Journal Article

Unique sperm haplotypes are associated with phenotypically different sperm subpopulations in Astyanax fish

Borowsky, R., Luk, A., He, X.J. and Kim, R.S.

Record Number:
4030
Year:
2018
Journal:
BMC Biology
Volume:
16:72
Abstract:
Background: The phenotypes of sperm are generally believed to be under the control of the diploid genotype of the male producing them rather than their own haploid genotypes, because developing spermatids share cytoplasm through intercellular bridges. This sharing is believed to homogenize their content of gene products. However, not all developing spermatids have identical gene products and estimates are that alleles at numerous gene loci are unequally expressed in sperm. This provides scope for the hypothesis that sperm phenotypes might be influenced by their unique haplotypes. Here we test a key prediction of this hypothesis. Results: The haploid hypothesis predicts that phenotypically different sperm subpopulations should be genetically distinct. We tested this by genotyping different sperm subpopulations that were generated by exposing sperm to a chemical dye challenge (Hoechst 33342). Dye treatment caused the cells to swell and tend to clump together. The three subpopulations of sperm we distinguished in flow cytometry corresponded to single cells, and clumps of two or three. Cell clumping in the presence of the dye may reflect variation in cell adhesivity. We found that allelic contents differed among the three populations. Importantly, the subpopulations with clumped sperm cells were significantly enriched in allelic combinations that had previously been observed to have significantly lower transmission success. Conclusions: We show that at least one sperm phenotype is correlated with its haploid genotype. This supports a broader hypothesis that the haploid genotypes of sperm cells may influence their fitness, with potentially significant implications for the transmission of deleterious alleles or combinations of alleles to their offspring. Keywords: Sperm competition, Sib sperm competition, Astyanax mexicanus, Cave fish, Sperm phenotypes
Times Cited:
2
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)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)Thines, G. (1954)Luling, K. H. (1954)Luling, K. H. (1954)Rasquin, P. and Rosenbloom, L. (1954)Stefanelli, A. (1954)Stefanelli, A. (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)Boucquey, C., Thines, G. and Van Der Borght, C. (1965)Thines, G., Wolff-Van Ermengem, F., Boucquey, C. and Soffie, M. (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)Mattheij, J. A. (1968)Wilkens, H. (1968)Mattheij, J. A. (1968)Sadoglu, P. and McKee, A. (1969)Weiss, B. A. (1969)Mattheij, J. A. (1969)Mattheij, J. A. and Sprangers, J. A. P. (1969)Gertychowa, R. (1970)Gertychowa, R. (1970)Weiss, B. and Martini, J. (1970)Popper, A. N. (1970)Whitt, G. S. and Maeda, F. S. (1970)Wilkens, H. (1970)Wilkens, H. (1970)Wilkens, H. (1970)Mattheij, J. A. (1970)Mattheij, J. A. (1970)Gertychowa, R. (1971)Popper, A. N. (1971)Wiley, S. and Mitchell, R. W. (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)Wilkens, H. (1972)Zaccone, G. (1972)Thines, G. and LeGrain, J. M. (1973)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)Zeitlin, S. M. and McDevitt, D. S. (1973)Schemmel, C. (1974)Schemmel, C. (1974)Chakraborty, R. and Nei, M. (1974)Sligar, C. (1974)Sadoglu, P. (1975)Peters, N., Scholl, A. and Wilkens, H. (1975)Omura, Y. (1975)Erckens, W. and Weber, F. (1976)Herwig, H. J. (1976)Voneida, T. J. and Sligar, C. (1976)Herwig, H. J. (1976)Sligar, C. and Voneida, T. J. (1976)Wilkens, H. (1976)Durand, J. P. (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)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)Herwig, H. J. (1981)Campenhausen, C., Riess, I. and