The Legacy of Parker, Baker and Smith 1972: Gamete Competition, the Evolution of Anisogamy, and Model Robustness

The evolution of anisogamy or gamete size dimorphism is a fundamental transition in evolutionary history, and it is the origin of the female and male sexes. Although mathematical models attempting to explain this transition have been published as early as 1932, the 1972 model of Parker, Baker, and Smith is considered to be the first explanation for the evolution of anisogamy that is consistent with modern evolutionary theory. The central idea of the model is ingenious in its simplicity: selection simultaneously favours large gametes for zygote provisioning, and small gametes for numerical competition, and under certain conditions the outcome is anisogamy. In this article, I derive novel analytical solutions to a 2002 game theoretical update of the 1972 anisogamy model, and use these solutions to examine its robustness to variation in its central assumptions. Combining new results with those from earlier papers, I find that the model is quite robust to variation in its central components. This kind of robustness is crucially important in a model for an early evolutionary transition where we may only have an approximate understanding of constraints that the different parts of the model must obey.

How Soon Hath Time… A History of Two “Seminal” Publications

This review documents the history of the two papers written half a century ago that relate to this special issue of Cells. The first, “Sperm competition and its evolutionary consequences in the insects” (Biological Reviews, 1970), stressed that sexual selection continues after ejaculation, resulting in many adaptations (e.g., postcopulatory guarding phases, copulatory plugs, seminal fluid components that modify female reproduction, and optimal ejaculation strategies), an aspect not considered by Darwin in his classic treatise of 1871. Sperm competition has subsequently been studied in many taxa, and post-copulatory sexual selection is now considered an important sequel to Darwinian pre-copulatory sexual selection. The second, “The origin and evolution of gamete dimorphism and the male-female phenomenon” (Journal of Theoretical Biology, 1972) showed how selection, based on gamete competition between individuals, can give rise to anisogamy in an isogamous broadcast spawning ancestor. This theory, which has subsequently been developed in various ways, is argued to form the most powerful explanation of why there are two sexes in most multicellular organisms. Together, the two papers have influenced our general understanding of the evolutionary differentiation of the two forms of gametic cells, and the divergence of sexual strategies between males and females under sexual selection.

The evolution of anisogamy does not always lead to male competition

Anisogamy has evolved in a large proportion of sexually reproducing multicellular organisms allowing the definition of the female and male sexes, producing large and small gametes, respectively. Anisogamy is the initial sexual dimorphism: it has lead the sexes to experience selection differently, which makes it a good starting point to understand the evolution of further sexual dimorphisms. For instance, it is generally accepted that anisogamy sets the stage for more intense intrasexual competition in the male sex than in the female sex. However, we argue that this idea may rely on assumptions on the conditions under which anisogamy has evolved in the first place. We consider here two widely accepted scenarios for the evolution of anisogamy: gamete competition or gamete limitation. We present a mechanistic mathematical model in which both gamete size and an intrasexual competition trait for fertilisation can coevolve in a population starting without dimorphism between its two mating types. Two different intrasexual competition traits are investigated, gamete motility and the ability of gametes to capture gametes of the opposite mating type. We show that gamete competition and gamete limitation can lead to greatly different outcomes in terms of which sex competes most for fertilisation. Our results suggest that gamete competition is most likely to lead to stronger competition in males. On the other hand, under gamete limitation, competition in form of motility can evolve in either sex while gamete capture mainly evolves in females. This study suggests that anisogamy does not per se lead to more intense male competition. The conditions under which anisogamy evolves matter, as well as the competition trait considered.

Conceptual developments in sperm competition: a very brief synopsis

The past half century has seen the development of the field of post-ejaculatory sexual selection, the sequel to sexual selection for mate-acquisition (pre-ejaculatory) described by Darwin. In richness and diversity of adaptations, post-ejaculatory selection rivals that of pre-ejaculatory sexual selection. Anisogamy—and hence two sexes—likely arose by primeval gamete competition, and sperm competition remains a major force maintaining high sperm numbers. The post-ejaculatory equivalent of male–male competition for matings, sperm competition was an intense ancestral form of sexual selection, typically weakening as mobility and internal fertilization developed in many taxa, when some expenditure became diverted into pre-ejaculatory competition. Sperm competition theory has been relatively successful in explaining variation in relative testes size and sperm numbers per ejaculate and is becoming more successful in explaining variation in sperm phenotype. Sperm competition has generated many other male adaptations such as seminal fluid proteins that variously modify female reproduction towards male interests, and copulatory plugs, prolonged copulations and post-ejaculatory guarding behaviour that reduce female remating probability, many of which result in sexual conflict. This short survey of conceptual developments is intended as a broad overview, mainly as a primer for new researchers. This article is part of the theme issue ‘Fifty years of sperm competition'.

