Making sense of intralocus and interlocus sexual conflict

Abstract

Sexual conflict occurs because males and females are exposed to different selection pressures. This can affect many aspects of female and male biology, such as physiology, behavior, genetics, and even population ecology. Its broad impact has caused widespread interest in sexual conflict. However, a key aspect of sexual conflict is often confused; it comprises two distinct forms: intralocus and interlocus sexual conflict (IASC and IRSC). Although both are caused by sex differences in selection, they operate via different proximate and ultimate mechanisms. Intralocus sexual conflict and IRSC are often not clearly defined as separate processes in the scientific literature, which impedes a proper understanding of each form as well as of their relative impact on sexual conflict. Furthermore, our current knowledge of the genetics of these phenomena is severely limited. This prevents us from empirically testing numerous theories regarding the role of these two forms of sexual conflict in evolution. Here, we clarify the distinction between IASC and IRSC, by discussing how male and female interests differ, how and when sex-specific adaptation occurs, and how this may lead to evolutionary change. We then describe a framework for their study, focusing on how future experiments may help identify the genetics underlying these phenomena. Through this, we hope to promote a more critical reflection on IASC and IRSC as well as underline the necessity of genetic and mechanistic studies of these two phenomena.

Keywords: natural selection; sexual antagonism; sexual selection; sexually antagonistic coevolution; sex‐specific adaptation.

Figure 1

(a) Intralocus sexual conflict occurs when males and females have different optimal genotypes. Sex‐specific selection affects males and females differently, resulting in different fitness landscapes for traits between the sexes (blue and pink curves). Fitness is then maximized at different trait values in males and females. When trait values are encoded by the same gene(s) in males and females, each sex has a different optimal genotype. Here, a single locus A with alleles A₁ and A₂ encodes the trait value; the optimal genotype for females is A₁A₁, but A₂A₂ for males. (b) Sex‐specific adaptation under IASC leads to maladaptation in the non‐focal sex. When allele frequencies are at equilibrium, both A₁ and A₂ may be present in the population, leading to males and females having on average suboptimal fitness because for both sexes the optimal allele is not fixed. When the selective pressures on one sex are increased (as shown here by selection for increased female fitness), the equilibrium between A₁ and A₂ may be disturbed, and the female‐beneficial A₁ allele may increase in frequency. Over time, this may lead to the fixation of A₁, and the average female fitness (pink curve) increases (relative to the average fitness at equilibrium or unselected controls) to the optimal fitness w_{FA 1A1}, while the average male fitness (blue curve) decreases to the suboptimal w_{MA 1A1} (relative to the average fitness at equilibrium or unselected controls). Note that within populations, male and female fitness components must be equal (assuming equal sex ratios), and that the changes in fitness can only be observed by comparing between, for example, populations selected for increased female fitness and control populations

Figure 2

Evolutionary change under IRSC can promote ongoing diversification in different ways. When males and females have different interests in reproduction, they both may express certain phenotypes (i.e., manipulations or counteradaptations) to achieve an outcome that increases their own fitness even when this decreases the fitness of their mates. (a) Male‐female coevolution promotes ongoing change at a pair of loci which encode sex‐specific phenotypes. Here, the male and female phenotype are determined by respectively a locus A and a locus B. Invasion of a novel allele A₂ at locus A can invoke the spread of a new allele B₂ at locus B, which itself can cause a second new allele A₃ to spread at locus A, Repetitions of this process can lead to alternating evolution at loci A and B. (b) New genes may acquire a role in IRSC, after which selection will favor the evolution of a correlated response in the other sex via alteration of genes underlying the interacting phenotype. Here, males and females originally express no sex‐specific phenotypes that affect IRSC, and all potential IRSC loci (A through D) are fixed for their “naïve” allele (A1 to D1, white). At some point, a new allele A₂ at locus A spreads that confers a manipulation phenotype in males through its interaction with B in females. This triggers the spread of a counteradaptive allele B₂ to negate the effect of A₂. Similarly, loci C and D may eventually become involved as well when a manipulation allele spreads on C. Note that the evolutionary dynamics at the interacting loci A and B as well as C and D here are simplified, and that they may also follow those as described under (a), such that newly evolved IRSC loci may also come to exhibit ongoing turnover of alleles. (c) Fitness of males and females during coevolutionary bouts of male adaptation‐female counteradaptation

Figure 3

Possible reproductive interactions under different reproductive systems. (a) Gonochorism; (b) hermaphroditism; (c) gynodioecy; (d) androdioecy; (e) trioecy. Colored circles indicate the presence of that sex in the reproductive system; hashed gray circles indicate absence; arrows indicate mate compatibility between sexes