Detecting sexual conflict and sexually antagonistic coevolution

We begin by providing an operational definition of sexual conflict that applies to both inter- and intralocus conflict. Using this definition, we examine a series of simple coevolutionary models to elucidate fruitful approaches for detecting interlocus sexual conflict and resultant sexually antagonistic coevolution. We then use published empirical examples to illustrate the utility of these approaches. Three relevant attributes emerge. First, the dynamics of sexually antagonistic coevolution may obscure the conflict itself. Second, competing models of inter-sexual coevolution may yield similar population patterns near equilibria. Third, a variety of evolutionary forces underlying competing models may be acting simultaneously near equilibria. One main conclusion is that studies of emergent patterns in extant populations (e.g. studies of population and/or female fitness) are unlikely to allow us to distinguish among competing coevolutionary models. Instead, we need more research aimed at identifying the forces of selection acting on shared traits and sexually antagonistic traits. More specifically, we need a greater number of functional studies of female traits as well as studies of the consequences of both male and female traits for female fitness. A mix of selection and manipulative studies on these is likely the most promising route.     

Detecting sexually antagonistic coevolution with population crosses

The result of population crosses on traits such as mating rate, oviposition rate and survivorship are increasingly used to distinguish between modes of coevolution between the sexes. Two key hypotheses, erected from a verbal theory of sexually antagonistic coevolution, have been the subject of several recent tests. First, statistical interactions arising in population crosses are suggested to be indicative of a complex signal/receiver system. In the case of oviposition rates, an interaction between populations (x, y and z) would be indicated by the rank order of female oviposition rates achieved by x, y and z males changing depending upon the female (x, y or z) with which they mated. Second, under sexually antagonistic coevolution females will do 'best' when mated with their own males, where best is defined by the weakest response to the signal and the highest fitness. We test these hypotheses by crossing strains generated from a formal model of sexually antagonistic coevolution. Strains differ in the strength of natural selection acting on male and female traits. In our model, we assume sexually antagonistic coevolution of a single male signal and female receptor. The female receptor is treated as a preference function where both the slope and intercept of the function can evolve. Our results suggest that neither prediction is consistently supported. Interactions are not diagnostic of complex signal-receiver systems, and even under sexually antagonistic coevolution, females may do better mating with males of strains other than their own. These results suggest a reinterpretation of several recent experiments and have important implications for developing theories of speciation when sexually antagonistic coevolution is involved.     

Sexual conflict and antagonistic coevolution across water strider populations

Microevolutionary studies have demonstrated sexually antagonistic selection on sexual traits, and existing evidence supports a macroevolutionary pattern of sexually antagonistic coevolution. Two current questions are how antagonistic selection within-populations scales to divergence among populations, and to what extent intraspecific divergence matches species-level patterns. To address these questions, we conducted an intraspecific comparative study of sexual armaments and mating behaviors in a water strider (Gerris incognitus) in which male genitals grasp resistant females and female abdominal structures help ward off males. The degree of exaggeration of these armaments coevolves across species. We found a similar strong pattern of antagonistic coevolution among populations, suggesting that sexual conflict drives population differentiation in morphology. Furthermore, relative exaggeration in armaments was closely related to mating outcomes in a common environment. Interestingly, the effect of armaments on mating was mediated by population sexual size dimorphism. When females had a large size advantage, mating activity was low and independent of armaments, but when males had a relative size advantage, mating activity depended on which sex had relatively exaggerated armaments. Thus, a strong signal of sexually antagonistic coevolution is apparent even among populations. These results open opportunities to understand links between sexual arms races, ecological variation, and reproductive isolation.     

