Hybrid speciation driven by multilocus introgression of ecological traits.

Hybridization allows adaptations to be shared among lineages and may trigger the evolution of new species1,2. However, convincing examples of homoploid hybrid speciation remain rare because it is challenging to demonstrate that hybridization was crucial in generating reproductive isolation3. Here we combine population genomic analysis with quantitative trait locus mapping of species-specific traits to examine a case of hybrid speciation in Heliconius butterflies. We show that Heliconius elevatus is a hybrid species that is sympatric with both parents and has persisted as an independently evolving lineage for at least 180,000 years. This is despite pervasive and ongoing gene flow with one parent, Heliconius pardalinus, which homogenizes 99% of their genomes. The remaining 1% introgressed from the other parent, Heliconius melpomene, and is scattered widely across the H. elevatus genome in islands of divergence from H. pardalinus. These islands contain multiple traits that are under disruptive selection, including colour pattern, wing shape, host plant preference, sex pheromones and mate choice. Collectively, these traits place H. elevatus on its own adaptive peak and permit coexistence with both parents. Our results show that speciation was driven by introgression of ecological traits, and that speciation with gene flow is possible with a multilocus genetic architecture.

A genetic cause of male mate preference.

A gene for mate preference has been shared between hybridizing butterfly species.

Adaptive introgression of a visual preference gene.

Visual preferences are important drivers of mate choice and sexual selection, but little is known of how they evolve at the genetic level. In this study, we took advantage of the diversity of bright warning patterns displayed by Heliconius butterflies, which are also used during mate choice. Combining behavioral, population genomic, and expression analyses, we show that two Heliconius species have evolved the same preferences for red patterns by exchanging genetic material through hybridization. Neural expression of regucalcin1 correlates with visual preference across populations, and disruption of regucalcin1 with CRISPR-Cas9 impairs courtship toward conspecific females, providing a direct link between gene and behavior. Our results support a role for hybridization during behavioral evolution and show how visually guided behaviors contributing to adaptation and speciation are encoded within the genome.

The hidden fitness of the male zebra finch courtship song.

Vocal learning in songbirds is thought to have evolved through sexual selection, with female preference driving males to develop large and varied song repertoires1-3. However, many songbird species learn only a single song in their lifetime4. How sexual selection drives the evolution of single-song repertoires is not known. Here, by applying dimensionality-reduction techniques to the singing behaviour of zebra finches (Taeniopygia guttata), we show that syllable spread in low-dimensional feature space explains how single songs function as honest indicators of fitness. We find that this Gestalt measure of behaviour captures the spectrotemporal distinctiveness of song syllables in zebra finches; that females strongly prefer songs that occupy more latent space; and that matching path lengths in low-dimensional space is difficult for young males. Our findings clarify how simple vocal repertoires may have evolved in songbirds and indicate divergent strategies for how sexual selection can shape vocal learning.

Surviving the serenade: how conflicting selection pressures shape the early stages of sexual signal diversification.

Understanding how the early stages of sexual signal diversification proceed is critically important because these microevolutionary dynamics directly shape species trajectories and impact macroevolutionary patterns. Unfortunately, studying this is challenging because signals involve complex interactions between behavior, morphology, and physiology, much of which can only be measured in real-time. In Hawaii, male Pacific field cricket song attracts both females and a deadly parasitoid fly. Over the past two decades, there has been a marked increase in signal variation in Hawaiian populations of these crickets, including novel male morphs with distinct mating songs. We capitalize on this rare opportunity to track changes in morph composition over time in a population with three novel morphs, investigating how mate and parasitoid attraction (components of sexual and natural selection) may shape signal evolution. We find dramatic fluctuation in morph proportions over the three years of the study, including the arrival and rapid increase of one novel morph. Natural and sexual selection pressures act differently among morphs, with some more attractive to mates and others more protected from parasitism. Collectively, our results suggest that differential protection from parasitism among morphs, rather than mate attraction, aligns with recent patterns of phenotypic change in the wild.