Weissert, R. (1981)Weissert, R. and Campenhausen, C. (1981)Reddell, J. R. (1981)Erckens, W. and Martin, W. (1982)Erckens, W. and Martin, W. (1982)Jankowska, M. and Thines, G. (1982)Tabata, M. (1982)Lamprecht, G. and Weber, F. (1982)Rose, F. L. and Mitchell, R. W. (1982)Parzefall, J. (1983)Romero, A. (1983)Zilles, K., Tillmann, B. and Bennemann, R. (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. (1986)Parzefall, J. (1986)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)Espinasa, L (1986)Wilkens, H. (1987)Huppop, K. (1987)De Fraipont, M. (1987)De Fraipont, M. (1987)Wilkens, H. (1988)Huppop, K. (1988)De Fraipont, M. (1988)Teyke, T. (1988)Fricke, D. (1988)Fricke, D. and Parzefall, J. (1989)Hassan, E. S. (1989)Huppop, K. (1989)Teyke, T. (1989)Fack, H. and Wilkens, H. (1989)Langecker, T. G. (1989)Langecker, T. G. (1990)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., 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)Langecker, T. G. and Longley, G. (1992)Wilkens, H. (1992)Parzefall, J. (1992)Parzefall, J. (1992)Hassan, E. S., Abdel-Latif, H. and Biebricher, R. (1992)Wilkens, H. and Meyer, M. (1992)De Fraipont, M. (1992)Lamprecht, G. and Weber, F. (1992)Langecker, T. G. (1993)Langecker, T. G., Schmale, H. and Wilkens, H. (1993)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)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)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)Wilkens, H. (1998)Contreras-Balderas, S. and Lozano-Vilano, M.D.L. (1998)Jeffery, WR and Martasian, DP (1998)Behrens, M, Wilkens, H and Schmale, H (1998)Baker, CF and Montgomery, J (1999)Kullander, S. O. (1999)Ford, D.C. (2000)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)Boudriot, F and Reutter, K (2001)Espinasa, L., Rivas-Manzano, P. and Perez, H.E. (2001)Jeffery, W. R. (2001)Strickler, A.G., Yamamoto, Y. and Jeffery, W. R. (2001)Espinasa, L. and Borowsky, R. (2001)Montgomery, J.C., Coombs, S. and Baker, C.F. (2001)Borowsky, RL and Wilkens, H (2002)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)Sarma, SSS, Lopez-Romulo, A and Nandini, S (2003)Porter, M.L. and Crandall, K.A. (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)Mirande, J.M. (2010)Yamamoto, Y. and Jeffery, W.R. (2011)Kish, P.E., Bohnsack, B.L., Gallina, D., Kasprick, D.S. and Kahana, A. (2011)Espinasa, L (2011)Esquivel-Bobadilla, S (2011)Kowalko, J, Rohner, N, Borowsky, RL and Tabin, C (2011)Bradic, M, Beerli, P and Borowsky, RL (2011)Esquivel-Bobadilla, S (2011)Wilkens, H. (2012)Jeffery, W.R. (2012)Trontelj, P. (2012)Protas, M. and Jeffery, W. R. (2012)Dufton, M, Hall, BK and Franz-Odendaal, T. (2012)Gross, J.B. (2012)Bradic, M., Beerli, P., Garcia-de Leon, F. J., Esquivel-Bobadilla, S. and Borowsky, R. L. (2012)Idda, M.L., Bertolucci, C., Vallone, D., Gothilf, Y., Sánchez-Vázquez, F.J. and Foulkes N.S. (2012)Pazza, R (2013)Pazza, R (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)Bibliowicz, J., Alie, A., Espinasa, L., Yoshizawa, M., Blin, M., Hinaux, H., Legendre, L., Pere, S. and Retaux, S. (2013)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)Moran, D., Softley, R. and Warrant, E.J. (2014)Gross, J.B., Krutzler, A.J. and Carlson, B.M. (2014)Atukorallaya, D. and Franz-Odendaal, T. (2014)Atukorala, A. D. S. and Franz-Odendaal, T. A. (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)Elliott, W.R. (2014)Moran, D., Softley, R. and Warrant, E.J. (2015)Silva, D. M. Z. A., Utsunomia, R., Pansonato-Alves, J.C., Oliveira, C. and Foresti, F. (2015)Silva, D. M. Z. A., Utsunomia, R., Pansonato-Alves, J.C., Oliveira, C. and Foresti, F. (2015)Carlson, B.M., Onusko, S.W. and Gross, J.B. (2015)Stahl, Bethany A. and Gross, Joshua B. (2015)Dufton, Megan and Franz-Odendaal, Tamara A. (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)Hinaux, H., Blin, M., Fumey, J., Legendre, L., Heuze, A., Casane, D. and