How cuckoldry can decrease the opportunity for sexual selection: data and theory from a genetic parentage analysis of the sand goby, Pomatoschistus minutus

Abstract

Alternative mating strategies are common in nature and are generally thought to increase the intensity of sexual selection. However, cuckoldry can theoretically decrease the opportunity for sexual selection, particularly in highly polygamous species. We address here the influence of sneaking (fertilization thievery) on the opportunity for sexual selection in the sand goby Pomatoschistus minutus, a marine fish species in which males build and defend nests. Our microsatellite-based analysis of the mating system in a natural sand goby population shows high rates of sneaking and multiple mating by males. Sneaker males had fertilized eggs in approximately 50% of the assayed nests, and multiple sneakers sometimes fertilized eggs from a single female. Successful males had received eggs from 2 to 6 females per nest (mean = 3.4). We developed a simple mathematical model showing that sneaking in this polygynous sand goby population almost certainly decreases the opportunity for sexual selection, an outcome that contrasts with the usual effects of cuckoldry in socially monogamous animals. These results highlight a more complex and interesting relationship between cuckoldry rates and the intensity of sexual selection than previously assumed in much of the literature on animal mating systems.

Figure 1

Distributions of mating success (i.e., the number of females with whom a male sired progeny) for sand goby males. Shown are (a) the observed distribution of mating success for males in the absence of sneaking (estimated directly from our parentage study), (b) the results of the model when all sneaking is done by males with eggs in their nests, and (c) the results of the model when all sneaking is done by nonnesting males (or unsuccessfully nesting males). This depiction assumes that N₀ = 0.425.

Figure 2

The relationship between the proportion of males attempting to sneak and the opportunity for sexual selection based on variance in male mating success when (a) N₀ = 0.425 or (b) N₀ = 0.689. Squares (connected by a solid line) indicate the opportunity for sexual selection when all sneaking is done by a percentage of the nest holders (i.e., p₀ = 0 and p_nh ranges from 0.1 to 1.0). Circles (connected by a dashed line) indicate the results for the cases in which all sneaking is done by some percentage of nonnesting males (i.e., p_nh = 0 and p₀ ranges from 0.1 to 1.0). The horizontal dashed line in each graph corresponds to the opportunity for sexual selection in the absence of sneaking.