Sperm Digestion and Reciprocal Sperm Transfer Can Drive Hermaphrodite Sex Allocation to Equality

Abstract

The intensity of sperm competition determines how much reproductive effort should be invested in sperm. One important factor affecting sperm competition in internally fertilizing organisms is the mating frequency of females, since it determines the extent of competition between ejaculates. In simultaneous hermaphrodites, energy spent on sperm has to be traded off against energy expended on ova production. By extending an existing model, we consider how the number of matings affects sperm competition and, thus, sex allocation in internally fertilizing simultaneous hermaphrodites. We then go on to explore the consequences of two common characteristics of hermaphroditic mating systems, namely, sperm digestion and reciprocal insemination. Since sperm digestion reduces the competitive ability of a given ejaculate, it selects for increased sperm investment. As a result, the amount of sperm digested and male allocation can enter a coevolutionary cycle in which both will increase up to the point of equal investment in male and female gametes and in high rates of digestion. Because of this high degree of sperm digestion, fitness through the male function becomes more dependent on the amount of resources invested in sperm than on the number of matings. As a result, sperm digestion reduces Bateman's principle. Hence, hermaphrodites with sperm digestion should be less likely to display traits that increase the number of matings. Once ejaculates are large and costly, animals insisting on reciprocal sperm transfer will be favored since they receive some compensation for their investment. Under reciprocity, an even higher investment in sperm is favored. This is the result of the compensation received in the form of the partner's ejaculate and a nuptial gift effect by increasing a partner's production of eggs.

Brainless but not clueless: earthworms boost their ejaculates when they detect fecund non-virgin partners

“…These results indicate that they may regulate the duration of copulation or, alternatively, that they may have mechanisms that prevent all sperm being released in a single mating event. Although we did not find sperm depletion after two consecutive ejaculations, the prudent sperm allocation shown by redworms is in line with the models suggesting non-trivial costs of ejaculate production (Greeff & Michiels 1999b).…”

“…However, interestingly, the volume of sperm donated to non-virgin partners was more variable than that transferred to virgin recipients. This variability may indicate that under high sperm competition intensity, resource allocation to sperm may become expensive (Greeff & Michiels 1999b), and sperm donors become more selective about to whom they donate sperm (Michiels et al 2003). To test this prediction, we examined the relationship between sperm volume donated and partner quality, estimated as body mass.…”

Sex allocation and investment into pre- and post-copulatory traits in simultaneous hermaphrodites: the role of polyandry and local sperm competition

“…Sperm digestion may be indiscriminate with respect to sperm donor identity, and may primarily serve to remove-and possibly gain resources from-superfluous sperm that have been received as a result of a mutual willingness to mate. It is important to note, however, that there currently exist no data in support of the notion that sperm digestion occurs at a net energetic benefit to the digesting individual, as is often assumed [69,71]. Instead, sperm digestion could occur at a net energetic loss to the digesting individual, while still being beneficial in terms of fitness returns, because it reduces potential harm imposed by, for example, polyspermy [72] or manipulative substances (see §5d).…”

Intra-locus sexual conflict and sexually antagonistic genetic variation in hermaphroditic animals

“…Total absolute fitness will be the sum of offspring output from each sex role, and total relative fitness will then be total offspring output relative to the population mean [25]. Whole-organism relative fitness will be the mean of the relative fitnesses from each sex role, assuming each role is played equally often (in simultaneous hermaphrodites [25,41]) or the time spent as male and as female is equal (in sequential hermaphrodites). What is interesting here is that the same relative total fitness can be achieved in different ways.…”