The role of indirect effects in coevolution as mutualism transitions into antagonism

Species interactions have evolved from antagonistic to mutualistic and back several times throughout life's history. Yet, it is unclear how changes in the type of interaction between species alter the coevolutionary dynamics of entire communities. This is a pressing matter, as transitions from mutualisms to antagonisms may be becoming more common with human-induced global change. Here, we combine network and evolutionary theory to simulate how shifts in interaction types alter the coevolution of empirical communities. We show that as mutualistic networks shift to antagonistic, selection imposed by direct partners begins to outweigh that imposed by indirect partners. This weakening of indirect effects is associated with communities losing their tight integration of traits and increasing their rate of adaptation. The above changes are more pronounced when specialist consumers are the first species to switch to antagonism. A shift in the outcome of species' interactions may therefore reverberate across communities and alter the direction and speed of coevolution.

Development of a Set of Microsatellite Markers to Investigate Sexually Antagonistic Selection in the Invasive Ant Nylanderia fulva

Sexually antagonistic selection (SAS) occurs when distinct alleles are differentially selected in each sex. In the invasive tawny crazy ant, Nylanderia fulva, a genomic region is under SAS, while the rest of the genome is randomly selected in males and females. In this study, we designed a suite of 15 microsatellite markers to study the origin and evolution of SAS in N. fulva. These SAS markers were polymorphic, with allelic frequencies that are highly different between males and females. All haploid males carry only a subset of the alleles present in the population, while females are reliably heterozygous, with one allele from the male gene pool and a different allele inherited from their mother. In addition, we identified six polymorphic markers not associated with SAS and six markers yielding consistent, yet monomorphic, amplification in the introduced range of this species. Reaction condition optimizations allowed all retained markers to be co-amplified in four PCR mixes. The SAS markers may be used to test for the strength and the extent of the genomic regions under SAS in both the native and introduced ranges of N. fulva, while the set of non-SAS loci may be used to assess the invasion route of this species. Overall, the application of these microsatellite markers will yield insights into the origin and evolution of SAS within and among species of the genus Nylanderia.

The genetic architecture of sexual dimorphism in the mossCeratodon purpureus

A central problem in evolutionary biology is to identify the forces that maintain genetic variation for fitness in natural populations. Sexual antagonism, in which selection favours different variants in males and females, can slow the transit of a polymorphism through a population or can actively maintain fitness variation. The amount of sexually antagonistic variation to be expected depends in part on the genetic architecture of sexual dimorphism, about which we know relatively little. Here, we used a multivariate quantitative genetic approach to examine the genetic architecture of sexual dimorphism in a scent-based fertilization syndrome of the mossCeratodon purpureus.We found sexual dimorphism in numerous traits, consistent with a history of sexually antagonistic selection. The cross-sex genetic correlations (rmf) were generally heterogeneous with many values indistinguishable from zero, which typically suggests that genetic constraints do not limit the response to sexually antagonistic selection. However, we detected no differentiation between the female- and male-specific trait (co)variance matrices (GfandGm, respectively), meaning the evolution of sexual dimorphism may be constrained. The cross-sex cross-trait covariance matrixBcontained both symmetric and asymmetric elements, indicating that the response to sexually antagonistic or sexually concordant selection, and the constraint to sexual dimorphism, are highly dependent on the traits experiencing selection. The patterns of genetic variances and covariances among these fitness components is consistent with partly sex-specific genetic architectures having evolved in order to partially resolve multivariate genetic constraints (i.e. sexual conflict), enabling the sexes to evolve towards their sex-specific multivariate trait optima.

Establishment of a new sex-determining allele driven by sexually antagonistic selection

The turnover of sex-determining loci has repeatedly occurred in a number of species, rather than having a diverged pair of sex chromosomes. We model the turnover process by considering a linked locus under sexually antagonistic selection. The entire process of a turnover may be divided into two phases, which are referred to as the stochastic and deterministic phases. The stochastic phase is when a new sex-determining allele just arises and is still rare and random genetic drift plays an important role. In the deterministic phase, the new allele further increases in frequency by positive selection. The theoretical results currently available are for the deterministic phase, which demonstrated that a turnover of a newly arisen sex-determining locus could benefit from selection at a linked locus under sexually antagonistic selection, by assuming that sexually antagonistic selection works in a form of balancing selection. In this work, we provide a comprehensive theoretical description of the entire process from the stochastic phase to the deterministic phase. In addition to balancing selection, we explore several other modes of selection on the linked locus. Our theory allows us make a quantitative argument on the rate of turnover and the effect of the mode of selection at the linked locus. We also performed simulations to explore the pattern of polymorphism around the new sex-determining locus. We find that the pattern of polymorphism is informative to infer how selection worked through the turnover process.

