The evolution of polyandry I: intragenomic conflict and genetic incompatibility

Abstract

Why do females across a wide range of taxa mate with more than one male? We suggest that a better understanding of polyandry may be gained by considering the implications of intragenomic conflict for female reproductive success. Here, we revisit the literature on cellular endosymbionts, transposable elements, segregation distorters, maternal-effect lethals and genomically imprinted genes to show that each of these selfish genetic elements can modify maternal and paternal haplotypes in ways that render them incompatible within the developing embryo. We propose that the cumulative threat to female reproductive success of genetic incompatibility arising from intragenomic conflict may be an important force driving the evolution of polyandry. By mating with more than one male, females can potentially exploit post-copulatory mechanisms for minimizing the risk and/or cost of fertilization by genetically incompatible sperm. This hypothesis differs fundamentally from other genetic benefit models of polyandry in that the fitness consequences of intragenomic conflict depend on an interaction between parental genomes and are thus non-additive. Reciprocal evolutionary change between selfish genetic elements and their suppressors, combined with the capacity of these elements for horizontal transfer between species, is likely to ensure the persistence of genetic incompatibility as a threat to female reproductive success.