Polyandry provides reproductive and genetic benefits in colonising populations

Abstract

Polyandry, when females mate with more than one male, is theorised to play an important role in successful colonisation of new habitats. In addition to possible benefits from sexual selection, even mild polyandry could facilitate colonisation by protecting against inbreeding and reducing the costs of mating with incompatible or infertile males. Here, we measure the importance of mild polyandry for population viability and reproductive fitness following experimental founder events into a highertemperature regime. Using colonisation experiments with the model beetle Tribolium castaneum, in which females can produce offspring for up to 140 days following a single mating, we founded more than 100 replicate populations using single females that had been given the opportunity to mate with either one or two males and then tracked their subsequent population dynamics. Following population viability and fitness across 10 generations, we found that extinction rates were significantly lower in populations founded by females given polyandrous opportunities to mate with two males (9%) compared to populations founded by monogamous females (34%). In addition, populations founded by females that had been provided with opportunities to store sperm from two different males showed double the median productivity following colonisation compared to monogamous-founded populations. Notably, we identified short-term and longer-term benefits to post-colonisation populations from double-mating, with results suggesting that polyandry acts to both protect against mating with incompatible males through the founder event, and reduce inbreeding depression as the colonisation proceeds for 10 generations. Our results therefore show that even mild polyandry provides both reproductive and genetic benefits for colonising populations.

Obituary: Professor Matthew James George Gage (1967–2022)

“…2020), and polyandry during colonization (Lewis et al. 2020) and when females copulate with subfertile heatwave‐exposed males (Vasudeva et al. 2021).…”

“…Many other studies in Tribolium investigated different aspects of sexual selection, for example, combining experiments and population genetic simulations to demonstrate the widespread benefits of sexual selection on net population fitness (Godwin et al 2018). One of the key areas that Matt really helped to clarify is how sexual selection operates to benefit both males and females under scenarios of stress through the process of mate choice (Godwin et al 2020), and polyandry during colonization (Lewis et al 2020) and when females copulate with subfertile heatwave-exposed males (Vasudeva et al 2021). His research also focused on broad and challenging questions for which there are currently very few definitive answers, for example, using Tribolium beetles to ask, "why does same sex behaviours evolve within mating systems?"…”

An empirical test of the bet‐hedging polyandry hypothesis: Female red flour beetles avoid extinction via multiple mating

“…22% of the males in a population are infertile (according to the estimate of Garcia-Gonzalez, 2004) and females cannot discriminate such males, polyandry achieve higher fixation probability than monandry in the structured metapopulations. However, limited empirical studies have been performed to test this hypothesis (but see Fox & Rauter, 2003;Garcia-Gonzalez et al, 2015;Lewis et al, 2020;Power & Holman, 2014;Schmoll et al, 2007;Yuta et al, 2018). In particular, very few experimental studies examined whether polyandry enhances the geometric mean fitness across successive generations (Fox & Rauter, 2003;Garcia-Gonzalez et al, 2015).…”

“…These hypotheses have been investigated by numerous empirical and theoretical studies (e.g., Jennions & Petrie, 2000; Meade et al., 2017; Nason & Kelly, 2020; Pizzari & Wedell, 2013; Simmons, 2005; Zeh & Zeh, 2003). Today, the increasing studies have reported the benefits of female multiple mating with different males (e.g., García‐González et al., 2015; Lewis et al., 2020; Power & Holman, 2014; Snook, 2014). However, it is still controversial whether the costs of remating could be compensated by the proposed benefits.…”

“…However, limited empirical studies have been performed to test this hypothesis (but see Fox & Rauter, 2003; Garcia‐Gonzalez et al., 2015; Lewis et al., 2020; Power & Holman, 2014; Schmoll et al., 2007; Yuta et al., 2018). In particular, very few experimental studies examined whether polyandry enhances the geometric mean fitness across successive generations (Fox & Rauter, 2003; Garcia‐Gonzalez et al., 2015).…”