Superorganismal anisogamy: queen–male dimorphism in eusocial insects

Colonies of insects such as ants and honeybees are commonly viewed as ‘superorganisms’, with division of labour between reproductive ‘germline-like’ queens and males and ‘somatic’ workers. On this view, properties of the superorganismal colony are comparable with those of solitary organisms to such an extent that the colony itself can be viewed as a unit analogous to an organism. Thus, the concept of a superorganism can be useful as a guide to thinking about life history and allocation traits of colonies as a whole. A pattern that seems to reoccur in insects with superorganismal societies is size dimorphism between queens and males, where queens tend to be larger than males. It has been proposed that this is analogous to the phenomenon of anisogamy at the level of gametes in organisms with separate sexes; more specifically, it is suggested that this caste dimorphism may have evolved via similar selection pressures as gamete dimorphism arises in the ‘gamete competition’ theory for the evolution of anisogamy. In this analogy, queens are analogous to female gametes, males are analogous to male gametes, and colony survival is analogous to zygote survival in gamete competition theory. Here, we explore if this question can be taken beyond an analogy, and whether a mathematical model at the superorganism level, analogous to gamete competition at the organism level, may explain the caste dimorphism seen in superorganismal insects. We find that the central theoretical idea holds, but that there are also significant differences between the way this generalized ‘propagule competition’ theory operates at the levels of solitary organisms and superorganisms. In particular, we find that the theory can explain superorganismal caste dimorphism, but compared with anisogamy evolution, a central coevolutionary link is broken, making the requirements for the theory to work less stringent than those found for the evolution of anisogamy.

Isogamy in large and complex volvocine algae is consistent with the gamete competition theory of the evolution of anisogamy

Although the gamete competition theory remains the dominant explanation for the evolution of anisogamy, well-known exceptions to its predictions have raised doubts about the completeness of the theory. One of these exceptions is isogamy in large or complex species of green algae. Here, we show that this exception may be explained in a manner consistent with a game-theoretic extension of the original theory: a constraint on the minimum size of a gamete may prevent the evolution of continuously stable anisogamy. We show that in the volvocine algae, both gametes of isogamous species retain an intact chloroplast, whereas the chloroplast of the microgamete in anisogamous species is invariably degenerate. The chloroplast, which functions in photosynthesis and starch storage, may be necessary to provision a gamete for an extended period when gamete encounter rates are low. The single chloroplast accounts for most of the volume of a typical gamete, and thus may constrain the minimum size of a gamete, preventing the evolution of anisogamy. A prediction from this hypothesis, that isogametes should be larger than the microgametes of similar-size species, is confirmed for the volvocine algae. Our results support the gamete competition theory.

Gamete evolution and sperm numbers: sperm competition versus sperm limitation

Both gamete competition and gamete limitation can generate anisogamy from ancestral isogamy, and both sperm competition (SC) and sperm limitation (SL) can increase sperm numbers. Here, we compare the marginal benefits due to these two components at any given population level of sperm production using the risk and intensity models in sperm economics. We show quite generally for the intensity model (where N males compete for each set of eggs) that however severe the degree of SL, if there is at least one competitor for fertilization ( N − 1 ≥ 1), the marginal gains through SC exceed those for SL, provided that the relationship between the probability of fertilization ( F ) and increasing sperm numbers ( x ) is a concave function. In the risk model, as fertility F increases from 0 to 1.0, the threshold SC risk (the probability q that two males compete for fertilization) for SC to be the dominant force drops from 1.0 to 0. The gamete competition and gamete limitation theories for the evolution of anisogamy rely on very similar considerations: our results imply that gamete limitation could dominate only if ancestral reproduction took place in highly isolated, small spawning groups.