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Post‐Ejaculatory Modifications to Sperm (PEMS)

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Post‐Ejaculatory Modifications to Sperm (PEMS) Biol. Rev. (2020), 95, pp. 365–392. 365 doi: 10.1111/brv.12569 Post-ejaculatory modifications to sperm (PEMS) Scott Pitnick1∗ , Mariana F. Wolfner2 and Steve Dorus1 1Department of Biology, Center for Reproductive Evolution, Syacuse University, Syracuse, NY 13244, USA 2Department of Molecular Biology and Genetics, Cornell University, Ithaca, NY 14853, USA ABSTRACT 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. Key words: spermatozoa, morphogenesis, capacitation, hyperactivation, motility, seminal proteins, female reproductive tract, post-copulatory sexual selection, sperm competition, fertility. CONTENTS I. Introduction .............................................................................................. 366 II. Defining PEMS and suggested nomenclature ............................................................ 367 III. Elements of the life history of sperm ...................................................................... 368 (1) Sperm maturation rarely ends in the testes ........................................................... 368 (2) The female reproductive tract is a complex, interactive and selective environment .................. 369 IV. Taxonomically widespread forms of PEMS .............................................................. 370 (1) Sperm activation and chemotaxis .................................................................... 370 (2) Dissociation of sperm conjugates ..................................................................... 370 * Author for correspondence (Tel.: +315 443 5128; E-mail: [email protected]). Biological Reviews 95 (2020) 365–392 © 2019 Cambridge Philosophical Society 366 Scott Pitnick and others V. A survey of PEMS throughout the kingdom Animalia ................................................... 371 VI. Hypotheses for the adaptive significance of PEMS ....................................................... 372 (1) H1: economy of sperm transfer ....................................................................... 375 (2) H2: protecting sperm from stress during transfer and storage ........................................ 375 (3) H3: aiding sperm reaching a critical location in the FRT ............................................ 375 (4) H4: aiding sperm to remain in a critical location in the FRT ......................................... 376 (5) H5: enhancing sperm longevity ...................................................................... 376 (6) H6: delivering male-derived materials to the female in a temporally and/or spatially critical manner 376 (7) H7: priming sperm for extragenic contributions to early embryogenesis ............................. 378 (8) H8: female assessment of sperm quality .............................................................. 379 VII. Evolutionary implications of PEMS ...................................................................... 380 (1) Genomic consequences of PEMS ..................................................................... 380 (2) PEMS and sexual selection ........................................................................... 380 (3) PEMS and reproductive isolation .................................................................... 382 VIII. Future directions ......................................................................................... 382 IX. Conclusions .............................................................................................. 384 X. Acknowledgments ........................................................................................ 384 XI. References ................................................................................................ 384 XII. Supporting Information .................................................................................. 392 I. INTRODUCTION (Roldan & Gomendio, 2009) may not have been possible (Visconti, 2009). Between the 1870s and the 1950s, numerous research Capacitation in mammals has subsequently been inves- programs employed an in vitro approach to the study of tigated intensively [see online Supporting Information, fertilization in echinoderms, amphibians and mammals. Appendix S1 (Section VII.5); Gervasi & Visconti, 2016]. The These studies were fruitful in elucidating, for example, term is now used widely to refer to a combination of cellular processes that include specific molecular modifications to the interactions between sperm and eggs, and between sperm and + the cumulus cells surrounding the egg in mammals. However, sperm plasma membrane, increased Ca2 permeability, the and despite numerous erroneous claims to the contrary elevation of intracellular cyclic AMP levels, hyperactivation (reviewed by Austin, 1951; but see Moricard, 1950 as of motility, the induction of sperm protein tyrosine phospho- discussed in Austin, 1951), the goal of achieving fertilization rylation and, eventually, the acrosome reaction (Vadnais, in vitro in a mammal was stymied. The breakthrough came Galantino-Homer, & Althouse, 2007; Gadella & Boerke, in a pair of studies published by C. R. ‘Bunny’ Austin 2016; Gervasi & Visconti, 2016). These modifications occur and Min Chueh Chang in 1951. Working with rabbits naturally within the FRT, but can also be induced in vitro. and rats, and seemingly inspired by previous investigations Although capacitation is frequently suggested to be exclusive of the timing of fertilization relative to insemination (i.e. to mammals, evidence suggests that this phenomenon is more delays were not attributable to the time required by sperm taxonomically widespread (e.g. Nixon et al., 2016a, 2019b). to reach the site of fertilization, nor for large numbers of This point depends in part, of course, on the definition of sperm to accumulate there; e.g. Hammond, 1934) both ‘capacitation’. Numerous reports in the literature describe Austin (1951) and Chang (1951) showed that sperm must an array of post-ejaculatory modifications to sperm (PEMS) spend some minimum threshold amount of time within occurring in the FRT in a diversity of internally fertilizing the female reproductive tract (FRT) before fertilization can taxa, of which capacitation as described for mammals repre- occur. Specifically, sperm introduced into the periovarian sac sents but one example. Because there is no cohesive field of of the rat or the Fallopian tubes of the rabbit required several study encompassing such modifications, the descriptions are hours to lapse before fertilization was observed (Austin, mostly anecdotal and lack consistent nomenclature. Never- 1951; Chang, 1951). However, fertilization occurred swiftly theless, there is cause to postulate that critical modifications and efficiently if sperm had first spent 5 h within the uterus of to sperm within the FRT are the rule rather than the excep- another rabbit (Chang, 1951). Both authors
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