Aesthetic preference for artificially selected color variant affects mate choice copying behavior in female Poecilia latipinna.

Three experiments were conducted examining whether an artificially selected "gold" color variant in female "models" affects mate choice copying behavior in sailfin mollies (Poecilia latipinna). Experiment I consisted of a pair of female preference assays, first assessing preference for male body size, followed by a mate choice copying assay that paired a model female with the smaller, non-preferred male from the initial preference test. Female subjects were divided into three groups that used either a wildtype female model, an artificially selected "gold" variant (cultivated within the aquarium fish trade) model, or control wherein no model was presented. Results showed females consistently copied the model's choice, switching preferences from the larger to smaller male when paired with a model regardless of color. In the second experiment wildtype females were presented with a pair of size-matched dummy males both of which paired with model females (one gold and the other wild type). Subjects consistently preferred the male previously paired with the gold- over the male with the wildtype-model, suggesting pre-existing sensory/perceptual biases may have affected their mate choice copying behavior. Previous studies have offered evidence for the spread of novel traits in males via sensory exploitation. However, these results indicate such biases may influence courtship behavior in circumstances where the novel trait is expressed in females as well. For the third experiment, wildtype females were presented with a choice between gold vs wildtype dummy males, the results of which revealing significant preferences for gold. In a follow-up assay pairing a wild type model with the non-preferred wildtype male, females maintained their preference for gold males despite the conflicting social driver of mate choice copying. These data offer evidence for the existence of a perceptual/cognitive bias in the context of mate choice copying, favoring the gold phenotype and/or novelty in general.

Parental kinship coefficient but not paternal coloration predicts early offspring growth in lake char.

The 'good genes' hypotheses of sexual selection predict that females prefer males with strong ornaments because they are in good health and vigor and can afford the costs of the ornaments. A key assumption of this concept is that male health and vigor are useful predictors of genetic quality and hence offspring performance. We tested this prediction in wild-caught lake char (Salvelinus umbla) whose breeding coloration is known to reveal aspects of male health. We first reanalyzed results from sperm competition trials in which embryos of known parenthood had been raised singly in either a stress- or non-stress environment. Paternal coloration did not correlate with any measures of offspring performance. However, offspring growth was reduced with higher kinship coefficients between the parents. To test the robustness of these first observations, we collected a new sample of wild males and females, used their gametes in a full-factorial in vitro breeding experiment, and singly raised about 3000 embryos in either a stress- or non-stress environment (stress induced by microbes). Again, paternal coloration did not predict offspring performance, while offspring growth was reduced with higher kinship between the parents. We conclude that, in lake char, the genetic benefits of mate choice would be strongest if females could recognize and avoid genetically related males, while male breeding colors may be more relevant in intra-sexual selection.

Sexual selection and mate limitation shape evolution of species' range limits.

Understanding what processes shape the formation of species' geographic range limits is one central objective linking ecology and evolutionary biology. One potentially key process is sexual selection; yet, theory examining how sexual selection could shape eco-evolutionary dynamics in marginal populations is still lacking. In species with separate sexes, range limits could be shaped by limitations in encountering mates at low densities. Sexual selection could therefore modulate mate limitation and resulting extinction-colonization dynamics at range margins, through evolution of mate encounter ability and/or mate competition traits, and their demographic consequences. We use a spatially explicit eco-genetic model to reveal how different forms of sexual selection can variably affect emerging range limits. Larger ranges emerged when sexual selection acted exclusively on traits increasing mate encounter probability, thus reducing female's mate limitation toward the range margins. In contrast, sexual selection via mate competition narrowed range limits due to increased trait-dependent mortality in males and elevated mate limitation for females. When mate encounter coevolved with mate competition, their combined effects on range limits depended on the mating system (polygyny vs. monogamy). Our results demonstrate that evolution of species' ranges may be importantly shaped by feedbacks between sexual selection and spatial population demography and dynamics.

Environmental complexity mitigates the demographic impact of sexual selection.

