Evolution

When two populations come into secondary contact, assortative mating can act as a barrier to gene flow. However, when assortative mating is incomplete, associations between preference and cue loci can break down, eroding assortative mating and collapsing species boundaries. Here, we investigate factors that can contribute to the maintenance of differentiated reproductive populations despite gene flow, resulting in either clinal hybrid zones or overlap zones between distinct populations. By simulating secondary contact on a uniform two-dimensional landscape using an individual-based computer model, we examine how the potential outcomes of secondary contact depend on search costs and/or pleiotropy between various combinations of mating cue, mating preference, and hybrid viability traits. We find that search costs can maintain stable mating trait clines, even in the absence of hybrid inviability traits. Pleiotropy between mating cues and hybrid inviability (i.e., "magic cues") temporarily stabilizes the mating cue cline but fails to maintain mating preference differentiation, since preference is not itself under direct selection. As the preference cline collapses, assortative mating breaks down, and -- absent search costs or very strong hybrid inviability -- the mating cue cline subsequently collapses as well. Thus, without preference-cue or preference-viability pleiotropy, search costs are essential for maintaining mating trait differentiation. Changes to the genetic architecture of mating traits strongly alter the distribution of phenotypes, affecting whether parental populations can coexist spatially. Small parameter changes can abruptly shift outcomes, highlighting the sensitivity of these systems.

Understanding how divergence in reproductive traits can promote speciation remains a fundamental question in evolutionary biology. Sperm morphology and kinematics diverge rapidly across species. However, the effect of hybridization between recently diverged species on sperm traits remains unclear, limiting our understanding of how reproductive isolation evolves. Here, we evaluated sperm morphology, kinematics, and trait integration in species of a young (~10,000 years), sympatric Cyprinodon pupfish radiation from San Salvador Island, Bahamas, as well as fertile advanced-generation hybrids between two of these species. We found significant divergence in flagellum length, midpiece area, and sperm velocity among species. In contrast, hybrids displayed transgressive kinematic profiles defined by high velocities, reduced path curvature, and distinct patterns of sperm kinematic integration. Our findings suggest that hybridization between recently diverged species may reorganize the underlying control of sperm locomotor mechanisms, generating novel phenotypes that could contribute to reproductive isolation in the early stages of speciation.

Assortative mating for a trait under selection can increase the rate of adaptive evolution and limit introgression of detrimental alleles. We therefore hypothesized that assortative mating facilitated the rapid evolution of flowering phenology observed in the self-incompatible perennial Lythrum salicaria (purple loosestrife) as it invaded eastern North America. We characterized flowering schedules of 600 individuals representing 20 populations sampled along a latitudinal gradient of 10 degrees and grown in a common garden at mid-latitude. Consistent with our hypothesis, we found that flowering schedules were less synchronous in the mixed population of the common garden (s = 0.50) relative to the 20 locally adapted populations comprising it (s = 0.56 to 0.86), and flowering synchrony decreased towards higher latitudes of origin. Despite high synchrony, assortment potential ({rho}) by growth and phenology varied by population ({rho} = 0.03 to 0.61), but the predicted negative correlation between s and {rho} was masked by among-individual fitness variation in the common garden. We show how fitness variation and asynchrony associated with locally adapted phenology can reduce the fitness impacts of maladaptive gene flow and accelerate the rate of adaptive evolution during invasion.

