Thines, G. (1986)Huppop, K. (1986)Romero, A. (1986)Wilkens, H. (1986)Wilkens, H. (1987)De Fraipont, M. (1987)De Fraipont, M. (1987)Huppop, K. (1987)Wilkens, H. (1988)Fricke, D. (1988)De Fraipont, M. (1988)Teyke, T. (1988)Huppop, K. (1988)Fack, H. and Wilkens, H. (1989)Langecker, T. G. (1989)Fricke, D. and Parzefall, J. (1989)Hassan, E. S. (1989)Teyke, T. (1989)Huppop, K. (1989)Klimpel, B. and Parzefall, J. (1990)Parzefall, J. and Fricke, D. (1990)Peters, N., Schmidt, W. and Fricke, D. (1990)Langecker, T. G. (1990)Abdel-Latif, H., Hassan, E. S. and von Campenhausen, C. (1990)Yokoyama, R. and Yokoyama, S. (1990)Yokoyama, R and Yokoyama, S (1990)Teyke, T. (1990)Huppop, K. (1991)Parzefall, J. and Fricke, D. (1991)Campenhausen, C. (1991)Langecker, T. G., Wilkens, H. and Junge, P. (1991)Riedel, G. and Krug, L. (1991)Huppop, K. and Wilkens, H. (1991)Wilkens, H. (1992)Parzefall, J. (1992)Parzefall, J. (1992)Wilkens, H. and Meyer, M. (1992)Lamprecht, G. and Weber, F. (1992)Langecker, T. G. and Longley, G. (1992)Hassan, E. S., Abdel-Latif, H. and Biebricher, R. (1992)De Fraipont, M. (1992)Parzefall, J. (1993)Peters, N., Schacht, V., Schmidt, W. and Wilkens, H. (1993)Langecker, T. G. (1993)Langecker, T. G., Schmale, H. and Wilkens, H. (1993)Langecker, T. G., Schmale, H. and Wilkens, H. (1993)Hoffman, S. and Hausberg, C. (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)Wilkens, H. (1998)Jeffery, WR and Martasian, DP (1998)Behrens, M, Wilkens, H and Schmale, H (1998)Contreras-Balderas, S. and Lozano-Vilano, M.D.L. (1998)Kullander, S. O. (1999)Baker, CF and Montgomery, J (1999)Espinasa, L. and Borowsky, R. (2000)Jeffery, W. R., Strickler, A.G., Guiney, S., Heyser, D.G. and Tomarev, S.I. (2000)Yamamoto, Y. and Jeffery, W. R. (2000)Ford, D.C. (2000)Espinasa, L. and Borowsky, R. (2001)Jeffery, W. R. (2001)Strickler, A.G., Yamamoto, Y. and Jeffery, W. R. (2001)Boudriot, F and Reutter, K (2001)Montgomery, J.C., Coombs, S. and Baker, C.F. (2001)Romero, A., Jeffery, W.R. and Yamamoto, Y. (2002)Berg, A. and Watson, G.M. (2002)Dowling, TE, Martasian, DP and Jeffery, WR (2002)Strickler, AG, Famuditimi, K and Jeffery, WR (2002)Krejca, J. (2002)Borowsky, RL and Wilkens, H (2002)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)Porter, M.L. and Crandall, K.A. (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)Salin, K, Voituron, Y, Colson, C and Hervant, F (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)Esquivel-Bobadilla, S (2011)Kowalko, J, Rohner, N, Borowsky, RL and Tabin, C (2011)Bradic, M, Beerli, P and Borowsky, RL (2011)Salin, K, Voituron, Y, Mourin, J and Hervant, F (2011)Yamamoto, Y. and Jeffery, W.R. (2011)Kish, P.E., Bohnsack, B.L., Gallina, D., Kasprick, D.S. and Kahana, A. (2011)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)Hervant, F. (2012)Wilkens, H. (2012)Trontelj, P. (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)Jeffery, W.R. (2012)Beale, A., Guibal, C., Tamai, T. K., Klotz, L., Cowen, S., Peyric, E., Reynoso, V. H., Yamamoto, Y. and Whitmore, D. (2013)Elliott, William R. (2013)Beale, 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)Bradic, M., Teotonio, H. and Borowsky, R. L. 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