The evolution of anisogamy: a game-theoretic approach

Abstract

A popular theory has proposed that anisogamy originated through disruptive selection acting on an ancestral isogamous population, though recent work has emphasized the importance of other factors in its evolution. We re-examine the disruptive selection theory, starting from an isogamous population with two mating types and taking into account the functional relationship, g(m), between the fitness of a gamete and its size, m, as well as the relationship, f(S ), between the fitness of a zygote and its size, S. Evolutionary game theory is used to determine the existence and continuous stability of isogamous and anisogamous strategies for the two mating types under various models for the two functions g(m) and f(S ). In the ancestral unicellular state, these two functions are likely to have been similar; this leads to isogamy whether they are sigmoidal or concave, though in the latter case allowance must be made for a minimal gamete size. The development of multicellularity may leave g(m) relatively unchanged while f(S ) moves to the right, leading to the evolution of anisogamy. Thus, the disruptive selection theory provides a powerful explanation of the origin of anisogamy, though other selective forces may have been involved in the subsequent specialization of micro-and macrogametes.

What do isogamous organisms teach us about sex and the two sexes?

“…They used the same form for f (S) as in (3.2), but used a related form for g(m) that more realistically modelled survivorship before fusion, by allowing this to increase with gamete size and by also tracking the time it takes until fusion occurs (this time is longer if fusion opportunities are limited). For high gamete competition, their results matched those of Bulmer & Parker [73], but the opposite assumptions (few adults in the local mating group) led to a new reason for isogamy to be stable. If the group consists of just one individual of each mating type, isogamy can be favoured since both individuals do best when they act jointly to maximize the number of viable zygotes; cooperation is maintained even though each parent is, of course, acting in its own best interests.…”

“…As we have seen, there are theoretical reasons to expect isogamy to be evolutionarily unstable in complex, multicellular organisms [67,73,77]. This has some fundamentally important consequences beyond the obvious one of having two different gamete sizes.…”

“…First, the twofold cost of males applies only to anisogamous species (see above; [66,99,100]). Second, anisogamous eukaryotes have likely evolved from isogamous ones [2,3,73,77], which were hence free of the twofold cost. Third, the ancestral reproductive strategy in eukaryotes was facultative sexual reproduction [9,10].…”

“…Bulmer & Parker [73] used a game theoretical approach in models with separate zygote 'fitness' f (S) and gamete 'fitness' rstb.royalsocietypublishing.org Phil. Trans.…”

Maternal inheritance, sexual conflict and the maladapted male

“…Because egg and sperm are under disruptive selection for size and motility [30], sexual asymmetry in selection might be most extreme for mitochondrial mutations that influence gamete function. In humans, mtDNA abnormalities, including nucleotide substitutions, deletions and insertions, result in poor sperm motility (asthenozoospermia), a common cause of male infertility [27,31].…”