A long-standing question in evolutionary biology is: Under what circumstances can speciation occur despite hybridisation or because of hybridisation? Some models of hybrid incompatibilities predict that speciation can occur even in the presence of gene flow and strong selection against hybrids, an outcome also influenced by genetic contributions from parental species and genetic architecture. On the other hand, empirical work has shown that heterosis can counteract the effect of incompatibilities, hindering the speciation process. Theoretical models that simultaneously consider the positive and negative impacts of hybridisation on fitness remain scarce, raising questions about the effects of hybrid incompatibilities in the presence of heterosis. To address this question, we study how (Bateson)-Dobzhansky-Muller incompatibilities (BDMIs) interact with overdominant mutations in a two-locus population genetics model of an isolated hybrid population. We find that the strength of overdominance relative to incompatibilities determines the long-term genetic composition of the hybrid population. We show that high recombination exposes incompatibilities to selection and reduces the frequency of derived alleles in the hybrid population, limiting the strength of BDMIs that can be maintained by the balance with overdominance. We also show how neutral variation is affected by the strength of selection and the recombination rate between incompatible loci, generating patterns that include an increase in local variation resembling associative overdominance, or a reduction resembling background selection. Such variation of neutral variation, particularly at intermediate distances from BDMI loci, can generate peaks or troughs of diversity that are explained by the recombination rate between BDMI loci, and initial proportions of admixture between parental populations. Our work demonstrates how the genomic conflict caused by the interplay of overdominance and hybrid incompatibilities, recombination, and parental contributions, shape the genome of an isolated hybrid population.

Species interactions shape ecological dynamics, but adaptation to one interaction can trade off with others. Experiments that measure such evolved fitness changes across multiple interactions remain rare. We used experimental evolution to test whether recent selection under one ecological interaction changes fitness under other interactions in a fly-parasitoid system. We evolved a genetically diverse Drosophila melanogaster population for 15-17 generations under three regimes: benign conditions (control), high intraspecific competition, and infection by the parasitoid wasp Leptopilina boulardi. We then measured fly fitness (egg-to-adult survival and subsequent reproduction) under benign conditions, high intraspecific competition, and infection by three other parasitoid species and an additional conspecific L. boulardi strain. Selection history strongly influenced fitness across interactions. Populations maintained under high larval density showed reduced survival under infection by L. boulardi and L. victoriae, indicating a trade-off between past selection for competition and defence against some parasitoids. Populations evolved under parasitoid infection by L. boulardi showed increased resistance to a conspecific strain but reduced fitness when infected by another species, L. heterotoma. Our results show that rapid evolution in response to a single interaction can reshape multiple ecological interactions through fitness trade-offs, highlighting how recent evolutionary history may influence community dynamics and invasion susceptibility.

Dominance is an important and evolvable property of the genotype-phenotype map. A longstanding debate in evolutionary genetics concerns whether dominance is determined primarily by intrinsic properties of alleles at the focal locus or by modifiers elsewhere in the genome. Theoretical models show that second-site modifiers of dominance can evolve under some conditions. However, direct empirical tests of these models are rare because they require holding the focal heterozygous genotype constant while changing the rest of the genome. In the Drosophila montium species subgroup, female pigmentation is a Mendelian trait controlled by a single gene, POU domain motif 3 (pdm3), but the dominance relationships between pdm3 alleles differ among species. Using reciprocal introgressions among three closely related species, we compared females carrying the same Light/Dark pdm3 allele combinations in different homozygous or heterozygous genomic backgrounds and across different temperatures. In both species-pair comparisons, changing genomic background significantly altered the phenotype of identical pdm3 heterozygotes, demonstrating the existence of second-site modifiers of dominance. The effects of dominance modifiers depend on the particular pair of pdm3 alleles and on rearing temperature. These results show that dominance in this system is a genotype-by-genotype-by-environment trait, rather than a fixed attribute of individual alleles. The finding that second-site modifiers can alter dominance by reshaping reaction norms provides a developmental mechanism that links the evolution of dominance to phenotypic plasticity.

The evolutionary patterns of trait diversification provide insights into the function of the trait. Early burst of trait evolution is often associated with adaptive radiation, rapidly diversifying the trait in response to vacant niches followed by the slowdown of the diversification with niche filling, whereas late burst is more likely to be associated with sexual selection, possibly contributing to reproductive barriers between closely related species. Here, we studied the diversification of tail fork depth through time in hirundines to infer its function, which remains unclear due to the competing two alternative hypotheses: the sexual selection hypothesis, which is a classic explanation of deeply forked tails, proposed that this trait has evolved via sexual selection, which was then challenged by the viability selection hypothesis, which proposed that deeply forked tails have mainly evolved via viability selection for enhancing aerodynamic performance during aerial foraging on large prey. We found a late burst of tail fork depth, but not of bill length, i.e., an index of prey size. The observed pattern is consistent with the sexual selection hypothesis but not with the viability selection hypothesis.

