Male harm suppresses female fitness, affecting the dynamics of adaptation and evolutionary rescue.

One of the most pressing questions we face as biologists is to understand how climate change will affect the evolutionary dynamics of natural populations and how these dynamics will in turn affect population recovery. Increasing evidence shows that sexual selection favors population viability and local adaptation. However, sexual selection can also foster sexual conflict and drive the evolution of male harm to females. Male harm is extraordinarily widespread and has the potential to suppress female fitness and compromise population growth, yet we currently ignore its net effects across taxa or its influence on local adaptation and evolutionary rescue. We conducted a comparative meta-analysis to quantify the impact of male harm on female fitness and found an overall negative effect of male harm on female fitness. Negative effects seem to depend on proxies of sexual selection, increasing inversely to the female relative size and in species with strong sperm competition. We then developed theoretical models to explore how male harm affects adaptation and evolutionary rescue. We show that, when sexual conflict depends on local adaptation, population decline is reduced, but at the cost of slowing down genetic adaptation. This trade-off suggests that eco-evolutionary feedback on sexual conflict can act like a double-edged sword, reducing extinction risk by buffering the demographic costs of climate change, but delaying genetic adaptation. However, variation in the mating system and male harm type can mitigate this trade-off. Our work shows that male harm has widespread negative effects on female fitness and productivity, identifies potential mechanistic factors underlying variability in such costs across taxa, and underscores how acknowledging the condition-dependence of male harm may be important to understand the demographic and evolutionary processes that impact how species adapt to environmental change.

Kin discrimination and demography modulate patterns of sexual conflict.

Recent years have seen an explosion of interest in the overlap between kin selection and sexual selection, particularly concerning how kin selection can put the brakes on harmful sexual conflict. However, there remains a significant disconnect between theory and empirical research. Whilst empirical work has focused on kin-discriminating behaviour, theoretical models have assumed indiscriminating behaviour. Additionally, theoretical work makes particular demographic assumptions that constrain the relationship between genetic relatedness and the scale of competition, and it is not clear that these assumptions reflect the natural setting in which sexual conflict has been empirically studied. Here, we plug this gap between current theoretical and empirical understanding by developing a mathematical model of sexual conflict that incorporates kin discrimination and different patterns of dispersal. We find that kin discrimination and group dispersal inhibit harmful male behaviours at an individual level, but kin discrimination intensifies sexual conflict at the population level.

Does kin discrimination promote cooperation?

Genetic relatedness is a key driver of the evolution of cooperation. One mechanism that may ensure social partners are genetically related is kin discrimination, in which individuals are able to distinguish kin from non-kin and adjust their behaviour accordingly. However, the impact of kin discrimination upon the overall level of cooperation remains obscure. Specifically, while kin discrimination allows an individual to help more-related social partners over less-related social partners, it is unclear whether and how the population average level of cooperation that is evolutionarily favoured should differ under kin discrimination versus indiscriminate social behaviour. Here, we perform a general mathematical analysis in order to assess whether, when and in which direction kin discrimination changes the average level of cooperation in an evolving population. We find that kin discrimination may increase, decrease or leave unchanged the average level of cooperation, depending upon whether the optimal level of cooperation is a convex, concave or linear function of genetic relatedness. We develop an extension of the classic 'tragedy of the commons' model of cooperation in order to provide an illustration of these results. Our analysis provides a method to guide future research on the evolutionary consequences of kin discrimination.

The social evolution of sleep: sex differences, intragenomic conflicts and clinical pathologies.

Sleep appears to be essential for most animals, including humans. Accordingly, individuals who sacrifice sleep are expected to incur costs and so should only be evolutionarily favoured to do this when these costs are offset by other benefits. For instance, a social group might benefit from having some level of wakefulness during the sleeping period if this guards against possible threats. Alternatively, individuals might sacrifice sleep in order to gain an advantage over mate competitors. Here, we perform a theoretical analysis of the social evolutionary pressures that drive investment into sleep versus wakefulness. Specifically, we: investigate how relatedness between social partners may modulate sleeping strategies, depending upon whether sleep sacrifice is selfish or altruistic; determine the conditions under which the sexes are favoured to adopt different sleeping strategies; identify the potential for intragenomic conflict between maternal-origin versus paternal-origin genes regarding an individual's sleeping behaviour; translate this conflict into novel and readily testable predictions concerning patterns of gene expression; and explore the concomitant effects of different kinds of mutations, epimutations, and uniparental disomies in relation to sleep disorders and other clinical pathologies. Our aim is to provide a theoretical framework for future empirical data and stimulate further research on this neglected topic.

Different Genomic Changes Underlie Adaptive Evolution in Populations of Contrasting History.

