Social Games and Genic Selection Drive Mammalian Mating System Evolution and Speciation

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 frequencydependent 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 four stable outcomes driven by the balance between cooperative and agonistic behaviors: promiscuity (two or three strategies), polygyny, and monogamy. Phylogenetic analysis of 288 rodent species supports assumptions of our model and is consistent with patterns of evolutionarily stable states and mating system transitions. Support for model assumptions include that monogamy and polygyny evolve from promiscuity and that 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 by 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.

The triadic structure of personality space in the house mouse resembles that of species with known personality badges; suggesting reciprocal hierarchies are an evolutionary motif with mixed strategies being more common

“…A likely candidate for this green-beard is the Vasopressin receptor, V1aR which evolves mutations when rodents evolve from the promiscuous types of males to purely polygynous types of males. Sinervo et al (27) also found that purely monogamous lineages gave rise to polygynous lineages at a high rate.…”

“…A likely candidate for this green-beard is the Vasopressin receptor, V1aR which evolves mutations when rodents evolve from the promiscuous types of males to purely polygynous types of males. Sinervo et al (27) also found that purely monogamous lineages gave rise to polygynous lineages at a high rate. These evolutionary transitions between monogamy and polygyny in rodents are linked to a point mutation in a Vasopressin receptor gene [V1aR: (31–33)].…”

“…The mice also tended to be more pro-social with higher social synchronicity and contact durations, which might be of more similarity to the monogamous nature of the blue lizards. The pro-sociality is akin to a rock-paper-scissors model of rodent mating systems in which promiscuous species occur in 3 types of territoriality: polygynous males with multiple males, monogamous males with a single female, but the monogamous males are more likely to care for progeny and sneaker males that lack territories and float about the matrix of polygynous and monogamous types (27). Thus, monogamous rodent males have genic care, akin to the genic (green-bearded) altruism of blue lizards.…”

Evolution of social organization: phylogenetic analyses of ecology and sexual selection in weavers

“…However, in our study, we failed to find a direct relationship between either habitat type or diet with weaver mating system. Indeed, recent studies on mating system evolution emphasized the link between parental care and social monogamy, which indicates that paternal care and monogamy are coadapted (Lukas and Clutton-Brock 2013;Sinervo et al 2020). Male parental care behaviors can increase female fecundity, which shows that parental conflict may be symmetric between sexes (West and Capellini 2016).…”

Theoretical and material species and the concept of speciesness (about the reality of species, types of species and their diversity)

“…В розвитку ідей видовості особливе місце має посісти концепція еволюції репродуктивних систем, детально досліджена у ссавців у контексті видоутворення (Sinervo et al 2019). Еволюція видовості може бути пояснена через еволюцію систем «охорони репродуктивних систем».…”