Sensory systems mediate the interaction between organisms and their environment, but how complex sensory pathways evolve and relate to variation in perception and behavior across ecological contexts, remains poorly understood, especially for terrestrial taxa. Here, we investigate whole-visual-system adaptation in Heliconius erato butterflies. Using continent-wide sampling, we demonstrate that within H. erato, facet count significantly decreased with increasing elevation. Common-garden rearing of low-elevation H. erato populations from Ecuador and their high-elevation sister species, H. himera, showed that eye and brain morphology are heritable, and comparisons to genomic measures of divergence indicates that this variation is due to divergent selection. Parallel comparisons from Colombia involving H. chestertonii (high elevation) and H. erato venus (low elevation) further revealed that eye and brain morphology can evolve as independent, decoupled traits. For both locations, differences in visual acuity correlated with variation in facet count. We also observed parallel evolution of spectral sensitivity, with independent high-elevation populations having fewer red-reflecting lateral filtering pigments. To experimentally link visual system morphology to behavior, we assessed visual acuity in second-generation H. erato cyrbia-H. himera hybrids. Overall, acuity was influenced by facet count, and when analyzed together with brain morphology, by a positive interaction between facet count and optic lobe volume, demonstrating that structural investment in the eye and neural expansion combine to maximize visual perception. This work shows that visual adaptation is a multi-layered process whereby sensory traits can evolve independently under localized ecological pressures, but evolution across the visual pathway contributes to refinements in behavioral performance.

Populations that have detectable additive genetic variance for fitness (VA(W)) have the capacity for increase in their mean fitness through natural selection. The extent to which the magnitude of VA(W) in wild populations is predictive of the rate of adaptation is not well known, because few empirical field-based studies have been designed to address this question. Here, we report a two-year field experiment with pedigreed seeds embedded in four natural populations of the annual wildflower Baby Blue Eyes (Nemophila menziesii H. & A.), a species native to western North America. We first estimated VA(W) in a parental generation and then evaluated whether that estimate accurately predicted the adaptive response observed in the subsequent offspring generation grown under natural field conditions. We achieved this by directly comparing the mean fitnesses of the parental generation and their progeny grown under the same environmental conditions. We detected VA(W) and evidence of adaptation in all populations despite inter-annual differences in environmental conditions that directly affected fitness. Genotype-by-year interactions in fitness indicate that the fitness ranking of families differed between years, implying that the selective environment shifted over time. Additionally, although the environment in the second year reduced population mean fitness in three sites, the offspring generation maintained mean fitness at or above replacement, suggesting that adaptive evolution may have buffered the effects of environmental change. Overall, our results suggest that the four populations harbored sufficient VA(W) for adaptation through natural selection to the environmental conditions observed during the two years of this study.

Understanding how populations persist in gradually deteriorating environments through evolution is a central question in ecology and evolutionary biology. Previous studies have primarily focused on identifying the critical rate of environmental change beyond which extinction is certain. However, the existence of a viable equilibrium when the rate is below the threshold does not guarantee that a population can survive the transient dynamics to reach it. Using a quantitative genetic model that explicitly incorporates feedback among population size, genetic variance, and mean trait evolution, we show that population persistence can exhibit bistability when the rate of environmental change is below the extinction threshold. Specifically, extinction still occurs if the initial population size and genetic variance fall below a critical level. The initial state also influences the eco-evolutionary dynamics, such that a temporary increase or decline in population size and/or genetic variance does not necessarily predict the ultimate fate of the population. Therefore, in addition to estimating the critical rate of environmental change for extinction, characterizing current population size, genetic variation, and the degree of maladaptation may improve predictions of extinction risk in deteriorating environments.

