Local Gamete Competition Explains Sex Allocation and Fertilization Strategies in the Sea

Abstract

Within and across taxa, there is much variation in the mode of fertilization, that is, whether eggs and/or sperm are released or kept inside or on the surface of the parent's body. Although the evolutionary consequences of fertilization mode are far-reaching, transitions in the fertilization mode itself have largely escaped theoretical attention. Here we develop the first evolutionary model of egg retention and release, which also considers transitions between hermaphroditism and dioecy as well as egg size evolution. We provide a unifying explanation for reported associations between small body size, hermaphroditism, and egg retention in marine invertebrates that have puzzled researchers for more than 3 decades. Our model, by including sperm limitation, shows that all these patterns can arise as an evolutionary response to local competition between eggs for fertilization. This can provide a general explanation for three empirical patterns: sperm casters tend to be smaller than related broadcast spawners, hermaphroditism is disproportionately common in sperm casters, and offspring of sperm casters are larger. Local gamete competition also explains a universal sexual asymmetry: females of some species retain their gametes while males release theirs, but the opposite ("egg casting") lacks evolutionary stability and is apparently not found in nature.

The evolution of expenditure on testes

“…Henshaw et al . () differentiate between two forms of broadcast spawning in marine invertebrates: that where only sperm are released (‘sperm casting’) and that where both eggs and sperm are released (for which Henshaw et al . reserve the term broadcast spawning).…”

An Organismal Perspective on the Evolution of Insect Societies

“…Organisms also vary widely in how the fertilization occurs, i.e., whether both types of gametes are released into the environment (broadcast spawning or external fertilization), or whether fertilization occurs internally through sperm casting (i.e., that sperm disperse, eggs don't) or mating (Henshaw et al, 2014). If insect societies are seen as hermaphroditic sessile organisms, at least one type of gametes, queens or males, needs to leave the colony for a non-selfing fertilization to take place, and direct mating with internal fertilization between two superorganisms is not an option.…”

“…In plants, sperm/pollen casting is dominant, although the evolutionary reasons for absence of cases where both gametes disperse are not well understood (Fromhage and Kokko, 2010;Henshaw et al, 2014). Patterns of variation described in marine invertebrates show that in general, sperm casting goes with small size (Strathmann and Strathmann, 1982), sperm casters are predominantly hermaphrodites and have larger offspring than broadcast spawners (Kupriyanova et al, 2001).…”

“…Patterns of variation described in marine invertebrates show that in general, sperm casting goes with small size (Strathmann and Strathmann, 1982), sperm casters are predominantly hermaphrodites and have larger offspring than broadcast spawners (Kupriyanova et al, 2001). Recent theory explains this in the light of local gamete competition (Henshaw et al, 2014): if gamete availability is limiting for reproduction, large individuals should release both gametes if their fecundity increases faster than sperm availability for retained gametes, and gamete limitation causes diminishing returns for female production, favoring hermaphroditism.…”

“…Note that the same proviso applies to mating in the nest as an analog of selfing. Second, gamete limitation might not be an important selection pressure for many social insects since intra-nest mating is common in polygynous social insects (the model of Henshaw et al, 2014 assumed absence of selfing), intra-nest mating might not even result in significant inbreeding in genetically diverse societies, and even a complete lack of mating would not prevent a queen from reproduction since they can still produce males. Furthermore, as all social insect nests are potentially simultaneous hermaphrodites, no correlations can be found with respect to hermaphroditism and fertilization strategies.…”