The impact of parasite dispersal on antagonistic host-parasite coevolution

Coevolving populations of hosts and parasites are often subdivided into a set of patches connected by dispersal. Higher relative rates of parasite compared with host dispersal are expected to lead to parasite local adaptation. However, we know of no studies that have considered the implications of higher relative rates of parasite dispersal for other aspects of the coevolutionary process, such as the rate of coevolution and extent of evolutionary escalation of resistance and infectivity traits. We investigated the effect of phage dispersal on coevolution in experimental metapopulations of the bacterium Pseudomonas fluorescens SBW25 and its viral parasite, phage SBW25Phi2. Both the rate of coevolution and the breadth of evolved infectivity and resistance ranges peaked at intermediate rates of parasite dispersal. These results suggest that parasite dispersal can enhance the evolutionary potential of parasites through provision of novel genetic variation, but that high rates of parasite dispersal can impede the evolution of parasites by homogenizing genetic variation between patches, thereby constraining coevolution.     

The coevolution of human fertility and wealth inheritance strategies.

Life history theory concerns the scheduling of births and the level of parental investment in each offspring. In most human societies the inheritance of wealth is an important part of parental investment. Patterns of wealth inheritance and other reproductive decisions, such as family size, would be expected to influence each other. Here I present an adaptive model of human reproductive decision-making, using a state-dependent dynamic model. Two decisions made by parents are considered: when to have another baby, and thus the pattern of reproduction through life; and how to allocate resources between children at the end of the parents'' life. Optimal decision rules are those that maximize the number of grandchildren. Decisions are assumed to depend on the state of the parent, which is described at any time by two variables: number of living sons, and wealth. The dynamics of the model are based on a traditional African pastoralist system, but it is general enough to approximate to any means of subsistence where an increase in the amount of wealth owned increases the capacity for future production of resources. The model is used to show that, in the unpredictable environment of a traditional pastoralist society, high fertility and a biasing of wealth inheritance to a small number of children are frequently optimal. Most such societies are now undergoing a transition to lower fertility, known as the demographic transition. The effects on fertility and wealth inheritance strategies of reducing mortality risks, reducing the unpredictability of the environment and increasing the costs of raising children are explored. Reducing mortality has little effect on completed family sizes of living children or on the wealth they inherit. Increasing the costs of raising children decreases optimal fertility and increases the inheritance left to each child at each level of wealth, and has the potential to reduce fertility to very low levels. The results offer an explanation for why wealthy families are frequently also those with the smallest number of children in heterogeneous, post-transition societies.     

Rapid antagonistic coevolution between strains of the social amoeba Dictyostelium discoideum

Social groups face a fundamental problem of overcoming selfish individuals capable of destroying cooperation. In the social amoeba Dictyostelium discoideum, there is evidence that some clones (‘cheaters’) contribute disproportionately to the viable spores in a fruiting body while avoiding the dead stalk cell fate. It remains unclear, however, whether this cheating is actually the product of selection. Here, I report the results of an experimental evolution study designed to test whether clones of D. discoideum will evolve resistance to cheating in the laboratory with genetic variation created only through spontaneous mutation. Two strains, one green fluorescent protein (GFP)-labelled and one wild-type, were allowed to grow and develop together before the wild-type strain was removed and replaced with a naïve strain evolving in parallel. Over the course of 10 social generations, the GFP-labelled strain reliably increased its representation in the spores relative to control populations that had never experienced the competitor. This competitive advantage extended to the non-social, vegetative growth portion of the life cycle, but not to pairwise competition with two other strains. These results indicate strong antagonism between strains, mediated by ample mutational variation for cheating and also suggest that arms races between strains in the wild may be common.     

