Softness of selection and mating system interact to shape trait evolution under sexual conflict

Abstract

Sexual selection and sexual conflict play central roles in driving the evolution of male and female traits. Experimental evolution provides a powerful approach to study the operation of these forces under controlled environmental and demographic conditions, thereby allowing direct comparisons of evolutionary trajectories under different treatments such as mating systems. Despite the rapid progress of experimental and statistical techniques that support experimental evolution studies, we still lack clear theoretical predictions on the effects of different mating systems beyond what intuition suggests. For example, polygamy (several males and females in a mating group) and polyandry (one single female and multiple males in a mating group) have each been used as treatments that elevate sexual selection on males and sexual conflict relative to monogamy. However, polygamy and polyandry manipulations sometimes produce different evolutionary outcomes, and the precise reasons why remain elusive. In addition, the softness of selection (i.e., scale of competition within each sex) is known to affect trait evolution, and is an important factor to consider in experimental design. To date, no model has specifically investigated how the softness of selection interacts with different mating systems. Here, we try to fill these gaps by generating clear and readily testable predictions. Our set of models were designed to capture the most important life cycle events in typical experimental evolution studies, and we use simulated changes of sex‐specific gene expression profiles (i.e., feminization or masculinization) to quantify trait evolution under different selection schemes. We show that interactions between the softness of selection and the mating system can produce results that have been identified as counterintuitive in previous empirical work such as polyandry producing stronger feminization than monogamy. We conclude by encouraging a stronger integration of modelling in future experimental evolution studies and pointing out remaining knowledge gaps for future theoretical work.

Experimental evolution reveals differential evolutionary trajectories in male and female activity levels in response to sexual selection and metapopulation structure

“…A possibility is that the behavioral divergence that we have exposed responds to the differential softness of selection between the structured (where soft selection applies) and nonstructured (where hard selection operates) populations (see Fig. 1, Methods, Supporting Information;Wallace 1975;Saccheri and Hanski 2006;Débarre and Gandon 2011;Reznick 2016;Bell et al 2021;Li Richter and Hollis 2021). If this was the case, soft selection in structured populations would have allowed the evolution of plasticity in male behavior.…”

“…1, Methods , Supporting Information; Wallace 1975; Saccheri and Hanski 2006; Débarre and Gandon 2011; Reznick 2016; Bell et al. 2021; Li Richter and Hollis 2021). If this was the case, soft selection in structured populations would have allowed the evolution of plasticity in male behavior.…”

“…1, Supporting Information; Wallace 1975; Saccheri and Hanski 2006; Débarre and Gandon 2011; Reznick 2016; Bell et al. 2021; Li Richter and Hollis 2021).…”

The stagnation paradox: the ever-improving but (more or less) stationary population fitness

“…In anisogamous species, however, females tend to be demographically dominant [ 50 ], meaning that their performance is a stronger determinant of population growth than the number, or fitness, of males. One way to phrase this is that selection is softer on males than on females [ 51 ], and it is well known that soft selection can maintain population fitness at demographically adequate levels even if a straightforward computation of mutational load would predict dismal performance [ 52 , 53 ]. Classic theory on load and soft selection, however, does not differentiate between males and females, and because reproduction often involves direct behavioural contact between contestants or potential mates, very diverse outcomes are possible.…”

Sex-biased gene expression at single-cell resolution: Cause and consequence of sexual dimorphism

“…Male-biased genes in many species tend to exhibit higher rates of evolution at both the coding sequence and the expression level (Ranz et al 2003; Khaitovich et al 2005; Sharma et al 2014; Lipinska et al 2015; Whittle and Extavour 2019; Lichilin et al 2021). While early work in Drosophila melanogaster has interpreted this as the result of stronger sexual selection acting in males (Proschel et al 2006; Sawyer et al 2007), studies in other species have found that such accelerated patterns of evolution are instead more consistent with relaxed constraint (Gershoni and Pietrokovski et al 2014; Harrison et al 2015; Sayadi et al 2019; Dapper and Wade, 2020; Djordjevic et al 2021), and experimental evolution results were somewhat mixed (Hollis et al 2014; Veltsos et al 2017; Li Richter and Hollis 2021).…”