Dominance is a widespread feature of genetic variants which affects life-history traits and fitness. Although dominance is generally thought to be an intrinsic property of genetic variants, it can sometimes evolve, as in the classic case of melanism in the peppered moth. The broader question of how likely dominance is to evolve is, however, controversial, because conditions favouring dominance evolution are often restrictive. Here, we revisit Haldanes classic hypothesis that dominance might evolve during the spread of beneficial mutations to fixation (i.e., during selective sweeps). We first confirm results of earlier models that sweeps of unconditionally beneficial mutations generate little potential for dominance to evolve, even in cases where modifier alleles segregate prior to selective sweeps. However, when sweeping beneficial alleles trade off between different environments -- which we explore with the illustrative case of sexually antagonistic selection -- the scope for dominance evolution expands. This occurs because modifier alleles can alter dominance separately in each environment, increasing the mean fitness of heterozygotes, prolonging the sojourn time of the sweep, and generating more heterozygosity upon which the modifier can act. In extreme cases, beneficial mutations that were initially destined for fixation can undergo a "dominance reversal" as a result of dominance evolution, converting them to balanced polymorphisms. We quantify how regularly dominance reversals of sweeping sexually antagonistic alleles can be expected to evolve. Overall, our results highlight conditions that allow the dominance of beneficial mutations to evolve, which we discuss in light of data on the frequency of selective sweeps, standing genetic variation for modifiers, and plasticity of modifier effects.

How broad phenotypic variation is maintained in natural populations in the face of selection is a central question in evolutionary biology. We address this question in the water strider Microvelia longipes, where males exhibit striking variation in rear leg length used in male-male contests for dominance. Using reaction norm experiments on inbred lines, we demonstrate that phenotypic plasticity contributes to expanding phenotypic variation, but requires high genetic variation to generate the broad range of trait expression observed in natural populations. Experimental evolution favouring trait exaggeration revealed that directional sexual selection not only fails to erode variation of male rear leg length, but rather amplifies it beyond the natural distribution. Additionally, male-limited selection in favour of dominance generated substantial fecundity costs in females, underscoring the role of sexual conflict driven by females in constraining exaggerated secondary sexual traits in males. Our findings show that sexually antagonistic selection and directional sexual selection jointly generate high genetic variation, which phenotypic plasticity inflates into broad phenotypic distribution of male weapon size. This provides an empirical explanation for the high variability of male exaggerated weapons in nature.

The repeated evolution of certain complex traits within a given lineage is compelling and presents an opportunity for understanding selective and genetic features that promote rapid multi-trait adaptation. The North American plant genus Penstemon is one such example, with numerous evolutionary shifts from ancestral bee syndrome to hummingbird syndrome flowers. Here, we traced the evolution of multi-trait floral phenotypes within a focal clade of Penstemon using a new whole genome phylogenomic estimate and found four independent origins of the hummingbird syndrome. We found strong evolutionary convergence in floral traits across these four origins and observed that the hummingbird syndrome assembled rapidly, without leaving a signal of stepwise modification of traits. Patterns of evolutionary correlations among floral traits in bee syndrome Penstemon species likely enable rapid shifts to hummingbird syndrome. Using phylogenomic tests for introgression, we found no evidence that adaptive introgression has fueled the four repeated origins of hummingbird syndrome flowers. Patterns of allele sharing were instead consistent with substantial levels of incomplete lineage sorting, suggesting repeated complex adaptation involves de novo mutation or adaptation from ancestral variation.