Inter-genomic sexual conflict drives antagonistic coevolution in harvester ants

The reproductive interests of males and females are not always aligned, leading to sexual conflict over parental investment, rate of reproduction and mate choice. Traits that increase the genetic interests of one sex often occur at the expense of the other, selecting for counter-adaptations leading to antagonistic coevolution. Reproductive conflict is not limited to intraspecific interactions; interspecific hybridization can produce pronounced sexual conflict between males and females of different species, but it is unclear whether such conflict can drive sexually antagonistic coevolution between reproductively isolated genomes. We tested for hybridization-driven sexually antagonistic adaptations in queens and males of the socially hybridogenetic ‘J’ lineages of Pogonomyrmex harvester ants, whose mating system promotes hybridization in queens but selects against it in males. We conducted no-choice mating assays to compare patterns of mating behaviour and sperm transfer between inter- and intra-lineage pairings. There was no evidence for mate discrimination on the basis of pair type, and the total quantity of sperm transferred did not differ between intra- and inter-lineage pairs; however, further dissection of the sperm transfer process into distinct mechanistic components revealed significant, and opposing, cryptic manipulation of copulatory investment by both sexes. Males of both lineages increased their rate of sperm transfer to high-fitness intra-lineage mates, with a stronger response in the rarer lineage for whom mating mistakes are the most likely. By contrast, the total duration of copulation for intra-lineage mating pairs was significantly shorter than for inter-lineage crosses, suggesting that queens respond to prevent excessive sperm loading by prematurely terminating copulation. These findings demonstrate that sexual conflict can lead to antagonistic coevolution in both intra-genomic and inter-genomic contexts. Indeed, the resolution of sexual conflict may be a key determinant of the long-term evolutionary potential of host-dependent reproductive strategies, counteracting the inherent instabilities arising from such systems.     

Host population bottlenecks drive parasite extinction during antagonistic coevolution

Host–parasite interactions are often characterized by large fluctuations in host population size, and we investigated how such host bottlenecks affected coevolution between a bacterium and a virus. Previous theory suggests that host bottlenecks should provide parasites with an evolutionary advantage, but instead we found that phages were rapidly driven to extinction when coevolving with hosts exposed to large genetic bottlenecks. This was caused by the stochastic loss of sensitive bacteria, which are required for phage persistence and infectivity evolution. Our findings emphasize the importance of feedbacks between ecological and coevolutionary dynamics, and how this feedback can qualitatively alter coevolutionary dynamics.     

Short- and long-term benefits and detriments to recombination under antagonistic coevolution

We explored the evolution of recombination under antagonistic coevolution, concentrating on the equilibrium frequencies of modifier alleles causing recombination in initially nonrecombining populations. We found that the equilibrium level of recombination in the host depended not only on parasite virulence, but also on the strength of the modifier allele, and on whether or not the modifier was physically linked to the parasite interaction loci. Nonetheless, the maximum level of recombination for linked loci at equilibrium was about 0.3 (60% of free recombination) for interactions with highly virulent parasites; the level decreased for unlinked modifiers, and for lower levels of parasite virulence. We conclude that recombination spreads because it provides a combination of an immediate (next-generation) fitness benefit and a delayed (two or more generations) increase in the rate of response to directional selection. The relative impact of these two mechanisms depends on the virulence of parasites early in the spread of the modifier, but a trade-off between the two dictates the equilibrium modifier frequency for all nonzero virulences that we examined. In addition, population mean fitness was higher in populations at intermediate equilibria than populations fixed for free recombination or no recombination. The difference, however, was not enough on its own to overcome the two-fold cost of producing males.     

The impact of migration from parasite-free patches on antagonistic host-parasite coevolution

Natural populations of hosts and parasites are often subdivided and patchily distributed such that some regions of a host species' range will be free from a given parasite. Host migration from parasite-free to parasite-containing patches is expected to alter coevolutionary dynamics by changing the evolutionary potential of antagonists. Specifically, host immigration can favor parasites by increasing transmission opportunities, or hosts by introducing genetic variation. We tested these predictions in coevolving populations of Pseudomonas fluorescens and phage Phi2 that received immigrants from phage-free populations. We observed a negative quadratic relationship between sympatric resistance to phage and host immigration rate (highest at intermediate immigration) but a positive quadratic relationship between coevolution rate and host immigration rate (lowest at intermediate immigration). These results indicate that for a wide range of rates, host immigration from parasite-free patches can increase the evolutionary potential of parasites, and increase the coevolutionary rate if parasite adaptation is limiting in the absence of immigration.     

