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

Abstract

Inbreeding depression is widely hypothesised to drive adaptive evolution of pre-copulatory and post-copulatory mechanisms of inbreeding avoidance, which in turn are hypothesised to affect evolution of polyandry (i.e., female multiple mating). However, surprisingly little theory or modelling critically examines selection for pre-copulatory or post-copulatory inbreeding avoidance, or both strategies, given evolutionary constraints and direct costs, or examines how evolution of inbreeding avoidance strategies might feed back to affect evolution of polyandry. Selection for post-copulatory inbreeding avoidance, but not for pre-copulatory inbreeding avoidance, requires polyandry, while interactions between pre-copulatory and post-copulatory inbreeding avoidance might cause functional redundancy (i.e., `degeneracy') potentially generating complex evolutionary dynamics among inbreeding strategies and polyandry. We used individual-based modelling to quantify evolution of interacting pre-copulatory and post-copulatory inbreeding avoidance and associated polyandry given strong inbreeding depression and different evolutionary constraints and direct costs. We found that evolution of post-copulatory inbreeding avoidance increased selection for initially rare polyandry, and that evolution of a costly inbreeding avoidance strategy became negligible over time given a lower cost alternative strategy. Further, fixed pre-copulatory inbreeding avoidance often completely precluded evolution of polyandry and hence post-copulatory inbreeding avoidance, but fixed post-copulatory inbreeding avoidance did not preclude evolution of pre-copulatory inbreeding avoidance. Evolution of inbreeding avoidance phenotypes and associated polyandry are therefore affected by evolutionary feedbacks and degeneracy. All else being equal, evolution of pre-copulatory inbreeding avoidance and resulting low polyandry is more likely when post-copulatory inbreeding avoidance is precluded or costly, and evolution of post-copulatory inbreeding avoidance greatly facilitates evolution of costly polyandry.