Sperm Competition and the Evolution of Nonfertilizing Sperm in Mammals

Abstract

Nonfertilizing sperm with special morphologies have long been known to exist in invertebrates. Until recently, abnormal sperm in mammals were considered errors in production. Now, however, Baker and Bellis (1988, 1989) have proposed that mammalian sperm, like some invertebrate sperm, are polymorphic and adapted to a variety of nonfertilizing roles in sperm competition, including prevention of passage of sperm inseminated by another male. More specifically, their "kamikaze" sperm hypothesis proposes that deformed mammalian sperm are adapted to facilitate the formation and functioning of copulatory plugs (Baker and Bellis, 1988). Here I argue that most, maybe all, mammals are unlikely to produce nonfertilizing sperm. First, mammals might not be able to afford to evolve nonfertilizing sperm, given that a) fertilization is often unlikely despite the huge numbers of sperm produced; b) production of larger numbers of sperm is constrained, presumably because of metabolic costs, evidence for which includes the fact that in species in which sperm morphology and anatomy of the female reproductive tract increase the probability of fertilization, the numbers of sperm produced is lower than in others; and c) selection appears to act against the production of deformed sperm. Second, some of the evidence advanced for the existence of nonfertilizing sperm does not in fact support the idea. Third, accessory gland secretions are sufficient on their own to coagulate semen and produce fully functioning plugs; thus the male that used accessory gland secretions would be at a clear advantage over the male that diluted his fertilizing sperm with "kamikaze" sperm; and indeed, current evidence indicates selection on accessory glands, not sperm morphology, to enhance coagulation of semen. Fourth, predictions made on the basis of the "kamikaze" sperm hypothesis are not supported by quantitative comparisons of data from polyandrous and monandrous primates (i.e., those in which several males mate with a fertile female, and therefore in which sperm competition should be operating, and those in which only one male mates). Although sperm competition is almost certainly more intense in polyandrous genera than in monandrous genera (as indicated by, e.g., more frequent copulations and the production of more sperm per ejaculate from larger spermatogenic organs), polyandrous genera do not produce a greater proportion of deformed (i.e., nonfertilizing) sperm than do monandrous genera, or even necessarily a greater number of deformed sperm; nor a greater variety of sperm sizes-indeed they might produce fewer; nor fewer motile sperm (as might be expected if sperm are selected to stay behind and compete with sperm from subsequent males); and nor larger sperm (as might be expected if sperm are produced for functions other than to reach the egg). In sum, currently available evidence suggests that the function of all mammalian sperm is to fertilize, and that sperm competition in mammals occurs through scramble competition, not contest competition.

Relative testis size and sperm morphometry across mammals: no evidence for an association between sperm competition and sperm length

“…Gomendio & Roldan (1991) found that sperm size was greater in primate and rodent taxa that generated higher risks of sperm competition. By contrast, Harcourt (1991) and Dixson (1998) found no evidence for a relationship between sperm size and mating pattern across primates, although Dixson (1993) found some evidence for a positive relationship between relative testis size and sperm length across 15 primate species but suggested caution interpreting these results and did not control for Proc. R. Soc.…”

Gamete plasticity in a broadcast spawning marine invertebrate

“…In contrast, tests of predicted changes in sperm quality have yielded mixed results (7,14). Interspecific comparisons show that sperm size can increase (15)(16)(17), decrease (18), or have no relationship (19)(20)(21)(22) with increased risk of sperm competition-with some studies of the same taxonomic groups producing conflicting results (reviewed in ref. 7).…”

Mechanisms Underlying the Sperm Quality Advantage in Drosophila Melanogaster

“…Second, selection lines of C. elegans evolved larger sperm in response to experimentally increased levels of sperm competition (LaMunyon and Ward 2002), and males from lines of the fruit fly, D. melanogaster, experimentally selected to have longer sperm demonstrated enhanced competitive fertilization success (Miller and Pitnick 2002; but see Gage and Morrow 2003, discussed in detail below). Third, comparative studies of a diverse array of taxa have found a significant positive relationship between sperm length and the risk or intensity of sperm competition (mammals: Gomendio and Roldan 1991;primates: Dixson 1993;birds: Briskie and Montgomerie 1992;Briskie et al 1997;Johnson and Briskie 1999;butterflies: Gage 1994; nematodes: LaMunyon and Ward 1999; moths: Morrow and Gage 2000; cichlid fish: Balshine et al 2001;frogs: Byrne et al 2003;rodents: Breed 2004; but for exceptions see Stockley et al 1997 on fish andHarcourt 1991;Hosken 1997;Anderson and Dixson 2002;Gage and Freckleton 2003 on mammals, discussed in detail below). Fourth, comparative studies on diverse taxa have found significant correlated evolution between sperm length and dimensions of some critical region of the female reproductive tract (featherwing beetles: Dybas and Dybas 1981;birds: Briskie and Montgomerie 1993;fruit flies: Pitnick et al 1999fruit flies: Pitnick et al , 2003stalk-eyed flies: Presgraves et al 1999;moths: Morrow and Gage 2000;dung flies: Minder et al 2005; but for megachiropteran bats see Hosken 1998).…”