“Multiple evolutionary routes to monogamy: modeling the coevolution of mating decisions and parental investment”

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Arne Jungwirth and Rufus A. Johnstone (Feb 2019)

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Monogamy is difficult to achieve, and mating and parenting are intimately intertwined

Routes to monogamy: how parenting and mating co-evolve

Successful sexual reproduction has two components: mating (to produce offspring) and parenting (to ensure offspring survival), and these are typically traded off against one another. Caring for offspring may, e.g., get in the way of finding mates. Why some animals invest heavily in mating (think salmons) while others focus on parenting (think albatrosses) is a question as old as evolutionary biology. In addition, biologists have long tried to explain why in some species both males and females invest in parenting (think penguins), while in others it is mainly one sex (think sea horses or elephant seals). The relative rarity of our own breeding system (monogamous mating with extended parenting by both sexes) has received special attention. The current manuscript shows that monogamy should indeed be rare unless at least one of the following criteria is fulfilled: (i) competition for mates is low, e.g. when populations are very sparse, (ii) individuals can interfere with mating decisions of others, e.g. by aggressively driving away competitors, (iii) accepting polygamy incurs fitness costs, e.g. reducing fecundity or increasing mortality. The models track how parenting co-evolves with mating decisions and predict that egalitarian sharing among the sexes will only be observed under monogamy. Crucially, the mechanism by which monogamy is favoured (i-iii above) influences both how much absolute investment is allocated towards parenting, and how much relative investment each sex is selected to provide. The most skewed sharing occurs among polygamously mated individuals, where polygamy incurs fecundity costs.


Abstract

The relationships between mating decisions and parental investment are central to evolution, but to date few theoretical treatments of their co-evolution have been developed. Here we adopt a demographically explicit, adaptive dynamics approach to analyze the co-evolution of female mating decisions and parental investment of both sexes in a self-consistent way. Our models predict that where females cannot interfere with one another’s mating decisions, and where they do not differ in their survival- and fecundity prospects, monogamy should be rare, and favored only under harsh environmental conditions, in sparse populations. However, allowing for interference or asymmetries among females leads to selection for monogamy over a much broader range of environments and demographies. Interference by paired, resident females may prevent unmated rivals from joining existing monogamous pairs, thus barring the formation of polygynous groups. Asymmetries between established, primary females and subsequently joining secondary females may increase the relative costs of early polygynous reproduction compared to delayed monogamy for the latter. The models thus highlight different routes by which monogamy may evolve. We further track how parental investment by the sexes co-evolves with female mating decisions, highlighting how sexual conflict over parental investment is both cause and effect of mating behavior.