Many endosymbioses in eukaryotes superficially appear to be beneficial to both participants. However, there is little direct evidence for this, and symbioses naturally set up conditions in which each member of the pair is under selection to extract resources from the other. Ultimately, the endosymbiont either evolves to be in conflict with the interests of the host or to act cooperatively with the host contrary to its own best interests. Focusing on obligate symbioses, we develop theory to clarify the population-genetic conditions favoring the alternative outcomes. The balance is usually tipped in favor of exploitation by the symbiont, particularly when the number of symbionts within host cells is high, selection is strong on symbionts relative to hosts, there is horizontal transfer of symbionts, and/or the symbionts have accelerated mutation rates or turnover times. If the symbiont conditions the host-cell biology to enhance within-host population sizes, selection for selfish symbionts will be further enhanced by the diminished level of within-host drift. Although the host evolves in parallel to exploit resources from the endosymbiont, the net result is often a stalemate in which the host is no better off than prior to host-symbiont coevolution. Strict vertical inheritance can result in an evolutionary alignment of interests of the endosymbiont and the host, as this minimizes the possibility of within-host selection, but even here there is a critical host population size below which the symbiont evolves to exploit the host. These results suggest that the evolutionary enslavement of a symbiont to benefit a host species requires a narrow mix of population-biological features of both participants.

Reproductive success often depends on coordinated combinations of morphology, dispersal ability, and mating behavior. Supergenes, genomic regions of suppressed recombination, allow such combinations to be inherited by offspring as a single unit. In ants, independently evolved supergenes control colony queen number, yet few studies have investigated their joint influence on morphology, mating, and colony-founding in sexuals. Formica cinerea provides a unique opportunity to address this question because it harbors two supergenes that together produce three queen and male morphs: large monogyne, large polygyne, and small polygyne. Here we show that these supergenes jointly shape an integrated suite of traits across the reproductive cycle. Wing area was primarily associated with the chromosome 3 supergene, with monogyne individuals having larger wings than polygyne individuals. Thorax volume was associated with the chromosome 9 supergene, with small polygyne individuals having reduced thorax volume regardless of social origin. Mating was assortative for both supergenes in large morphs but random in small polygyne queens. Independent colony founding was almost exclusively performed by large monogyne queens; initial egg production was unaffected by mate genotype. These findings show that the two supergenes jointly coordinate dispersal morphology, mate choice, and colony-founding into coherent reproductive strategies, preventing maladaptive intermediate phenotypes.

Delayed germination is classically explained as a bet-hedging strategy against environmental variability: by withholding a fraction of seeds from germination, plants spread establishment risk across years that vary in temperature, precipitation, and other conditions governing seedling survival. Whether biotic interactions can generate analogous selective pressure has received comparatively little theoretical attention. Here we examine the evolution of germination timing in a host-pathogen model in which a saturating (Holling Type II) transmission function couples seed bank dynamics to epidemic cycles. The model produces three qualitatively distinct ecological regimes: a pathogen-free equilibrium, a stable endemic equilibrium, and an oscillatory endemic regime arising through a bifurcation, a transition from stable to oscillatory endemic dynamics. Using adaptive dynamics, namely invasion analysis, we show that the evolutionarily stable germination rate depends critically on which regime the resident population occupies. When pathogen dynamics settle to an equilibrium, selection favours ever-faster germination with no finite optimum, regardless of pathogen presence. When dynamics are limit cycles, periodic epidemic peaks create recurrent windows of high establishment mortality that function as biotic analogues of abiotic interactions (environmental), and selection drives the germination rate toward the bifurcation boundary. The evolutionary attractor thus coincides with an ecological bifurcation point. Trait substitution sequence simulations confirm convergence to this attractor, and multi-trait eco-evolutionary simulations provide evidence that the attractor is evolutionarily stable, consistent with a continuously stable strategy (CSS).These results extend classical bet-hedging theory to biotic drivers and suggest that pathogens capable of sustaining population cycles may be an underappreciated selective force on germination timing and, more broadly, on the pace of life-history evolution.

