Downloaded from http://cshperspectives.cshlp.org/ on September 24, 2021 - Published by Cold Spring Harbor Laboratory Press The Relationship between Sexual Selection and Sexual Conflict Hanna Kokko and Michael D. Jennions Center of Excellence in Biological Interactions, Ecology, Evolution & Genetics, Research School of Biology, The Australian National University, Canberra ACT 0200, Australia Correspondence: [email protected], [email protected] Evolutionary conflicts of interest arise whenever genetically different individuals interact and their routes to fitness maximization differ. Sexual selection favors traits that increase an individual’s competitiveness to acquire mates and fertilizations. Sexual conflict occurs if an individual of sex A’s relative fitness would increase if it had a “tool” that could alter what an individual of sex B does (including the parental genes transferred), at a cost to B’s fitness. This definition clarifies several issues: Conflict is very common and, although it extends outside traits under sexual selection, sexual selection is a ready source of sexual conflict. Sexual conflict and sexual selection should not be presented as alternative expla- nations for trait evolution. Conflict is closely linked to the concept of a lag load, which is context-dependent and sex-specific. This makes it possible to ask if one sex can “win.” We expect higher population fitness if females win. any published studies ask if sexual selec- one or the other shapes the natural world, when Mtion or sexual conflict drives the evolution obviously both interact to determine the out- of key reproductive traits (e.g., mate choice). come. Here we argue that this is an inappropriate So why have sexual conflict and sexual selec- question. By analogy, G. Evelyn Hutchinson tion sometimes been elevated to alternate expla- (1965) coined the phrase “the ecological theatre nations? This approach is often associated with and the evolutionary play” to capture how fac- an assumption that sexual conflict affects traits tors that influence the birth, death, and repro- under direct selection, favoring traits that alter duction of individuals (studied by ecologists) the likelihood of a potential mate agreeing or determine which individuals reproduce, and refusing to mate because it affects the bearer’s “sets the stage” for the selective forces that drive immediate reproductive output, whereas “tra- evolutionary trajectories (studied by evolution- ditional” sexual selection is assumed to favor ary biologists). The more modern concept of traits that are under indirect selection because “eco-evolutionary feedback” (Schoener 2011) they increase offspring fitness. These “tradition- emphasizes that selection changes the character al” models are sometimes described as “mutu- of the actors over time, altering their ecological alistic” (e.g., Pizzari and Snook 2003; Rice et al. interactions. No one would sensibly ask whether 2006), although this term appears to be used Editors: William R. Rice and Sergey Gavrilets Additional Perspectives on The Genetics and Biology of Sexual Conflict available at www.cshperspectives.org Copyright # 2014 Cold Spring Harbor Laboratory Press; all rights reserved. Advanced Online Article. Cite this article as Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a017517 1 Downloaded from http://cshperspectives.cshlp.org/ on September 24, 2021 - Published by Cold Spring Harbor Laboratory Press H. Kokko and M.D. Jennions only when contrasting them with sexual conflict There are many definitions of sexual selec- models. The investigators of the original models tion, extending Darwin’s original proposal that never describe them as “mutualistic,” which is sexual selection “depends on the advantage that hardly surprising given that some males are re- certain individuals have over other individuals jected by females. of the same sex and species, in exclusive relation In this review, we first define sexual conflict to reproduction” (Darwin 1871, p. 256). One and sexual selection. We then describe how the widely accepted definition is that “sexual selec- notion of a “lag load” can reveal which sex cur- tion is the differences in reproduction that arise rently has greater “power” in a sexual conflict from variation among individuals in traits that over a specific resource. Next, we discuss why affect success in competition over mates and sexual conflict and sexual selection are some- fertilizations” (Andersson 1994, p. 31). There times implicitly (or explicitly) presented as al- can be practical difficulties in applying this ternative explanations for sexual traits (usually definition to identify sexually selected traits. female mate choice/resistance). Toillustrate the For example, is a male stickleback that builds problems with the assumptions made to take a nest selected to do so because it improves off- this stance, we present a “toy model” of snake spring survival (natural selection) or because mating behavior based on a study by Shine et he needs a nest to attract mates? Such “gray al. (2005). We show that empirical predictions zones” aside, sexual selection is a straightfor- about