Sexual repurposing of juvenile aposematism in locusts.

Adaptive plasticity requires an integrated suite of functional responses to environmental variation, which can include social communication across life stages. Desert locusts (Schistocerca gregaria) exhibit an extreme example of phenotypic plasticity called phase polyphenism, in which a suite of behavioral and morphological traits differ according to local population density. Male and female juveniles developing at low population densities exhibit green- or sand-colored background-matching camouflage, while at high densities they show contrasting yellow and black aposematic patterning that deters predators. The predominant background colors of these phenotypes (green/sand/yellow) all depend on expression of the carotenoid-binding "Yellow Protein" (YP). Gregarious (high-density) adults of both sexes are initially pinkish, before a YP-mediated yellowing reoccurs upon sexual maturation. Yellow color is especially prominent in gregarious males, but the reason for this difference has been unknown since phase polyphenism was first described in 1921. Here, we use RNA interference to show that gregarious male yellowing acts as an intrasexual warning signal, which forms a multimodal signal with the antiaphrodisiac pheromone phenylacetonitrile (PAN) to prevent mistaken sexual harassment from other males during scramble mating in a swarm. Socially mediated reexpression of YP thus adaptively repurposes a juvenile signal that deters predators into an adult signal that deters undesirable mates. These findings reveal a previously underappreciated sexual dimension to locust phase polyphenism, and promote locusts as a model for investigating the relative contributions of natural versus sexual selection in the evolution of phenotypic plasticity.

Genomic insights into variation in thermotolerance between hybridizing swordtail fishes.

Understanding how organisms adapt to changing environments is a core focus of research in evolutionary biology. One common mechanism is adaptive introgression, which has received increasing attention as a potential route to rapid adaptation in populations struggling in the face of ecological change, particularly global climate change. However, hybridization can also result in deleterious genetic interactions that may limit the benefits of adaptive introgression. Here, we used a combination of genome-wide quantitative trait locus mapping and differential gene expression analyses between the swordtail fish species Xiphophorus malinche and X. birchmanni to study the consequences of hybridization on thermotolerance. While these two species are adapted to different thermal environments, we document a complicated architecture of thermotolerance in hybrids. We identify a region of the genome that contributes to reduced thermotolerance in individuals heterozygous for X. malinche and X. birchmanni ancestry, as well as widespread misexpression in hybrids of genes that respond to thermal stress in the parental species, particularly in the circadian clock pathway. We also show that a previously mapped hybrid incompatibility between X. malinche and X. birchmanni contributes to reduced thermotolerance in hybrids. Together, our results highlight the challenges of understanding the impact of hybridization on complex ecological traits and its potential impact on adaptive introgression.

Evolutionary novelty in communication between the sexes.

The diversity of signalling traits within and across taxa is vast and striking, prompting us to consider how novelty evolves in the context of animal communication. Sexual selection contributes to diversification, and here we endeavour to understand the initial conditions that facilitate the maintenance or elimination of new sexual signals and receiver features. New sender and receiver variants can occur through mutation, plasticity, hybridization and cultural innovation, and the initial conditions of the sender, the receiver and the environment then dictate whether a novel cue becomes a signal. New features may arise in the sender, the receiver or both simultaneously. We contend that it may be easier than assumed to evolve new sexual signals because sexual signals may be arbitrary, sexual conflict is common and receivers are capable of perceiving much more of the world than just existing sexual signals. Additionally, changes in the signalling environment can approximate both signal and receiver changes through a change in transmission characteristics of a given environment or the use of new environments. The Anthropocene has led to wide-scale disruption of the environment and may thus generate opportunity to directly observe the evolution of new signals to address questions that are beyond the reach of phylogenetic approaches.

Divergent neurogenomic responses shape social learning of both personality and mate preference.

Behavior plays a fundamental role in shaping the origin and fate of species. Mating decisions can act to promote or restrict gene flow, as can personality traits that influence dispersal and niche use. Mate choice and personality are often both learned and therefore influenced by an individual's social environment throughout development. Likewise, the molecular pathways that shape these behaviors may also be co-expressed. In this study on swordtail fish (Xiphophorus birchmanni), we show that female mating preferences for species-typical pheromone cues are entirely dependent on social experience with adult males. Experience with adults also shapes development along the shy-bold personality axis, with shy behaviors arising from exposure to risk-averse heterospecifics as a potential stress-coping strategy. In maturing females, conspecific exposure results in a strong upregulation of olfaction and vision genes compared with heterospecific exposure, as well as immune response genes previously linked to anxiety, learning and memory. Conversely, heterospecific exposure involves an increased expression of genes important for neurogenesis, synaptic plasticity and social decision-making. We identify subsets of genes within the social decision-making network and with known stress-coping roles that may be directly coupled to the olfactory processes females rely on for social communication. Based on these results, we conclude that the social environment affects the neurogenomic trajectory through which socially sensitive behaviors are learned, resulting in adult phenotypes adapted for specific social groupings.