Retaux, S. (2015)Jaggard, J. B. (2015)McGaugh, S. E. (2015)Fumey, J. (2015)Devos, Lucie, Alie, A. and Retaux, S (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)Rohner, N (2015)Caballero-Hernandez, O., Hernandez-Patricio, M., Sigala-Regalado, I., Morales-Malacara, J. B. and Miranda-Anaya, M. (2015)Stemmer, Manuel, Schuhmacher, Laura-Nadine, Foulkes, Nicholas S., Bertolucci, Cristiano and Wittbrodt, Joachim (2015)Casane, D. and Retaux, S. (2016)Aspiras, A., Tabin, C. and Rohner, N. (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)Keene, A.C., Yoshizawa, M. and McGaugh, S.E. (2016)Atukorala, A. D. S. and Franz-Odendaal, Tamara A. (2016)Gross, J.B., Stahl, B.A., Powers, A.K. and Carlson, B.M. (2016)Schmitter-Soto, JJ (2016)Schmitter-Soto, JJ (2016)O'Quin, Kelly and McGaugh, Suzanne E. (2016)Retaux, S., Alie, A., Blin, M., Devos, L., Elipot, Y. and Hinaux, H. (2016)Yoshizawa, M., Settle, A., Macaspac, C., Fernandes, V. Yoshida, M. and Keene, A. (2016)Rohner, Nicolas (2016)Krishnan, J and Rohner, N (2017)Torres-Paz, J (2017)Alvarado, C.G. (2017)Wilkens, H. and Strecker, U. (2017)Jaggard, J. B., Robinson, B. G., Stahl, B, Oh, I, Masek, P, Yoshizawa, M and Keene, A. (2017)Schmitter-Soto, JJ (2017)Stahl, B (2017)Schmitter-Soto, JJ (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)Kaplan, S.A., Powers, A.K. and Gross, J.B. (2017)Jaggard, J. B. (2017)Fumey J, Hinaux H, Noirot C, Thermes C, Re´ taux S, Casane D. (2017)Hinaux, H, Recher, G, Alie, A., Legendre, L, Blin, M. and Retaux, S (2017)Yoshizawa, M (2017)Devitsina, G.V. and Golovkina, T.V. (2018)Espinasa, L., Legendre, L., Fumey, J., Blin, M., Rétaux, S. and Espinasa, M. (2018)Mirande, J.M. (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)Kopp, J., Avasthi, S. and Espinasa, L. (2018)Rohner, N. (2018)Torres-Paz,J., Hyacinthe, C., Pierre, C., Retaux, S. (2018)Mirande, J.M. (2018)Fumey, J., Hinaux, H., Noirot, C., Thermes, C., Rétaux, S. and Casane, D. (2018)Borowsky, R. (2018)Ojha, A. and Watve, M. (2018)Tabin, J.A., Aspiras, A., Martineau, B., Riddle, M., Kowalko, J. Borowsky, R. Rohner, N. and Tabin, C.J. (2018)Gore, A., Jeffery, W., Retaux, S. and Rohner, N. (2018)Pazza, R., Dergam, J.A. and Kavalco, K.F. (2018)Borowsky, R., Luk, A., He, X.J. and Kim, R.S. (2018)Gore, A.V., Rohner, N., Rétaux, S. and Jeffery, W.R. (2018)Pazza, R., Dergam, J.A. and Kavalco, K.F. (2018)Carlson, B.M., Klingler, I.B., Meyer, B.J. and Gross, J.B. (2018)Borowsky, R., Luk, A., He, X.J. and Kim, R.S. (2018)Ma, L., Strickler, A.G., Parkhurst, A., Yoshizawa, M., Shi, J. and Jeffery, W.R. (2018)Ren, X.Y., Hamilton, N., Müller, F. and Yamamoto, Y. (2018)Garita-Alvarado, C.A., Barluenga, M. and Ornelas-García, C.P. (2018)Kling, J. (2018)Devitsina, G.V. and Golovkina, T.V. (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)Stern, D.B and Crandall, K.A. (2018)Xiong, S., Krishnan, J., Peuß, F. and Rohner, N. (2018)Devi, A., Atukorala, S. and Franz-Odendaal, T.A. (2018)Retaux, S. (2018)Espinasa, L. (2018)Blin, M., Tine, E., Meister, L., Elipot, Y., Bibliowicz, J., Espinasa, L. and Rétaux, S. (2018)Powers, A.K., Kaplan, S.A., Boggs, T.E. and Gross, J. (2018)Jaggard, J.B., Stahl, B.A., Lloyd, E., Prober, D.A., Duboue, E.R. and Keene, A.C. (2018)Carlson, B.M. and Gross, J.B. (2018)Gross, J.B., Weagley, J., Stahl, B.A., Ma, L., Espinasa, L. and McGaugh, S.E. (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)Alie, A., Devos, L., Torres-Paz, J., Prunier, L., Boulet, F., Blin, M., Elipot, Y. and Retaux, S. (2018)Yoshizawa, M., Settle, A., Hermosura, M.C., Tuttle, L.J., Cetraro, N., Passow, C.N. and McGaugh, S.E. (2018)Elliott, W.R. (2018)Fernandes, V.F.L., Macaspac, C., Lu, L. and Yoshizawa, M. (2018)Elliott, W.R. (2018)Espinasa, L. (2018)