Sexual selection and the evolution of costly mating strategies can negatively impact population viability and adaptive potential. While laboratory studies have documented outcomes stemming from these processes, recent observations suggest that the demographic impact of sexual selection is contingent on the environment and therefore may have been overestimated in simple laboratory settings. Here we find support for this claim. We exposed copies of beetle populations, previously evolved with or without sexual selection, to a 10-generation heatwave while maintaining half of them in a simple environment and the other half in a complex environment. Populations with an evolutionary history of sexual selection maintained larger sizes and more stable growth rates in complex (relative to simple) environments, an effect not seen in populations evolved without sexual selection. These results have implications for evolutionary forecasting and suggest that the negative demographic impact of sexually selected mating strategies might be low in natural populations.

Sexual selection and the nonrandom union of gametes: retesting for assortative mating by fitness in Drosophila melanogaster.

While numerous theoretical population genetic models predict that mating assortatively by genetic "quality" will enhance the efficiency of purging of deleterious mutations and/or the spread of beneficial alleles in the gene pool, empirical examples of assortative mating by quality are surprisingly rare and often inconclusive. Here, we set out to examine whether fruit flies (Drosophila melanogaster) engage in assortative mating by body-size phenotype, a composite trait strongly associated with both reproductive success and survival and is considered a reliable indicator of natural genetic quality. Male and female flies of different body-size classes (large and small) were obtained under typical culture conditions, which allows us to use standing variation of body size without involving artificial nutritional manipulation, so that their interactions and mating patterns could be measured. While flies did not exhibit assortative courtship behavior, when patterns of offspring production were analyzed, it was found that individuals produced more offspring with partners of similar quality/body size, resulting produced from disassortative mating. Together, these results validate theoretical predictions that sexual selection can enhance the effects of natural selection and consequently the rate of adaptive evolution in a positive correlation in fitness between mates. Subsequent assays of offspring fitness indicated that assortative mating produced sons and daughters that had greater or equal reproductive success than those.

Individual Variation in Male Pheromone Production in Xylocopa sonorina Correlates with size and Gland Color.

Sex pheromones are species-specific chemical signals that facilitate the location, identification, and selection of mating partners. These pheromones can vary between individuals, and act as signals of mate quality. Here, we investigate the variation of male pheromones in the mesosomal glands of the large carpenter bee Xylocopa sonorina, within a Northern California population. We tested the hypothesis that morphological traits are correlated with the observed variation in chemical blend composition of these bees. We also conducted behavioral assays to test whether these male pheromones act as long-range attractants to conspecifics. We found that larger males with darker mesosomal glands have a higher pheromone amount in their glands. Our analysis also suggests that this pheromone blend functions as a long-range attractant to both males and females. We show that both male body size and sexual maturation are important factors influencing pheromone abundance, and that this pheromone blend acts as a long-range attractant. We hypothesize that this recorded variation in male pheromone could be important for female choice.

Love Matters: The Effect of Mating Motive on Female Food Choice.

The prevalence of obesity has been increasing globally in recent decades. Behind the phenomenon, high-fat food consumption has been conceived as an important driver. In the current study, we explored whether mating motive caused an effect on female food choice as well as the psychological mechanism underlying it. In Study 1, we recruited 64 participants from a university and asked them to complete a mating prime, after which they would finish a food choice task in which food with different flavors were shown. In Study 2, we replicated Study 1 with a different mating priming method and examined the mediating role of body shaping desire on the relation between mating motive and female food choice. Results showed that: (1) The salience of mating motive decreased female's high-fat food choice but increased male's high-fat food choice; (2) the effect of mating motive in females was robust and more salient for sweet food rather than salty food; and (3) the body shaping desire partially mediated the effect of mating motive on female food choice.

Divergent preference functions generate directional selection in a jumping spider.