Assortative mating and persistent reproductive isolation in hybrids.

The emergence of new species is driven by the establishment of mechanisms that limit gene flow between populations. A major challenge is reconciling the theoretical and empirical importance of assortative mating in speciation with the ease with which it can fail. Swordtail fish have an evolutionary history of hybridization and fragile prezygotic isolating mechanisms. Hybridization between two swordtail species likely arose via pollution-mediated breakdown of assortative mating in the 1990s. Here we track unusual genetic patterns in one hybrid population over the past decade using whole-genome sequencing. Hybrids in this population formed separate genetic clusters by 2003, and maintained near-perfect isolation over 25 generations through strong ancestry-assortative mating. However, we also find that assortative mating was plastic, varying in strength over time and disappearing under manipulated conditions. In addition, a nearby population did not show evidence of assortative mating. Thus, our findings suggest that assortative mating may constitute an intermittent and unpredictable barrier to gene flow, but that variation in its strength can have a major effect on how hybrid populations evolve. Understanding how reproductive isolation varies across populations and through time is critical to understanding speciation and hybridization, as well as their dependence on disturbance.

Reproductive isolation of hybrid populations driven by genetic incompatibilities.

Despite its role in homogenizing populations, hybridization has also been proposed as a means to generate new species. The conceptual basis for this idea is that hybridization can result in novel phenotypes through recombination between the parental genomes, allowing a hybrid population to occupy ecological niches unavailable to parental species. Here we present an alternative model of the evolution of reproductive isolation in hybrid populations that occurs as a simple consequence of selection against genetic incompatibilities. Unlike previous models of hybrid speciation, our model does not incorporate inbreeding, or assume that hybrids have an ecological or reproductive fitness advantage relative to parental populations. We show that reproductive isolation between hybrids and parental species can evolve frequently and rapidly under this model, even in the presence of substantial ongoing immigration from parental species and strong selection against hybrids. An interesting prediction of our model is that replicate hybrid populations formed from the same pair of parental species can evolve reproductive isolation from each other. This non-adaptive process can therefore generate patterns of species diversity and relatedness that resemble an adaptive radiation. Intriguingly, several known hybrid species exhibit patterns of reproductive isolation consistent with the predictions of our model.

Early social learning triggers neurogenomic expression changes in a swordtail fish.

Mate choice can play a pivotal role in the nature and extent of reproductive isolation between species. Mating preferences are often dependent on an individual's social experience with adult phenotypes throughout development. We show that olfactory preference in a swordtail fish (Xiphophorus malinche) is affected by previous experience with adult olfactory signals. We compare transcriptome-wide gene expression levels of pooled sensory and brain tissues between three treatment groups that differ by social experience: females with no adult exposure, females exposed to conspecifics and females exposed to heterospecifics. We identify potential functionally relevant genes and biological pathways differentially expressed not only between control and exposure groups, but also between groups exposed to conspecifics and heterospecifics. Based on our results, we speculate that vomeronasal receptor type 2 paralogs may detect species-specific pheromone components and thus play an important role in reproductive isolation between species.

Admix'em: a flexible framework for forward-time simulations of hybrid populations with selection and mate choice.

UNLABELLED: We introduce a new forward-time simulator, Admix'em, that allows for rapid and realistic simulations of admixed populations with selection. Complex selection can be achieved through user-defined fitness and mating-preference probability functions. Users can specify realistic genomic landscapes and model neutral SNPs in addition to sites under selection. Admix'em is designed to simulate selection in admixed populations but can also be used as a general population simulator. Usage and examples are in the supplement. AVAILABILITY AND IMPLEMENTATION: C ++ and OpenMP, supports 64-bit Linux/Unix-like platforms. https://github.com/melop/admixem CONTACT: rcui@age.mpg.de SUPPLEMENTARY INFORMATION: Supplementary data are available at Bioinformatics online.

Ancient hybridization and genomic stabilization in a swordtail fish.

A rapidly increasing body of work is revealing that the genomes of distinct species often exhibit hybrid ancestry, presumably due to postspeciation hybridization between closely related species. Despite the growing number of documented cases, we still know relatively little about how genomes evolve and stabilize following hybridization, and to what extent hybridization is functionally relevant. Here, we examine the case of Xiphophorus nezahualcoyotl, a teleost fish whose genome exhibits significant hybrid ancestry. We show that hybridization was relatively ancient and is unlikely to be ongoing. Strikingly, the genome of X. nezahualcoyotl has largely stabilized following hybridization, distinguishing it from examples such as human-Neanderthal hybridization. Hybridization-derived regions are remarkably distinct from other regions of the genome, tending to be enriched in genomic regions with reduced constraint. These results suggest that selection has played a role in removing hybrid ancestry from certain functionally important regions. Combined with findings in other systems, our results raise many questions about the process of genomic stabilization and the role of selection in shaping patterns of hybrid ancestry in the genome.

