Paternal indirect genetic effects on offspring viability and the benefits of polyandry

Although females are expected to maximize their reproductive success with only one or a few matings [1], the females of many species mate with multiple partners [2]. Experimental studies have found evidence for an increase in egg or embryo viability when females mate polyandrously [3]. These studies have been interpreted in the context of genetic-benefit models that propose that multiple mating increases offspring viability because it allows females to select male genotypes that influence viability directly or because it allows females to avoid genetic incompatibility [2, 4-8]. However, no studies have examined directly the precise mechanisms by which parents influence embryo viability. Using a morphological marker that enabled us to determine paternity and survival of embryos sired by individual male crickets in both sperm-competitive and -noncompetitive situations, we show that males inducing high embryo viability enhance the viability of embryos sired by inferior males. These results indicate that paternal effects and interacting phenotypes determine embryo viability. They show that a male's reproductive success is modified by the interaction between indirect genetic effects of sperm competitors. Importantly, our findings show that the benefits accruing to offspring of multiply mated females need not be transmitted genetically.