Sexual selection has long been thought to promote speciation, but this possibility still remains a topic of controversy. Many theoretical models have been developed to understand the relationship between sexual selection and speciation, but such relationship seems complex and sexual selection has also been argued to prevent speciation in many scenarios. Here, I model for the first time the tendency of speciation due to sexual selection using realistic model parameters input collected from an existing species, the jumping spider Hasarius adansoni. I show that, even though the species has substantial female variance in preference (the model typically thought to link sexual selection to speciation), when realistic parameters are input in the model, it predicts directional selection, rather than disruptive selection. I propose that including realistic parameters in speciation models is a new tool that will help us understand how common sexual selection helps or hinders speciation in the real world.

Social Plasticity Enhances Signal-Preference Codivergence.

AbstractThe social environment is often the most dynamic and fitness-relevant environment animals experience. Here we tested whether plasticity arising from variation in social environments can promote signal-preference divergence-a key prediction of recent speciation theory but one that has proven difficult to test in natural systems. Interactions in mixed social aggregations could reduce, create, or enhance signal-preference differences. In the latter case, social plasticity could establish or increase assortative mating. We tested this by rearing two recently diverged species of Enchenopa treehoppers-sap-feeding insects that communicate with plant-borne vibrational signals-in treatments consisting of mixed-species versus own-species aggregations. Social experience with heterospecifics (in the mixed-species treatment) resulted in enhanced signal-preference species differences. For one of the two species, we tested but found no differences in the plastic response between sympatric and allopatric sites, suggesting the absence of reinforcement in the signals and preferences and their plastic response. Our results support the hypothesis that social plasticity can create or enhance signal-preference differences and that this might occur in the absence of long-term selection against hybridization on plastic responses themselves. Such social plasticity may facilitate rapid bursts of diversification.

Social opportunities and mate preference improve breeding success in Caribbean iguanas.

Conservation breeding of West Indian rock iguanas (Cyclura) has met with limited success historically. Many facilities witness high levels of aggression and mate incompatibility resulting in failed breeding introductions which often require animals to be separated. This may be due, in part, to lack of knowledge of how mate familiarity and preference affect reproductive outcomes in these species. We investigated whether social exposure during the pre-breeding season influenced copulation success, egg production, and breeding behaviors. Additionally, we examined whether mate preference, as determined by pre-mating dichotomous choice tests, increased these reproductive outcomes. Female rock iguanas that were socialized with males prior to breeding opportunities copulated with familiar males for longer periods of time than females that were not socialized. Socialization opportunities did not alter male reproductive success measurements or breeding behavior. Female rock iguanas introduced for mating to their preferred partners had a higher probability of successful copulations, higher average number of copulations, and less resting behavior during introductions than females mated to non-preferred males. Male mate preference had no effect on reproductive success measurements during mating introductions. These results indicate that socializing animals and providing mate choice opportunities increase breeding success of rock iguanas under managed care.

Inferred Attractiveness: A generalized mechanism for sexual selection that can maintain variation in traits and preferences over time.

Sexual selection by mate choice is a powerful force that can lead to evolutionary change, and models of why females choose particular mates are central to understanding its effects. Predominant mate choice theories assume preferences are determined solely by genetic inheritance, an assumption still lacking widespread support. Moreover, preferences often vary among individuals or populations, fail to correspond with conspicuous male traits, or change with context, patterns not predicted by dominant models. Here, we propose a new model that explains this mate choice complexity with one general hypothesized mechanism, "Inferred Attractiveness." In this model, females acquire mating preferences by observing others' choices and use context-dependent information to infer which traits are attractive. They learn to prefer the feature of a chosen male that most distinguishes him from other available males. Over generations, this process produces repeated population-level switches in preference and maintains male trait variation. When viability selection is strong, Inferred Attractiveness produces population-wide adaptive preferences superficially resembling "good genes." However, it results in widespread preference variation or nonadaptive preferences under other predictable circumstances. By casting the female brain as the central selective agent, Inferred Attractiveness captures novel and dynamic aspects of sexual selection and reconciles inconsistencies between mate choice theory and observed behavior.

When less is more: coy display behaviours and the temporal dynamics of animal courtship.