The additive genetic variances and covariances of traits, collected in the G-matrix, summarise heritable variation within populations and are commonly used to predict the rate and direction of short-term multivariate evolution. These (co)variances are shaped by pleiotropy and genetic linkage, two features often associated with supergenes formed by chromosomal inversions. Yet how supergene evolution affects the structure and temporal stability of the G-matrix remains unclear. Here, we use mathematical analysis and individual-based simulations to investigate the evolution and genetic consequences of inversions capturing multiple pleiotropic loci underlying two traits subject to disruptive and correlational selection (selection favouring particular combinations of trait values). We show that inversions evolve under disruptive selection and are maintained by balancing selection because they preserve associations among alleles that together generate discrete phenotypic morphs. The genetic architecture reflects how selection acts on the traits: selection favouring diversification along a joint trait combination generally produces a single multi-trait supergene, whereas selection favouring independent diversification of each trait produces multiple independently segregating inversions. By suppressing recombination, these inversions increase additive genetic variance and narrow-sense heritability, and stabilise the overall amount of additive genetic variation through time. When dominance is allowed to evolve, dominance relationships become coordinated across linked loci within supergenes, although most genetic variance remains additive at the population level. Together, these results link the form of multivariate selection to the evolution of supergenes and to their consequences for the structure and temporal stability of the G-matrix.

Stabilizing selection commonly acts on complex traits that affect individual fitness. Here, we relate mean fitness under stabilizing selection to population size and trait architecture, using a simple application of theoretical predictions for the distribution of phenotypic values in a single-trait Gaussian stabilizing selection model. We show that mean fitness is maximized by a finite (often small) population size when the total diploid mutation rate U across trait-affecting loci is reasonably large. Namely, this occurs when U > {sigma}2/(4(VS+VE)), where {sigma}2 is the variance of the distribution of effect sizes of new mutations, VS determines the strength of stabilizing selection, and VE is the environmental variance. We validate these predictions using individual-based simulations and briefly discuss their implications for interpreting genetic load and adaptability in small populations.

A prominent developmental plasticity theory proposes that early life adversity accelerates life history trajectories so organisms can maximize fitness in challenging environments. Standard tests of this hypothesis rely on empirical predictions about observable life history variables (e.g., age at first birth), because the proposed internal processes cannot be directly measured. However, the observable proxies are themselves mechanically linked, and regressions that ignore this may conflate causal effects with mechanical relationships among proxies. Here, we develop theory that explicitly justifies some existing empirical tests but rejects others. We integrate an accounting model that incorporates age at first birth, interbirth intervals, and lifespan with an optimization model, to derive the mathematical form that tests of the hypothesis should take. We apply these tests to data from wild female baboons, using early life rainfall as an exogenous proxy for early adversity so that estimates can plausibly be interpreted causally. The accounting model explains >98% of the variation in lifetime reproductive success among females that reproduced. However, our theory-derived tests find no evidence for the reproductive acceleration hypothesis. Our study illustrates the value of formal theory for causal inference in developmental plasticity research, where intertwined measurable variables may be obscured by strictly verbal hypotheses.

Genetic variation exists for many male reproductive traits despite apparent strong sexual selection in favor of particular males. Understanding how that variation is maintained is an unresolved problem in evolutionary biology. One proposed solution to this problem is genotype-by-environment interactions (GEIs), where no male genotype is universally superior across environments. Another proposed answer is variation in female preference, such that different females prefer different male genotypes. Additionally, male genotypes may differ in their reproductive output as they age. The house fly Musca domestica is a well-suited system to evaluate these explanations for genetic variation in male reproductive traits because two male genotypes (YM and IIIM) differ in mating performance. Specifically, IIIM males outcompete YM males in mating assays because IIIM males have a shorter copulation latency. To determine the relative importance of GEIs, female variation, and male age on the maintenance of genetic variation in male reproductive behaviors, we performed non-competitive (one male to one female) and competitive (one IIIM male and one YM male to one female) mating assays while considering multiple ages and different female strains. IIIM males attempted more matings regardless of competition level, female genotype or age, but mated faster than YM males only with females of their own strain and only performed more matings in non-competitive trials. However, female strain did not improve the mating success of YM males. We also did not observe evidence for genotype-by-age interactions on male mating success. Importantly, we did not identify any conditions where YM males outcompeted IIIM males, and therefore there was no evidence for interactions or trade-offs that could explain the maintenance of genetic variation for male mating success. To explain the maintenance of IIIM and YM males, other factors such as additional social environments or varying temperature should be investigated, as the genotypes are found in natural environments with contrasting temperatures.