Effects of antagonistic coevolution on parasite‐mediated host coexistence

Parasites can promote diversity by mediating coexistence between a poorer and superior competitor, if the superior competitor is more susceptible to parasitism. However, hosts and parasites frequently undergo antagonistic coevolution. This process may result in the accumulation of pleiotropic fitness costs associated with host resistance, and could breakdown coexistence. We experimentally investigated parasite‐mediated coexistence of two genotypes of the bacterium Pseudomonas fluorescens, where one genotype underwent coevolution with a parasite (a virulent bacteriophage), whereas the other genotype was resistant to the evolving phages at all time points, but a poorer competitor. In the absence of phages, the resistant genotype was rapidly driven extinct in all populations. In the presence of the phages, the resistant genotype persisted in four of six populations and eventually reached higher frequencies than the sensitive genotype. The coevolving genotype showed a reduction in the growth rate, consistent with a cost of resistance, which may be responsible for a decline in its relative fitness. These results demonstrate that the stability of parasite‐mediated coexistence of resistant and susceptible species or genotypes is likely to be affected if parasites and susceptible hosts coevolve.     

Rapid antagonistic coevolution between primary and secondary sexual characters in horned beetles

Different structures may compete during development for a shared and limited pool of resources to sustain growth and differentiation. The resulting resource allocation trade-offs have the potential to alter both ontogenetic outcomes and evolutionary trajectories. However, little is known about the evolutionary causes and consequences of resource allocation trade-offs in natural populations. Here, we explore the significance of resource allocation trade-offs between primary and secondary sexual traits in shaping early morphological divergences between four recently separated populations of the horned beetle Onthophagus taurus as well as macroevolutionary divergence patterns across 10 Onthophagus species. We show that resource allocation trade-offs leave a strong signature in morphological divergence patterns both within and between species. Furthermore, our results suggest that genital divergence may, under certain circumstances, occur as a byproduct of evolutionary changes in secondary sexual traits. Given the importance of copulatory organ morphology for reproductive isolation our findings begin to raise the possibility that secondary sexual trait evolution may promote speciation as a byproduct. We discuss the implications of our results on the causes and consequences of resource allocation trade-offs in insects.     

Rapid genetic change underpins antagonistic coevolution in a natural host-pathogen metapopulation

Antagonistic coevolution is a critical force driving the evolution of diversity, yet the selective processes underpinning reciprocal adaptive changes in nature are not well understood. Local adaptation studies demonstrate partner impacts on fitness and adaptive change, but do not directly expose genetic processes predicted by theory. Specifically, we have little knowledge of the relative importance of fluctuating selection vs. arms-race dynamics in maintaining polymorphism in natural systems where metapopulation processes predominate. We conducted cross-year epidemiological, infection and genetic studies of multiple wild host and pathogen populations in the Linum-Melampsora association. We observed asynchronous phenotypic fluctuations in resistance and infectivity among demes. Importantly, changes in allelic frequencies at pathogen infectivity loci, and in host recognition of these genetic variants, correlated with disease prevalence during natural epidemics. These data strongly support reciprocal coevolution maintaining balanced resistance and infectivity polymorphisms, and highlight the importance of characterising spatial and temporal dynamics in antagonistic interactions.     

Trophic network structure emerges through antagonistic coevolution in temporally varying environments

Understanding the mechanisms underlying ecological specialization is central to our understanding of community ecology and evolution. Although theoretical work has investigated how variable environments may affect specialization in single species, little is known about how such variation impacts bipartite network structure in antagonistically coevolving systems. Here, we develop and analyse a general model of victim-enemy coevolution that explicitly includes resource and population dynamics. We investigate how temporal environmental heterogeneity affects the evolution of specialization and associated community structure. Environmental productivity influences victim investment in resistance, which will shape patterns of specialization through its regulating effect on enemy investment in infectivity. We also investigate the epidemiological consequences of environmental variability and show that enemy population density is maximized for intermediate lengths of productive seasons, which corresponds to situations where enemies can evolve higher infectivity than victims can evolve defence. We discuss our results in the light of empirical studies, and further highlight ways in which our model applies to a range of natural systems.     

