Evolution of Inbreeding Avoidance and Inbreeding Preference through Mate Choice among Interacting Relatives

Abstract

While extensive population genetic theory predicts conditions favoring evolution of self-fertilization versus outcrossing, there is no analogous theory that predicts conditions favoring evolution of inbreeding avoidance or inbreeding preference enacted through mate choice given obligate biparental reproduction. Multiple interacting processes complicate the dynamics of alleles underlying such inbreeding strategies, including sexual conflict, distributions of kinship, genetic drift, purging of mutation load, direct costs, and restricted kin discrimination. We incorporated these processes into an individual-based model to predict conditions where selection should increase or decrease frequencies of alleles causing inbreeding avoidance or inbreeding preference when females or males controlled mating. Selection for inbreeding avoidance occurred given strong inbreeding depression when either sex chose mates, while selection for inbreeding preference occurred given very weak inbreeding depression when females chose but never occurred when males chose. Selection for both strategies was constrained by direct costs and restricted kin discrimination. Purging was negligible, but allele frequencies were strongly affected by drift in small populations, while selection for inbreeding avoidance was weak in larger populations because inbreeding risk decreased. Therefore, while selection sometimes favored alleles underlying inbreeding avoidance or preference, evolution of such strategies may be much more restricted and stochastic than is commonly presumed.

Evolution of precopulatory and post-copulatory strategies of inbreeding avoidance and associated polyandry

“…This formulation ensures that the relationship between and the magnitude of inbreeding depression in offspring is consistent across replicate simulations. This choice, as opposed to a more mechanistic model of inbreeding depression that allows purging, is further justified because previous genetically explicit modelling (Duthie & Reid, ) showed that inbreeding avoidance in biparental populations has a negligible effect on load given small‐effect deleterious mutations (see also Wang et al ., ; Guillaume & Perrin, ).…”

“…Offspring that are viable after the Bernoulli trial become adults. Given our current objectives, we simulate evolution under conditions where inbreeding avoidance is adaptive due to strong inbreeding depression, not where inbreeding preference is adaptive due to weak or zero inbreeding depression (Parker, ; Kokko & Ots, ; Duthie & Reid, ) or outbreeding depression (Bateson, ; Greeff et al ., ). However, as described above, positive and values resulting in inbreeding preference are not precluded from evolving, and could potentially arise due to mutation or drift.…”

“…Further, immigrants’ , and allele values are randomly sampled from normal distributions with means and standard deviations equal to those in the focal population at the time of immigration, meaning that they do not directly cause any change in the distribution of allele values. We thereby effectively assume that the focal population receives immigrants from other nearby populations that are subject to the same selection on , and (Duthie & Reid, ; Duthie et al ., ).…”

“…For all replicates, we set immigrants, which produced a range of kin and nonkin in each generation allowing females to express inbreeding strategies, and offspring, which was sufficient to keep populations consistently at carrying capacities and avoid population extinction. Values of and were both set to 100 because previous modelling showed that populations of this size are small enough that mate encounters between kin occur with sufficient frequency for selection on inbreeding strategy, but not so small that selection is typically overwhelmed by drift (Duthie & Reid, ).…”

“…The few previous models that considered evolution of biparental inbreeding avoidance through mate choice (as opposed to dispersal) have implicitly or explicitly considered the fate of a rare allele underlying precopulatory inbreeding avoidance in a population initially fixed for random mating (e.g. Parker, , ; Duthie & Reid, ; Duthie et al ., ). Such models are useful for isolating the invasion fitness of this single strategy.…”