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Sexual conflict and intrasexual polymorphism promote assortative mating and halt population differentiation.

ABSTRACT: Sexual conflict is thought to be an important evolutionary force in driving phenotypic diversification, population divergence, and speciation. However, empirical evidence is inconsistent with the generality that sexual conflict enhances population divergence. Here, we demonstrate an alternative evolutionary outcome in which sexual conflict plays a conservative role in maintaining male and female polymorphisms locally, rather than promoting population divergence. In diving beetles, female polymorphisms have evolved in response to male mating harassment and sexual conflict. We present the first empirical evidence that this female polymorphism is associated with (i) two distinct and sympatric male morphological mating clusters (morphs) and (ii) assortative mating between male and female morphs. Changes in mating traits in one sex led to a predictable change in the other sex which leads to predictable within-population evolutionary dynamics in male and female morph frequencies. Our results reveal that sexual conflict can lead to assortative mating between male offence and female defence traits, if a stable male and female mating polymorphisms are maintained. Stable male and female mating polymorphisms are an alternative outcome to an accelerating coevolutionary arms race driven by sexual conflict. Such stable polymorphisms challenge the common view of sexual conflict as an engine of rapid speciation via exaggerated coevolution between sexes.

SUBMITTER: Iversen LL

PROVIDER: S-EPMC6452078 | biostudies-literature | 2019 Mar

REPOSITORIES: biostudies-literature

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Sexual conflict and intrasexual polymorphism promote assortative mating and halt population differentiation.

Iversen Lars Lønsmann LL Svensson Erik I EI Christensen Søren Thromsholdt ST Bergsten Johannes J Sand-Jensen Kaj K

Proceedings. Biological sciences 20190301 1899

Sexual conflict is thought to be an important evolutionary force in driving phenotypic diversification, population divergence, and speciation. However, empirical evidence is inconsistent with the generality that sexual conflict enhances population divergence. Here, we demonstrate an alternative evolutionary outcome in which sexual conflict plays a conservative role in maintaining male and female polymorphisms locally, rather than promoting population divergence. In diving beetles, female polymor ...[more]

PMID: 30890096

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Project description:BackgroundSex pheromone communication systems may be a major force driving moth speciation by causing behavioral reproductive isolation via assortative meeting of conspecific individuals. The 'E' and 'Z' pheromone races of the European corn borer (ECB) are a textbook example in this respect. 'Z' females produce and 'Z' males preferentially respond to a 'Z' pheromone blend, while the 'E' race communicates via an 'E' blend. Both races do not freely hybridize in nature and their populations are genetically differentiated. A straightforward explanation would be that their reproductive isolation is a mere consequence of "assortative meeting" resulting from their different pheromones specifically attracting males towards same-race females at long range. However, previous laboratory experiments and those performed here show that even when moths are paired in a small box - i.e., when the meeting between sexual partners is forced - inter-race couples still have a lower mating success than intra-race ones. Hence, either the difference in attractivity of E vs. Z pheromones for males of either race still holds at short distance or the reproductive isolation between E and Z moths may not only be favoured by assortative meeting, but must also result from an additional mechanism ensuring significant assortative mating at close range. Here, we test whether this close-range mechanism is linked to the E/Z female sex pheromone communication system.Methodology/principal findingsUsing crosses and backcrosses of E and Z strains, we found no difference in mating success between full-sisters emitting different sex pheromones. Conversely, the mating success of females with identical pheromone types but different coefficients of relatedness to the two parental strains was significantly different, and was higher when their genetic background was closer to that of their male partner's pheromone race.Conclusions/significanceWe conclude that the close-range mechanism ensuring assortative mating between the E and Z ECB pheromone races is unrelated to the difference in female sex pheromone. Although the nature of this mechanism remains elusive, our results show that it is expressed in females, acts at close range, segregates independently of the autosome carrying Pher and of both sex chromosomes, and is widely distributed since it occurs both in France and in the USA.

Project description:BackgroundA major challenge in evolutionary biology is to understand the typically complex interactions between diverse counter-balancing factors of Darwinian selection for size assortative mating and sexual size dimorphism. It appears that rarely a simple mechanism could provide a major explanation of these phenomena. Mechanics of behaviors can predict animal morphology, such like adaptations to locomotion in animals from various of taxa, but its potential to predict size-assortative mating and its evolutionary consequences has been less explored. Mate-grasping by males, using specialized adaptive morphologies of their forelegs, midlegs or even antennae wrapped around female body at specific locations, is a general mating strategy of many animals, but the contribution of the mechanics of this wide-spread behavior to the evolution of mating behavior and sexual size dimorphism has been largely ignored.ResultsHere, we explore the consequences of a simple, and previously ignored, fact that in a grasping posture the position of the male's grasping appendages relative to the female's body is often a function of body size difference between the sexes. Using an approach taken from robot mechanics we model coercive grasping of females by water strider Gerris gracilicornis males during mating initiation struggles. We determine that the male optimal size (relative to the female size), which gives the males the highest grasping force, properly predicts the experimentally measured highest mating success. Through field sampling and simulation modeling of a natural population we determine that the simple mechanical model, which ignores most of the other hypothetical counter-balancing selection pressures on body size, is sufficient to account for size-assortative mating pattern as well as species-specific sexual dimorphism in body size of G. gracilicornis.ConclusionThe results indicate how a simple and previously overlooked physical mechanism common in many taxa is sufficient to account for, or importantly contribute to, size-assortative mating and its consequences for the evolution of sexual size dimorphism.

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Sexual conflict and intrasexual polymorphism promote assortative mating and halt population differentiation.

Publications

Sexual conflict and intrasexual polymorphism promote assortative mating and halt population differentiation.

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