TY - JOUR
T1 - Post-ejaculatory modifications to sperm (PEMS)
AU - Pitnick, Scott
AU - Wolfner, Mariana F.
AU - Dorus, Steve
N1 - Funding Information:
We would like to thank Sharleen Buel for technical assistance and Susan Suarez, Kirill Borziak, Ethan Degner, Tim Karr, Erin McCullough, Caitlin McDonough, Jane Pascar, Zeeshan Syed and Emma Whittington for fruitful advice, discussion, bringing relevant literature to our attention, and/or helpful comments on earlier drafts. We are also grateful for the detailed and perceptive comments from two anonymous reviewers. We are especially indebted to the myriad biologists whose curiosity and creative exploration of variation in reproductive systems made this synthesis possible and a joy to write. This work was supported by a generous gift by Mike and Jane Weeden to Syracuse University and by grants from the Eunice Shriver National Institute for Child Health and Human Development (R21-HD088910 to S.D., S.P. and M.F.W. and R01-HD038921 to M.F.W.) and the National Science Foundation (DEB-1655840 to S.D., S.P. and M.F.W.),
Publisher Copyright:
© 2019 Cambridge Philosophical Society
PY - 2020/4/1
Y1 - 2020/4/1
N2 - Mammalian sperm must spend a minimum period of time within a female reproductive tract to achieve the capacity to fertilize oocytes. This phenomenon, termed sperm ‘capacitation’, was discovered nearly seven decades ago and opened a window into the complexities of sperm–female interaction. Capacitation is most commonly used to refer to a specific combination of processes that are believed to be widespread in mammals and includes modifications to the sperm plasma membrane, elevation of intracellular cyclic AMP levels, induction of protein tyrosine phosphorylation, increased intracellular Ca2+ levels, hyperactivation of motility, and, eventually, the acrosome reaction. Capacitation is only one example of post-ejaculatory modifications to sperm (PEMS) that are widespread throughout the animal kingdom. Although PEMS are less well studied in non-mammalian taxa, they likely represent the rule rather than the exception in species with internal fertilization. These PEMS are diverse in form and collectively represent the outcome of selection fashioning complex maturational trajectories of sperm that include multiple, sequential phenotypes that are specialized for stage-specific functionality within the female. In many cases, PEMS are critical for sperm to migrate successfully through the female reproductive tract, survive a protracted period of storage, reach the site of fertilization and/or achieve the capacity to fertilize eggs. We predict that PEMS will exhibit widespread phenotypic plasticity mediated by sperm–female interactions. The successful execution of PEMS thus has important implications for variation in fitness and the operation of post-copulatory sexual selection. Furthermore, it may provide a widespread mechanism of reproductive isolation and the maintenance of species boundaries. Despite their possible ubiquity and importance, the investigation of PEMS has been largely descriptive, lacking any phylogenetic consideration with regard to divergence, and there have been no theoretical or empirical investigations of their evolutionary significance. Here, we (i) clarify PEMS-related nomenclature; (ii) address the evolutionary origin, maintenance and divergence in PEMS in the context of the protracted life history of sperm and the complex, selective environment of the female reproductive tract; (iii) describe taxonomically widespread types of PEMS: sperm activation, chemotaxis and the dissociation of sperm conjugates; (iv) review the occurence of PEMS throughout the animal kingdom; (v) consider alternative hypotheses for the adaptive value of PEMS; (vi) speculate on the evolutionary implications of PEMS for genomic architecture, sexual selection, and reproductive isolation; and (vii) suggest fruitful directions for future functional and evolutionary analyses of PEMS.
AB - Mammalian sperm must spend a minimum period of time within a female reproductive tract to achieve the capacity to fertilize oocytes. This phenomenon, termed sperm ‘capacitation’, was discovered nearly seven decades ago and opened a window into the complexities of sperm–female interaction. Capacitation is most commonly used to refer to a specific combination of processes that are believed to be widespread in mammals and includes modifications to the sperm plasma membrane, elevation of intracellular cyclic AMP levels, induction of protein tyrosine phosphorylation, increased intracellular Ca2+ levels, hyperactivation of motility, and, eventually, the acrosome reaction. Capacitation is only one example of post-ejaculatory modifications to sperm (PEMS) that are widespread throughout the animal kingdom. Although PEMS are less well studied in non-mammalian taxa, they likely represent the rule rather than the exception in species with internal fertilization. These PEMS are diverse in form and collectively represent the outcome of selection fashioning complex maturational trajectories of sperm that include multiple, sequential phenotypes that are specialized for stage-specific functionality within the female. In many cases, PEMS are critical for sperm to migrate successfully through the female reproductive tract, survive a protracted period of storage, reach the site of fertilization and/or achieve the capacity to fertilize eggs. We predict that PEMS will exhibit widespread phenotypic plasticity mediated by sperm–female interactions. The successful execution of PEMS thus has important implications for variation in fitness and the operation of post-copulatory sexual selection. Furthermore, it may provide a widespread mechanism of reproductive isolation and the maintenance of species boundaries. Despite their possible ubiquity and importance, the investigation of PEMS has been largely descriptive, lacking any phylogenetic consideration with regard to divergence, and there have been no theoretical or empirical investigations of their evolutionary significance. Here, we (i) clarify PEMS-related nomenclature; (ii) address the evolutionary origin, maintenance and divergence in PEMS in the context of the protracted life history of sperm and the complex, selective environment of the female reproductive tract; (iii) describe taxonomically widespread types of PEMS: sperm activation, chemotaxis and the dissociation of sperm conjugates; (iv) review the occurence of PEMS throughout the animal kingdom; (v) consider alternative hypotheses for the adaptive value of PEMS; (vi) speculate on the evolutionary implications of PEMS for genomic architecture, sexual selection, and reproductive isolation; and (vii) suggest fruitful directions for future functional and evolutionary analyses of PEMS.
KW - capacitation
KW - female reproductive tract
KW - fertility
KW - hyperactivation
KW - morphogenesis
KW - motility
KW - post-copulatory sexual selection
KW - seminal proteins
KW - sperm competition
KW - spermatozoa
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U2 - 10.1111/brv.12569
DO - 10.1111/brv.12569
M3 - Article
C2 - 31737992
AN - SCOPUS:85075431352
SN - 1464-7931
VL - 95
SP - 365
EP - 392
JO - Biological Reviews
JF - Biological Reviews
IS - 2
ER -