American Society of Naturalists

Barry Sinervo, Alexis S. Chaine, and Donald Miles (Feb 2020)

Genes drive mating system evolution in models and rodents

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Whether animals partner with just one mate or with many, or even if individuals in a population differ in their mating patterns, has largely been explained by control over territorial resources. In an upcoming issue of The American Naturalist, researchers from the US and France have proposed a new explanation: genes for three alternative behaviors of aggression, sneaking, and the combination of cooperation and care that underlie both mating and social behavior can drive the evolution of mating patterns. The research team used mathematical models to describe mating system evolution based on genes for male-male competition (vs. cooperation), choice of neighborhoods, and paternal care premised on shared genes between interacting individuals. Using published data on rodent mating behavior, they then tested whether the predictions generated by their genetic model captured patterns in mating system while ignoring resource distribution. Rodents exhibit behaviors that the researchers modeled, including alternative mating tactics, genetic recognition, and paternal care, which are often linked to specific genes identified in molecular studies. Both distribution of mating systems and reconstruction of the evolutionary history of rodent mating systems among 288 species across all families match predictions of the model. Interestingly, cooperation and care behaviors associated with a monogamous mating strategy moves species from a mixed-mating system containing alternative strategies towards either monogamous or polygynous species and accelerates speciation. Monogamy in rodents (~20%) is far more common than previously believed. Taken together, these findings open a new possibility for what drives mating patterns: genes that underlie cooperative and care behavior linked to how you interact with offspring and neighbors and drive a rock-paper-scissors (RPS) dynamic among alternative behavioral types. The model generalizes the RPS game from mating dynamics to speciation across vertebrate classes and other organisms.

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Abstract

Mating system theory based on economics of resource defense has been applied to describe social system diversity across taxa. Such models are generally successful, but fail to account for stable mating systems across different environments or shifts in mating system without a change in ecological conditions. We propose an alternative approach to resource defense theory based on frequency dependent competition among genetically determined alternative behavioral strategies characterizing many social systems (polygyny, monogamy, sneak). We modeled payoffs for competition, neighborhood choice, and paternal care to determine evolutionary transitions among mating systems. Our model predicts 4 stable outcomes driven by the balance between cooperative and agonistic behaviors: promiscuity (2 or 3 strategies), polygyny, and monogamy. Phylogenetic analysis of 288 rodent species support assumptions of our model and is consistent with patterns of evolutionarily stable states and mating system transitions. Support for model assumptions include monogamy and polygyny evolve from promiscuity and paternal care and monogamy are coadapted in rodents. As predicted by our model, monogamy and polygyny occur in sister taxa among rodents more often than chance. Transitions to monogamy also favor higher speciation rates in subsequent lineages, relative to polygynous sister lineages. Taken together, our results suggest that genetically based neighborhood choice behavior and paternal care can drive transitions in mating system evolution. While our genic mating system theory could complement resource based theory, it can explain mating system transitions regardless of resource distribution and provides alternative explanations such as evolutionary inertia when resource ecology and mating systems do not match.