the mating behavior that will be observed ward notion. if females seek to minimize direct cost of mat- Sexual conflict has been defined in many ing or to obtain indirect genetic benefits were subtly different ways, but these definitions all overlysimplistic. This allows us to make the wid- rely on the fact that evolutionary conflicts of er point that whom a female is willing to mate interest can arise whenever two genetically dif- with and how often she mates are often related ferent individuals (“actors”) interact (Dawkins questions. Finally, we discuss the effect of sexual 1976; Dawkins and Krebs 1979; Parker 1979). conflict on population fitness. Sexual conflict is comparable to parent–off- spring conflict (Parker 2006). In both cases there are shared interests between the two actors DEFINING SEXUAL SELECTION (parents“want”theiroffspringtosucceed;males AND SEXUAL CONFLICT and females “want” to breed), but this does not With the exception of artificial experimental preclude disagreements over how this common breeding designs (see below), sexual conflict is goal is achieved. likely to be present whenever there is sexual re- Sexual conflict can occur over every facet production. This is true regardless of whether of breeding. It starts with who will mate search there is anisogamy with males and females or (Hammerstein and Parker 1987), proceeds to isogamy with two or more mating types (Mat- whether to reject or accept a potential mate suda and Abrams 1999). Wetherefore argue that (Parker 1979), and then encompasses how mat- little is gained by asking how sexual selection ing and gamete transfer occur. After mat- will differ in the presence and in the absence ing, there might be conflict over whether or of sexual conflict. It makes more sense to ask not additional matings with other individuals what kinds of traits are favored in each sex, and are favored (Baer et al. 2001; Fromhage 2012). why, given the inevitable existence of sexual Finally, there is conflict over how many off- conflict over at least some aspects of reproduc- spring are produced, when they are produced, tion. Our argument relies on the fact that once and how much each parent invests into these sexual conflict and sexual selection are appro- offspring (e.g., disputes over parental care [Les- priately defined, it is near impossible to envis- sells 2006]). Sexual conflict extends beyond age a biologically plausible situation in which traits under sexual selection in one sex and re- sexual selection exists without sexual conflict, sponses by the other sex to their effects on its or vice versa. fitness. It is a much broader concept. 2 Advanced Online Article. Cite this article as Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a017517 Downloaded from http://cshperspectives.cshlp.org/ on September 24, 2021 - Published by Cold Spring Harbor Laboratory Press Relationship between Sexual Selection and Conflict Despite consensus that sexual conflict arises erroneously conclude that sexual conflict is ab- because of genetic differences between potential sent when sex-specific expression has not yet mates, its definitions are a confusing mixture evolved but would be selected for if it arose? of statements about costs imposed on a single No, because the potential for sex-specific expres- individual during a mating encounter, differ- sion to resolve a conflict does not prevent an- ences in mean fitness between the sexes (or tem- other tool from existing (e.g., alleles that simply poral changes in mean fitness), or lowered pop- lead to the optimal female phenotype at the ex- ulation fitness. To avoid some easy pitfalls, and pense of male fitness). Our definition as a whole to make conceptual points, we propose an un- resembles that of Hosken et al. (2009) who asked orthodox definition that is, hopefully, thought- what would happen if one sex had complete provoking. control of trait expression in the other sex. There is sexual conflict if a hypothetical cost- We have specified that possession of the hy- free “tool” allowed some individuals of sex A to pothetical tool is cost-free because the presence alter what individuals of sex B do at a cost to B, of costs might be the very factor preventing an such that sex A individuals with the “tool” are individual from reducing sexual conflict (from then selectively favored over those without it. its perspective). This, of course, would not The noun “tool” and the verb “to do” mean that sexual conflict had vanished. For ex- should be interpreted broadly. Most obviously, ample, resisting mating attempts might be so individuals of sex B could change their behavior costly for a female turtle that her best option is or morphology when interacting with A indi- to acquiesce (convenience polyandry [Lee and viduals who have the tool. For example, instead Hays 2004]). If she could do something to pre- of B incessantly attempting to mate with A, it vent males from mating, however, and this was now leaves A in peace; or B no longer includes cost-free, then the actual behaviors of males— chemicals in its ejaculate that reduce A’s life- that is, how often they actually mated with her— span.