The dynamics of sexually antagonistic coevolution and the complex influences of mating system and genetic correlation

Sexual conflict has been proposed to be a mediator of speciation but recent theoretical work, as well as empirical studies, suggests that sexual conflict may also be able to prevent speciation and to preserve genetic polymorphism within a species. Here, we develop a population genetic model and study the effects of sexual conflict in a polymorphic population. The morphs mate assortatively based on different sexually antagonistic traits and females are assumed to suffer a cost when the proportion of matching males is high. We consider the model in two different mating systems; promiscuity and polygyny. Our results show that genetic polymorphism may be maintained through negative frequency dependent selection established by assortative mating and female conflict costs. However, the outcome significantly differs between mating systems. Furthermore, we show that indirect selection may have profound effects on the evolutionary dynamics of a sexual conflict.     

Molecular evolution of imprinted genes: no evidence for antagonistic coevolution.

Genomically imprinted genes are those for which expression is dependent on the sex of the parent from which they are derived. Numerous theories have been proposed for the evolution of genomic imprinting: one theory is that it is an intra-individual manifestation of classical parent -offspring conflict. This theory is unique in predicting that an arms race may develop between maternally and paternally derived genes for the control of foetal growth demands. Such antagonistic coevolution may be mediated through changes in the structure of the proteins concerned. Comparable coevolution is the most likely explanation for the rapid changes seen in antigenic components of parasites and antigen recognition components of immune systems. We have examined the evolution of insulin-like growth factor Igf2, and its antagonistic receptor Igf2r) and find that in contrast to immune genes, at the sites of mutual binding they are highly conserved. In addition, we have analysed the rate of molecular evolution of seven imprinted genes including Igf2 and Igf2r), sequenced in both mouse and rat, and had that this is the same as that of nonimprinted receptors and significantly lower than that of immune genes controlling for differences in mutation rates. Contrary to the expectations of the conflict hypothesis, we hence find no evidence for antagonistic coevolution of imprinted genes mediated by changes in sequence.     

The evolution of hybrid infertility: perpetual coevolution between gender-specific and sexually antagonistic genes

A new hypothesis is proposed for the rapid evolution of postzygotic reproductive isolation via hybrid infertility. The hypothesis is motivated by two lines of experimental research from Drosophila melanogaster that demonstrate that sexually antagonistic fitness variation is abundant and that epistatic fitness variation on the Y chromosome is common. The hypothesis states that the expression of sexually antagonistic genes leads to a gender-load in each sex. In response, gender-limited reproductive genes are selected to ameliorate, through pleiotropy, the expression of sexually antagonistic genes. Chronic coevolution between gender-limited genes and gender-unlimited sexually antagonistic genes causes rapid divergence of reproductive proteins among allopatric populations, ultimately leading to hybrid infertility.     

Pulsed-resource dynamics increase the asymmetry of antagonistic coevolution between a predatory protist and a prey bacterium

Temporal resource fluctuations could affect the strength of antagonistic coevolution through population dynamics and costs of adaptation. We studied this by coevolving the prey bacterium Serratia marcescens with the predatory protozoa Tetrahymena thermophila in constant and pulsed-resource environments for approximately 1300 prey generations. Consistent with arms race theory, the prey evolved to be more defended, whereas the predator evolved to be more efficient in consuming the bacteria. Coevolutionary adaptations were costly in terms of reduced prey growth in resource-limited conditions and less efficient predator growth on nonliving resource medium. However, no differences in mean coevolutionary changes or adaptive costs were observed between environments, even though resource pulses increased fluctuations and mean densities of coevolving predator populations. Interestingly, a surface-associated prey defence mechanism (bacterial biofilm), to which predators were probably unable to counter-adapt, evolved to be stronger in pulsed-resource environment. These results suggest that temporal resource fluctuations can increase the asymmetry of antagonistic coevolution by imposing stronger selection on one of the interacting species.