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.

Association of polyandry andsex-ratiodrive prevalence in natural populations ofDrosophila neotestacea

“…Recently, multiple mating has been proposed as a force to protect a host against SGEs [18], and here we show that higher polyandry is associated with lower SR prevalence in natural populations. We do not find evidence, however, that multiple mating has evolved in response to the presence of the SGE.…”

The polyandry revolution

“…Clearly, there is a direct link between the mating patterns and the dynamics and evolution of diseases. It is likely that this association is even more widespread and important in influencing the dynamic relationship between SGEs and mating strategies, by affecting the movement patterns and encounter rate of infected individuals harbouring SGEs [30]. Furthermore, we may also predict that mating systems dominated by a few individuals should in general be associated with lower than average infection levels and potentially also lower virulence levels.…”

“…Wedell [30] reviews recent work investigating the relationship between polyandry and SGEs or endosymbionts. SGEs often increase their spread at the expense of the fertilizing efficiency of a male carrier.…”

The evolutionary ecology of testicular function: size isn't everything

“…It is now well established that TEs tend to be primarily active during different phases of germ-line formation and spermatogenesis (and also oogenesis) (Werren, 2011;Bao & Yan, 2012;Wedell, 2013), likely as a result of two main processes. Firstly, there is widespread reprogramming of TE-silencing epigenetic marks during the proliferation of the primordial germ cells (Werren, 2011;Bao & Yan, 2012), which could affect the number of mutations initially seeded into spermatogonia (and mutations that occur at this stage may also be important for tissue architecture: .…”