The dynamic relationship between polyandry and selfish genetic elements

Abstract

Selfish genetic elements (SGEs) are ubiquitous in eukaryotes and bacteria, and make up a large part of the genome. They frequently target sperm to increase their transmission success, but these manipulations are often associated with reduced male fertility. Low fertility of SGE-carrying males is suggested to promote polyandry as a female strategy to bias paternity against male carriers. Support for this hypothesis is found in several taxa, where SGE-carrying males have reduced sperm competitive ability. In contrast, when SGEs give rise to reproductive incompatibilities between SGE-carrying males and females, polyandry is not necessarily favoured, irrespective of the detrimental impact on male fertility. This is due to the frequency-dependent nature of these incompatibilities, because they will decrease in the population as the frequency of SGEs increases. However, reduced fertility of SGE-carrying males can prevent the successful population invasion of SGEs. In addition, SGEs can directly influence male and female mating behaviour, mating rates and reproductive traits (e.g. female reproductive tract length and male sperm). This reveals a potent and dynamic interaction between SGEs and polyandry highlighting the potential to generate sexual selection and conflict, but also indicates that polyandry can promote harmony within the genome by undermining the spread of SGEs.

Figure 1.

The mean ± s.e. offspring production of (a) monandrous females and (b) polyandrous Drosophila simulans females. Dark grey bars indicate crosses where all males are incompatible with females. Light grey bars indicate crosses where one of two males is incompatible. White bars indicate entirely compatible crosses. Female infection status is described in the lower divisions of the x-axes. Male infection status is given in the higher divisions of the x-axes. In (b), male infection status and order of mating is described as follows: I, infected male; U, uninfected male. The first letter indicates the infection status of the first male to mate and the second letter the infection status of the second male. Adapted from Champion de Crespigny et al. [64]

Figure 2.

(a) Spermatophore size as a function of male mating rate in the butterfly H. bolina. Negative correlation is highly significant (Spearman's rank correlation test, ρ =−0.66, S = 2206, p = 0.0002). (b) Female mating rate as a function of population sex ratio. Model comparison showed that a regression containing both a linear and a quadratic term (dashed curve) fits the data significantly better than a linear one (F_1,17 = 12.10, p = 0.002) or a purely quadratic one (F_1,17 = 11.34, p = 0.004). Female mating rate was estimated from the mean number of spermatophores per female. Sex ratio is given as log of number of females per male. Adapted from Charlat et al. [66]

Figure 3.

The proportion of experimental evolution line Drosophila pseudoobscura females remating at their first opportunity, for each selection regime (n = 11 lines), when offered standardized stock males, showing median, interquartile range, and range (*p = 0.0383; n.s., not significant). Adapted from Price et al. [69]