Sexual selection research has been dominated by the notion that mate choice selects for the most vigorous displays that best reflect the quality of the courter. However, courtship displays are often temporally structured, containing different elements with varying degrees of intensity and conspicuousness. For example, highly intense movements are often coupled with more subtle components such as static postures or hiding displays. Here, we refer to such subtle display traits as 'coy', as they involve the withholding of information about maximal display capabilities. We examine the role of intensity variation within temporally dynamic displays, and discuss three hypotheses for the evolution of coy courtship behaviours. We first review the threat reduction hypothesis, which points to sexual coercion and sexual autonomy as important facets of sexual selection. We then suggest that variation in display magnitude exploits pre-existing perceptual biases for temporal contrast. Lastly, we propose that information withholding may leverage receivers' predispositions for filling gaps in information-the 'curiosity bias'. Overall, our goal is to draw attention to temporal variation in display magnitude, and to advocate possible scenarios for the evolution of courtship traits that regularly occur below performance maxima. Throughout, we highlight novel directions for empirical and theoretical investigations.

Effect of light bias on male mating signal and female mate choice in a sexually dimorphic Amazon fish.

Colourful signals are usually honest indicators of mate quality since they are energetically costly. However, how colours are perceived by choosers is highly affected by the environmental light condition. Amazon black waters are strongly red-biased while clear waters show no apparent colour bias. The sailfin tetra Crenuchus spilurus is a sexually dimorphic Amazon fish species; males have hyperallometric dorsal and anal fins conspicuously ornamented with red and yellow markings. The species has two main lineages, which inhabit black and clear waters. A comparison of the red colouration of the ornaments of males from different lineages indicates that red bias increases the perceived intensity of red colouration but decreases the perceived among-individual variation in red colour. In mate choice experiments, females from all lineages preferred males with larger ornaments. Clear water lineage females were more likely to accept males under red-biased lighting, which increases the apparent red colouration, suggesting the importance of the red colouration in their mate choice. On the other hand, male acceptance by females from black waters did not change under different light conditions, suggesting that signals other than the red colouration (e.g. size of ornaments) were more important in their mate choice.

Mate Discrimination Using Chemical Cues by Male Guppies.

Males often perform mate choice with the aim of maximizing reproductive success. To identify profitable mates, the males of some animals are known to use visual and chemical cues derived from females. In this study, we aimed to examine mate discrimination by male guppies (Poecilia reticulata) using chemical cues received from females under different reproductive statuses, i.e., virgin females, pregnant females, females after copulation with another male, and post-partum females. We conducted a dichotomous choice experiment for each combination of chemical stimuli from females under different reproductive statuses. In experiment 1, in which females were removed from water that was subsequently used as a chemical stimulus, male preferences did not differ significantly in all combinations of chemical stimuli from females under different reproductive statuses. However, in experiment 2, in which females remained within bottles containing the water used as a chemical stimulus, with the exception of one combination of chemical stimuli, significant differences in male preferences were detected for chemical stimuli derived from females under different reproductive statuses. Overall, males generally showed a preference for chemical stimulus received from females after copulation with other males. The findings of this study indicate that male guppies can discriminate the reproductive status of females based solely on chemical cues that may disappear or degenerate within a short period of time, thereby facilitating profitable mate choice.

Interplay between male quality and male-female compatibility across episodes of sexual selection.

The processes underlying mate choice profoundly influence the dynamics of sexual selection and the evolution of male sexual traits. Consistent preference for certain phenotypes may erode genetic variation in populations through directional selection, whereas divergent preferences (e.g., genetically compatible mates) provide one mechanism to maintain such variation. However, the relative contributions of these processes across episodes of selection remain unknown. Using Drosophila melanogaster, we followed the fate of male genotypes, previously scored for their overall reproductive value and their compatibility with different female genotypes, across pre- and postmating episodes of selection. When pairs of competitor males differed in their intrinsic quality and their compatibility with the female, both factors influenced outcomes from mating success to paternity but to a varying degree between stages. These results add further dimensions to our understanding of how the interactions between genotypes and forms of selection shape reproductive outcomes and ultimately reproductive trait evolution.