Multiple mating and reproductive skew in parental and introgressed females of the live-bearing fish Xiphophorus birchmanni.

Just as mating patterns can promote speciation or hybridization, the presence of hybridization can shape mating patterns within a population. In this study, we characterized patterns of multiple mating and reproductive skew in a naturally hybridizing swordtail fish species, Xiphophorus birchmanni. We quantified multiple mating using microsatellite markers to genotype embryos from 43 females collected from 2 wild populations. We also used a suite of single-nucleotide polymorphism markers to categorize females and their inferred mates as either parental X. birchmanni or as introgressed individuals, which carried alleles from a sister species, X. malinche. We found that parental and introgressed X. birchmanni females mated multiply with both parental and introgressed males. We found no difference in mating patterns or reproductive skew between parental and introgressed X. birchmanni females. However, nonintrogressed X. birchmanni males mated more often with large, fecund females. These females also had the greatest levels of skew in fertilization success of males. Thus, our results show that X. birchmanni has a polygynandrous mating system and that introgression of X. malinche alleles has only subtle effects on mating patterns in this species.

Assortative mating and the maintenance of population structure in a natural hybrid zone.

Understanding the factors that give rise to natural hybrid zones and govern their dynamics and structure is important to predicting the evolutionary consequences of hybridization. Here we use a combination of multigenerational population genetic data, mating patterns from a natural population, behavioral assays, and mark-recapture data within clinal hybrid zones of the genus Xiphophorus to test the role of assortative mating in maintaining population structure and the potential for ongoing genetic exchange between heterospecifics. Our data demonstrate that population structure is temporally robust and driven largely by assortative mating stemming from precopulatory isolation between pure species. Furthermore, mark-recapture data revealed that rates of migration within the same stream reach are far below the level needed to support population structure. In contrast to many empirical studies of natural hybrid zones, there appeared to be no hybrid male dysfunction or discrimination against hybrid males by pure parental females, and hybrid females mated and associated with pure species and hybrid males at random. Despite strong isolation between pure parentals, hybrids therefore can act as a conduit for genetic exchange between heterospecifics, which has been shown to increase the tempo of evolutionary change. Additionally, our findings highlight the complexity of natural hybrid zone dynamics, demonstrating that sexual and ecological selection together can give rise to patterns that do not fit classical models of hybrid zone evolution.

Functional Test of a Naturally Occurred Tumor Modifier Gene Provides Insights to Melanoma Development.

Occurrence of degenerative interactions is thought to serve as a mechanism underlying hybrid unfitness. However, the molecular mechanisms underpinning the genetic interaction and how they contribute to overall hybrid incompatibilities are limited to only a handful of examples. A vertebrate model organism, Xiphophorus , is used to study hybrid dysfunction and it has been shown from this model that diseases, such as melanoma, can occur in certain interspecies hybrids. Melanoma development is due to hybrid inheritance of an oncogene, xmrk , and loss of a co-evolved tumor modifier. It was recently found that adgre5 , a G protein-coupled receptor involved in cell adhesion, is a tumor regulator gene in naturally hybridizing Xiphophorus species X. birchmanni and X. malinche . We hypothesized that one of the two parental alleles of adgre5 is involved in regulation of cell proliferation, migration and melanomagenesis. Accordingly, we assessed the function of adgre5 alleles from each parental species of the melanoma-bearing hybrids using in vitro cell proliferation and migration assays. In addition, we expressed each adgre5 allele with the xmrk oncogene in transgenic medaka. We found that cells transfected with the X. birchmanni adgre5 exhibited decreased proliferation and migration compared to those with the X. malinche allele. Moreover, X. birchmanni allele of adgre5 completely inhibited melanoma development in xmrk transgenic medaka, while X. malinche adgre5 expression did not exhibit melanoma suppressive activity in medaka. These findings showed that adgre5 is a natural melanoma suppressor and provide new insight in melanoma etiology.

Population-level mating patterns and fluctuating asymmetry in swordtail hybrids.

Morphological symmetry is a correlate of fitness-related traits or even a direct target of mate choice in a variety of taxa. In these taxa, when females discriminate among potential mates, increased selection on males should reduce fluctuating asymmetry (FA). Hybrid populations of the swordtails Xiphophorus birchmanni and Xiphophorus malinche vary from panmictic (unstructured) to highly structured, in which reproductive isolation is maintained among hybrids and parental species. We predicted that FA in flanking vertical bars used in sexual signalling should be lower in structured populations, where non-random mating patterns are observed. FA in vertical bars was markedly lower in structured populations than in parental and unstructured hybrid populations. There was no difference in FA between parentals and hybrids, suggesting that hybridisation does not directly affect FA. Rather, variation in FA likely results from contrasting mating patterns in unstructured and structured populations.