Evidence for tactically antagonistic selection on body size and the sword in a wild population of the swordtail fish, Xiphophorus multilineatus

Intralocus conflict has been well documented between the sexes, but much less is known about the potential for this genetic conflict in other polymorphisms, such as alternative reproductive tactics. Here we investigate two of three criteria necessary for demonstrating intralocus tactical conflict: the ARTs have different phenotypic optima for a shared trait, and one or both ARTs are not at their phenotypic optima for a shared trait. We address these two criteria in Xiphophorus multilineatus, a live-bearing freshwater fish that has two male alternative reproductive tactics, a behaviorally fixed courter male and a behaviorally plastic sneaker male that switches between courtship and force-copulatory behavior. We used measures of reproductive success from a wild population to estimate selection gradients on three tactically dimorphic traits involved in sexual selection: body size, body shape, and sword length. We present evidence that both body size and sword length are experiencing tactically antagonistic selection, providing evidence for both criteria. Additionally, selection on body shape in sneaker males appears to be buffered due to behavioral plasticity. Our study provides novel insight from a wild population into the role that intralocus tactical conflict can play in constraining ARTs from reaching their respective phenotypic optima despite tactical dimorphism.

Microgeographic divergence of functional responses among salamanders under antagonistic selection from apex predators

A predator's functional response determines predator–prey interactions by describing the relationship between the number of prey available and the number eaten. Its shape and parameters fundamentally govern the dynamic equilibrium of predator–prey interactions and their joint abundances. Yet, estimates of these key parameters generally assume stasis in space and time and ignore the potential for local adaptation to alter feeding responses and the stability of trophic dynamics. Here, we evaluate if functional responses diverge among populations of spotted salamander ( Ambystoma maculatum ) larvae that face antagonistic selection on feeding strategies based on their own risk of predation. Common garden experiments revealed that spotted salamander from ponds with varying predation risks differed in their functional responses, suggesting an evolutionary response. Applying mechanistic equations, we discovered that the combined changes in attack rates, handling times and shape of the functional response enhanced feeding rate in environments with high densities of gape-limited predators. We suggest how these parameter changes could alter community equilibria and other emergent properties of food webs. Community ecologists might often need to consider how local evolution at fine scales alters key relationships in ways that alter local diversity patterns, food web dynamics, resource gradients and community responses to disturbance.

Establishment of a new sex-determining allele driven by sexually antagonistic selection

ABSTRACTSome species undergo frequent turnovers of sex-determining locus, rather than having stable diverged sex chromosomes. In such species, how often turnover occurs is a fundamental evolutionary question. We model the process with considering a linked locus under sexually antagonistic selection. The entire process of a turnover may be divided into two phases, which are referred to as the stochastic and deterministic phases. The stochastic phase is when a new sex-determining allele just arises and is still rare and random genetic drift plays an important role. In the deterministic phase, the new allele further increases in frequency by positive selection. The theoretical results currently available are for the deterministic phase, which demonstrated that a turnover of a newly arisen sex determining locus could benefit from selection at a linked locus under sexually antagonistic selection, by assuming that sexually antagonistic selection works in a form of balancing selection. In this work, we provide a comprehensive theoretical description of the entire process from the stochastic phase to the deterministic phase. In addition to balancing selection, we explore several other modes of selection on the linked locus. Our theory allows us make a quantitative argument on the rate of turnover and the effect of the mode of selection at the linked locus. We also performed simulations to explore the pattern of polymorphism around the new sex determining locus. We find that the pattern of polymorphism is informative to infer how selection worked through the turnover process.

Detection of sexually antagonistic transmission distortions in trio datasets

ABSTRACTSex dimorphisms are widespread in animals and plants, for morphological as well as physiological traits. Understanding the genetic basis of sex dimorphism and its evolution is crucial for understanding biological differences between the sexes. Genetic variants with sex-antagonistic effects on fitness are expected to segregate in populations at the early phases of sexual dimorphism emergence. Detecting such variants is notoriously difficult, and the few genome-scan methods employed so far have limited power and little specificity. Here, we propose a new framework to detect a signature of sexually antagonistic selection. We rely on trio datasets where sex-biased transmission distortions can be directly tracked from parents to offspring, and allows identifying signal of sexually antagonistic transmission distortions in genomic regions. We report the genomic location and recombination pattern surrounding 66 regions detected as potentially under sexually antagonist selection. We find an enrichment of genes associated with embryonic development within these regions. Last, we highlight two candidates regions for sexually antagonistic selection in humans.