Spatial environmental complexity mediates sexual conflict and sexual selection in Drosophila melanogaster

Abstract

Sexual selection is an important agent of evolutionary change, but the strength and direction of selection often vary over space and time. One potential source of heterogeneity may lie in the opportunity for male–male and/or male–female interactions imposed by the spatial environment. It has been suggested that increased spatial complexity permits sexual selection to act in a complementary fashion with natural selection (hastening the loss of deleterious alleles and/or promoting the spread of beneficial alleles) via two (not mutually exclusive) pathways. In the first scenario, sexual selection potentially acts more strongly on males in complex environments, allowing males of greater genetic “quality” a greater chance of outcompeting rivals, with benefits manifested indirectly in offspring. In the second scenario, increased spatial complexity reduces opportunities for males to antagonistically harm females, allowing females (especially those of greater potential fecundities) to achieve greater reproductive success (direct fitness benefits). Here, using Drosophila melanogaster , we explore the importance of these mechanisms by measuring direct and indirect fitness of females housed in simple vial environments or in vials in which spatial complexity has been increased. We find strong evidence in favor of the female conflict‐mediated pathway as individuals in complex environments remated less frequently and produced more offspring than those housed in a simpler spatial environment, but no difference in the fitness of sons or daughters. We discuss these results in the context of other recent studies and what they mean for our understanding of how sexual selection operates.

Heightened condition-dependence of the sexual transcriptome as a function of genetic quality in Drosophila melanogaster head tissue

“…[51,52]) or indirect (e.g. [53]) costs associated with interacting and mating with preferred males, and the net outcome for females may depend on context [54][55][56].…”

Testing for local adaptation in adult male and female fitness among populations evolved under different mate competition regimes

“…; Yun et al. ; Malek and Long ), and likely because total sexual selection on males is stronger in cages than in vials (see Maclellan et al. ).…”

“…MC complex males are likely healthier and more vigorous (i.e., higher genetic quality); we have previously shown more efficient purging of deleterious mutations, reduced overall mutation load (evidenced by lower inbreeding depression), and faster adaptation with respect to egg-to-adult viability in these novel larval habitats in populations evolved in a complex polygamous mating environment compared to those evolved in a simple polygamous mating environment (Colpitts et al 2017;Singh et al 2017;Yun et al 2017). Evidence indicates that higher quality genotypes likely evolve in cages because sexual conflict does not diminish natural selection on females in cages as it does in vials (Colpitts et al 2017;Yun et al 2017;Malek and Long 2019), and likely because total sexual selection on males is stronger in cages than in vials (see Maclellan et al 2009).…”

Parasites Mediate Condition-Dependent Sexual Selection for Local Adaptation in a Natural Insect Population

“…Theory and limited empirical evidence suggest that condition-dependent sexual selection can improve population fitness, for instance by purging deleterious mutations or by favouring locally adapted males [1,2,4,61,62]. Most previous studies investigating the links between sexual selection, local adaptation and population fitness have been performed in laboratory settings using a few model organisms and a restricted set of taxa [8][9][10]16,[61][62][63][64][65][66].…”