A taste for the familiar: explaining the inbreeding paradox.

The negative consequences of inbreeding have led animal biologists to assume that mate choice is generally biased against relatives. However, inbreeding avoidance is highly variable and by no means the rule across animal taxa. Even when inbreeding is costly, there are numerous examples of animals failing to avoid inbreeding or even preferring to mate with close kin. We argue that selective and mechanistic constraints interact to limit the evolution of inbreeding avoidance, notably when there is a risk of mating with heterospecifics and losing fitness through hybridization. Further, balancing inbreeding avoidance with conspecific mate preference may drive the evolution of multivariate sexual communication. Studying different social and sexual decisions within the same species can illuminate trade-offs among mate-choice mechanisms.

Sexual selection and the ascent of women: Mate choice research since Darwin.

Darwin's theory of sexual selection fundamentally changed how we think about sex and evolution. The struggle over mating and fertilization is a powerful driver of diversification within and among species. Contemporaries dismissed Darwin's conjecture of a "taste for the beautiful" as favoring particular mates over others, but there is now overwhelming evidence for a primary role of both male and female mate choice in sexual selection. Darwin's misogyny precluded much analysis of the "taste"; an increasing focus on mate choice mechanisms before, during, and after mating reveals that these often evolve in response to selection pressures that have little to do with sexual selection on chosen traits. Where traits and preferences do coevolve, they can do so whether fitness effects on choosers are positive, neutral, or negative. The spectrum of selection on traits and preferences, and how traits and preferences respond to social effects, determine how sexual selection and mate choice influence broader-scale processes like reproductive isolation and population responses to environmental change.

Conflicting preferences within females: sexual selection versus species recognition.

Preferences for mates within and between species are often harmonious, as traits that females prefer are usually more developed in conspecifics than heterospecifics. This need not be the case, however. When it is not, conflict between these arenas of mate choice can be resolved if females attend to different cues for each task. But this raises the potential for correlations among preferences to limit the opportunity for these two processes to operate independently. Here, we show that, within individual female pygmy swordtails (Xiphophorus pygmaeus), directional preferences for conspicuous ornamentation are inversely associated with discrimination against a sympatric heterospecific, Xiphophorus cortezi. Thus, mate choice among and within species need not be separate, independent processes; instead, they can be mechanistically intertwined. As a consequence, different arenas of mate choice can constrain one another, even when females assess multiple cues.

A narrow window for geographic cline analysis using genomic data: Effects of age, drift, and migration on error rates.

The use of genomic and phenotypic data to scan for outliers is a mainstay for studies of hybridization and speciation. Geographic cline analysis of natural hybrid zones is widely used to identify putative signatures of selection by detecting deviations from baseline patterns of introgression. As with other outlier-based approaches, demographic histories can make neutral regions appear to be under selection and vice versa. In this study, we use a forward-time individual-based simulation approach to evaluate the robustness of geographic cline analysis under different evolutionary scenarios. We modelled multiple stepping-stone hybrid zones with distinct age, deme sizes, and migration rates, and evolving under different types of selection. We found that drift distorts cline shapes and increases false positive rates for signatures of selection. This effect increases with hybrid zone age, particularly if migration between demes is low. Drift can also distort the signature of deleterious effects of hybridization, with genetic incompatibilities and particularly underdominance prone to spurious typing as adaptive introgression. Our results suggest that geographic clines are most useful for outlier analysis in young hybrid zones with large populations of hybrid individuals. Current approaches may overestimate adaptive introgression and underestimate selection against maladaptive genotypes.

The Genetic Architecture of Variation in the Sexually Selected Sword Ornament and Its Evolution in Hybrid Populations.

Biologists since Darwin have been fascinated by the evolution of sexually selected ornaments, particularly those that reduce viability. Uncovering the genetic architecture of these traits is key to understanding how they evolve and are maintained. Here, we investigate the genetic architecture and evolutionary loss of a sexually selected ornament, the "sword" fin extension that characterizes many species of swordtail fish (Xiphophorus). Using sworded and swordless sister species of Xiphophorus, we generated a mapping population and show that the sword ornament is polygenic-with ancestry across the genome explaining substantial variation in the trait. After accounting for the impacts of genome-wide ancestry, we identify one major-effect quantitative trait locus (QTL) that explains ~5% of the overall variation in the trait. Using a series of approaches, we narrow this large QTL interval to several likely candidate genes, including genes involved in fin regeneration and growth. Furthermore, we find evidence of selection on ancestry at one of these candidates in four natural hybrid populations, consistent with selection against the sword in these populations.