Experimental evolution is a powerful tool to understand the adaptive potential of populations under environmental change. Here, we study the importance of the historical genetic background in the outcome of evolution at the genome-wide level. Using the natural clinal variation of Drosophila subobscura, we sampled populations from two contrasting latitudes (Adraga, Portugal and Groningen, Netherlands) and introduced them in a new common environment in the laboratory. We characterized the genome-wide temporal changes underlying the evolutionary dynamics of these populations, which had previously shown fast convergence at the phenotypic level, but not at chromosomal inversion frequencies. We found that initially differentiated populations did not converge either at genome-wide level or at candidate SNPs with signs of selection. In contrast, populations from Portugal showed convergence to the control population that derived from the same geographical origin and had been long-established in the laboratory. Candidate SNPs showed a variety of different allele frequency change patterns across generations, indicative of an underlying polygenic basis. We did not detect strong linkage around candidate SNPs, but rather a small but long-ranging effect. In conclusion, we found that history played a major role in genomic variation and evolution, with initially differentiated populations reaching the same adaptive outcome through different genetic routes.

Predictable phenotypic, but not karyotypic, evolution of populations with contrasting initial history.

The relative impact of selection, chance and history will determine the predictability of evolution. There is a lack of empirical research on this subject, particularly in sexual organisms. Here we use experimental evolution to test the predictability of evolution. We analyse the real-time evolution of Drosophila subobscura populations derived from contrasting European latitudes placed in a novel laboratory environment. Each natural population was sampled twice within a three-year interval. We study evolutionary responses at both phenotypic (life-history, morphological and physiological traits) and karyotypic levels for around 30 generations of laboratory culture. Our results show (1) repeatable historical effects between years in the initial state, at both phenotypic and karyotypic levels; (2) predictable phenotypic evolution with general convergence except for body size; and (3) unpredictable karyotypic evolution. We conclude that the predictability of evolution is contingent on the trait and level of organization, highlighting the importance of studying multiple biological levels with respect to evolutionary patterns.

Sexual selection modulates genetic conflicts and patterns of genomic imprinting.

Recent years have seen a surge of interest in linking the theories of kin selection and sexual selection. In particular, there is a growing appreciation that kin selection, arising through demographic factors such as sex-biased dispersal, may modulate sexual conflicts, including in the context of male-female arms races characterized by coevolutionary cycles. However, evolutionary conflicts of interest need not only occur between individuals, but may also occur within individuals, and sex-specific demography is known to foment such intragenomic conflict in relation to social behavior. Whether and how this logic holds in the context of sexual conflict-and, in particular, in relation to coevolutionary cycles-remains obscure. We develop a kin-selection model to investigate the interests of different genes involved in sexual and intragenomic conflict, and we show that consideration of these conflicting interests yields novel predictions concerning parent-of-origin specific patterns of gene expression and the detrimental effects of different classes of mutation and epimutation at loci underpinning sexually selected phenotypes.

Keeping your options open: Maintenance of thermal plasticity during adaptation to a stable environment.

Phenotypic plasticity may allow species to cope with environmental variation. The study of thermal plasticity and its evolution helps understanding how populations respond to variation in temperature. In the context of climate change, it is essential to realize the impact of historical differences in the ability of populations to exhibit a plastic response to thermal variation and how it evolves during colonization of new environments. We have analyzed the real-time evolution of thermal reaction norms of adult and juvenile traits in Drosophila subobscura populations from three locations of Europe in the laboratory. These populations were kept at a constant temperature of 18ºC, and were periodically assayed at three experimental temperatures (13ºC, 18ºC, and 23ºC). We found initial differentiation between populations in thermal plasticity as well as evolutionary convergence in the shape of reaction norms for some adult traits, but not for any of the juvenile traits. Contrary to theoretical expectations, an overall better performance of high latitude populations across temperatures in early generations was observed. Our study shows that the evolution of thermal plasticity is trait specific, and that a new stable environment did not limit the ability of populations to cope with environmental challenges.

Sex-biased dispersal, kin selection and the evolution of sexual conflict.

There is growing interest in resolving the curious disconnect between the fields of kin selection and sexual selection. Rankin's (2011, J. Evol. Biol. 24, 71-81) theoretical study of the impact of kin selection on the evolution of sexual conflict in viscous populations has been particularly valuable in stimulating empirical research in this area. An important goal of that study was to understand the impact of sex-specific rates of dispersal upon the coevolution of male-harm and female-resistance behaviours. But the fitness functions derived in Rankin's study do not flow from his model's assumptions and, in particular, are not consistent with sex-biased dispersal. Here, we develop new fitness functions that do logically flow from the model's assumptions, to determine the impact of sex-specific patterns of dispersal on the evolution of sexual conflict. Although Rankin's study suggested that increasing male dispersal always promotes the evolution of male harm and that increasing female dispersal always inhibits the evolution of male harm, we find that the opposite can also be true, depending upon parameter values.