Sexual conflict coevolution - population size, divergence and the emergence of new variation

Lead Research Organisation: University of Exeter
Department Name: Biosciences

Abstract

The role of selection in the generation of biodiversity is an exciting and controversial topic. It has long been recognised that adaptation to new environments can lead to the evolution of new forms, but recently there has been great interest in the potential for sexual selection and in particular sexual conflict to drive rapid evolution. The theory is that males are under constant pressure to evolve new ways to manipulate their mates so that they invest more in the offspring of that particular male rather than any of their past or future mates. Females in turn are under strong selection to regain control over their reproduction and optimise their own reproductive success rather than that of their mate's. There is some evidence for intraspecific arms-races but the key question of the extent to which sexual conflict can drive rapid evolution and population divergence remains poorly studied and several key issues remain almost completely neglected, particularly: 1. How important is population size in promoting or retarding evolution driven by sexual conflict? 2. Is divergence faster between small populations because random loss of alleles through genetic drift is important, or in large populations because there is greater mutational input and more standing genetic variation? 3. Can mutational input cause populations to vary in the rate of adaptation or is the level of standing variation always more important? These questions are of great interest to biologists attempting to understand the genesis and maintenance of variation. They also have implications for the design of conservation and captive breeding programmes where larger populations are more expensive to rear, but may retain more genetic variation and experience higher overall mutational inputs. A major problem in studying antagonistic coevolution, is that counter-adaptations often mask the adaptations which have driven their evolution. For instance a new male seminal chemical that accelerates egg laying might only be identified by observing the effects of males on their partners. However, once females evolve lack of sensitivity to the male chemical, it no longer becomes possible to detect either the adaptation or the counter-adaptation. In this proposal we use a novel approach to reveal such variation: we utilise a population of beetles Callosobruchus maculatus that naturally have substantial sexual conflict driven adaptations and counter-adaptations. Our study begins with populations that we have been keeping for over 7 years (90+ generations) under conditions of enforced monogamy (females and males only allowed a single mate). These monogamy populations will have lost many of their conflict adaptations and much of their genetic diversity. We will re-introduce sexual selection and sexual conflict to this system by creating a range of new populations where the natural mating regime is allowed, including conflicts of interest between males and females. These experimental populations will include replicates that differ in overall population size, and initial levels of standing genetic variation. We will examine populations at intervals crossing the new conflict populations with the baseline monogamy population to reveal new adaptations to conflict and the re-establishment of conflict traits that have been reduced to low frequencies by the removal of their selective advantages in the monogamy lines. After 30 generations we will conduct crosses between populations to gain direct measures of the degree of reproductive isolation that has evolved during our study and the influence that population size and genetic diversity has had on this process. Our study will reveal how rapidly sexual conflict can drive evolution, how this can translate into divergence between populations (the fuel for speciation) and the influences of population size and genetic variability on the rate of antagonistic coevolution.

Publications


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Gay L (2011) The evolution of harm--effect of sexual conflicts and population size. in Evolution; international journal of organic evolution
GAY L (2009) Costly sexual harassment in a beetle in Physiological Entomology
SHARMA M (2011) Sex combs, allometry, and asymmetry in Drosophila in Biological Journal of the Linnean Society
Wedell N (2008) Nuptial gifts fail to resolve a sexual conflict in an insect. in BMC evolutionary biology
 
Description Recently there has been great interest in the potential for sexual selection to drive rapid evolution. The theory is that males are under constant pressure to evolve new ways to manipulate their mates so that they invest more in the offspring of that particular male. Females in turn are under strong selection to regain control over their reproduction.



We used a novel approach to answer important questions about the demographic factors that facilitate or impede coevolutionary arms races caused by conflicts of interest between the sexes. We utilised a population of beetles that naturally have substantial sexual conflict driven adaptations and counter-adaptations. Our study began with populations that we had kept for 90+ generations under conditions of enforced monogamy (females and males only allowed a single mate). These monogamy populations had lost some of their conflict adaptations. We re-introduced sexual selection and sexual conflict to this system by creating a range of new populations where the natural mating regime was allowed. These experimental populations included replicates that differed in overall population size, and initial levels of standing genetic variation. After 19 generations we conducted crosses between populations to measure the degree of reproductive isolation that had evolved. This revealed that none of our treatments had evolved significant overall reproductive isolation among replicate lines. However, as predicted, measures of reproductive isolation tended to be greater among larger populations. Additionally we tested each population against a reference population after 30 generations of reintroduced conflict. We found that conflict favoured males that harmed females and more resistant females. Large population size rather than high initial genetic variation allowed males to evolve faster and become more harmful. This indicates that sexual selection creates conditions where males benefit from harming females and this selection is more effective in larger populations.
Exploitation Route Eventually, this work will inform efforts to manage conservation projects and possibly captive animal populations. None are obvious
Sectors Environment
 
Description This work has yet to make an impact outisde of its original intended outcome of furthering our understanding of the living world. This is an endeavour which will have incalculable impact over the longer term.