Not all sex ratios are equal: the Fisher condition, parental care and sexual selection

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Abstract

The term ‘sex roles’ encapsulates male–female differences in mate searching, competitive traits that increase mating/fertilization opportunities, choosiness about mates and parental care. Theoretical models suggest that biased sex ratios drive the evolution of sex roles. To model sex role evolution, it is essential to note that in most sexually reproducing species (haplodiploid insects are an exception), each offspring has one father and one mother. Consequently, the total number of offspring produced by each sex is identical, so the mean number of offspring produced by individuals of each sex depends on the sex ratio (Fisher condition). Similarly, the total number of heterosexual matings is identical for each sex. On average, neither sex can mate nor breed more often when the sex ratio is even. But equally common in which sex ratio? The Fisher condition only applies to some reproductive measures (e.g. lifetime offspring production or matings) for certain sex ratios (e.g. operational or adult sex ratio; OSR, ASR). Here, we review recent models that clarify whether a biased OSR, ASR or sex ratio at maturation (MSR) have a causal or correlational relationship with the evolution of sex differences in parental care and competitive traits—two key components of sex roles. We suggest that it is more fruitful to understand the combined effect of the MSR and mortality rates while caring and competing than that of the ASR itself. In short, we argue that the ASR does not have a causal role in the evolution of parental care. We point out, however, that the ASR can be a cue for adaptive phenotypic plasticity in how each sex invests in parental care. This article is part of the themed issue ‘Adult sex ratios and reproductive decisions: a critical re-examination of sex differences in human and animal societies’.

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Parental investment, sexual selection and sex ratios.

Hanna Kokko, Michael D. Jennions (2008)

Conventional sex roles imply caring females and competitive males. The evolution of sex role divergence is widely attributed to anisogamy initiating a self-reinforcing process. The initial asymmetry in pre-mating parental investment (eggs vs. sperm) is assumed to promote even greater divergence in post-mating parental investment (parental care). But do we really understand the process? Trivers [Sexual Selection and the Descent of Man 1871-1971 (1972), Aldine Press, Chicago] introduced two arguments with a female and male perspective on whether to care for offspring that try to link pre-mating and post-mating investment. Here we review their merits and subsequent theoretical developments. The first argument is that females are more committed than males to providing care because they stand to lose a greater initial investment. This, however, commits the 'Concorde Fallacy' as optimal decisions should depend on future pay-offs not past costs. Although the argument can be rephrased in terms of residual reproductive value when past investment affects future pay-offs, it remains weak. The factors likely to change future pay-offs seem to work against females providing more care than males. The second argument takes the reasonable premise that anisogamy produces a male-biased operational sex ratio (OSR) leading to males competing for mates. Male care is then predicted to be less likely to evolve as it consumes resources that could otherwise be used to increase competitiveness. However, given each offspring has precisely two genetic parents (the Fisher condition), a biased OSR generates frequency-dependent selection, analogous to Fisherian sex ratio selection, that favours increased parental investment by whichever sex faces more intense competition. Sex role divergence is therefore still an evolutionary conundrum. Here we review some possible solutions. Factors that promote conventional sex roles are sexual selection on males (but non-random variance in male mating success must be high to override the Fisher condition), loss of paternity because of female multiple mating or group spawning and patterns of mortality that generate female-biased adult sex ratios (ASR). We present an integrative model that shows how these factors interact to generate sex roles. We emphasize the need to distinguish between the ASR and the operational sex ratio (OSR). If mortality is higher when caring than competing this diminishes the likelihood of sex role divergence because this strongly limits the mating success of the earlier deserting sex. We illustrate this in a model where a change in relative mortality rates while caring and competing generates a shift from a mammalian type breeding system (female-only care, male-biased OSR and female-biased ASR) to an avian type system (biparental care and a male-biased OSR and ASR).