Sexual Selection Increases Male Behavioral Consistency in Drosophila melanogaster.

AbstractSexual selection has been suggested to influence the expression of male behavioral consistency. However, despite predictions, direct experimental support for this hypothesis has been lacking. Here, we investigated whether sexual selection altered male behavioral consistency in Drosophila melanogaster-a species with both pre- and postcopulatory sexual selection. We took 1,144 measures of locomotor activity (a fitness-related trait in D. melanogaster) from 286 flies derived from replicated populations that have experimentally evolved under either high or low levels of sexual selection for >320 generations. We found that high sexual selection males were more consistent (decreased within-individual variance) in their locomotor activity than male conspecifics from low sexual selection populations. There were no differences in behavioral consistency between females from the high and low sexual selection populations. Furthermore, while females were more behaviorally consistent than males in the low sexual selection populations, there were no sex differences in behavioral consistency in high sexual selection populations. Our results demonstrate that behavioral plasticity is reduced in males from populations exposed to high levels of sexual selection. Disentangling whether these effects represent an evolved response to changes in the intensity of selection or are manifested through nongenetic parental effects represents a challenge for future research.

No immediate attentional bias towards or choice bias for male secondary sexual characteristics in Bornean orang-utans (Pongo pygmaeus).

Primate faces provide information about a range of variant and invariant traits, including some that are relevant for mate choice. For example, faces of males may convey information about their health or genetic quality through symmetry or facial masculinity. Because perceiving and processing such information may have bearing on the reproductive success of an individual, cognitive systems are expected to be sensitive to facial cues of mate quality. However, few studies have investigated this topic in non-human primate species. Orang-utans are an interesting species to test mate-relevant cognitive biases, because they are characterised by male bimaturism: some adult males are fully developed and bear conspicuous flanges on the side of their face, while other males look relatively similar to females. Here, we describe two non-invasive computerised experiments with Bornean orang-utans (Pongo pygmaeus), testing (i) immediate attention towards large flanges and symmetrical faces using a dot-probe task (N = 3 individuals; 2F) and (ii) choice bias for pictures of flanged males over unflanged males using a preference test (N = 6 individuals; 4F). In contrast with our expectations, we found no immediate attentional bias towards either large flanges or symmetrical faces. In addition, individuals did not show a choice bias for stimuli of flanged males. We did find exploratory evidence for a colour bias and energy efficiency trade-offs in the preference task. We discuss our null results and exploratory results in the context of the evolutionary history of Bornean orang-utans, and provide suggestions for a more biocentric approach to the study of orang-utan cognition.

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.

Digest: Sexual selection may shape species' range limits.

In a recent study, Tschol et al. (2024) present a model that investigates how 2 different forms of sexual selection, selection for traits that increase mate encounters and selection for traits that enhance one's ability to compete for mates, affect geographical range limits. The model demonstrates that range limits expand in response to selection on mate-encountering traits and contract when selection acts on reproductive competitiveness. When traits coevolve, range limits depend on the mating system. This study demonstrates the importance of accounting for sexual selection and intraspecific interactions when investigating eco-evolutionary dynamics of geographic range limits.

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.

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.

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.

Partitioning variance in a signaling trade-off under sexual selection reveals among-individual covariance in trait allocation.

Understanding the evolution of traits subject to trade-offs is challenging because phenotypes can (co)vary at both the among- and within-individual levels. Among-individual covariation indicates consistent, possibly genetic, differences in how individuals resolve the trade-off, while within-individual covariation indicates trait plasticity. There is also the potential for consistent among-individual differences in behavioral plasticity, although this has rarely been investigated. We studied the sources of (co)variance in two characteristics of an acoustic advertisement signal that trade-off with one another and are under sexual selection in the gray treefrog, Hyla chrysoscelis: call duration and call rate. We recorded males on multiple nights calling spontaneously and in response to playbacks simulating different competition levels. Call duration, call rate, and their product, call effort, were all repeatable both within and across social contexts. Call duration and call rate covaried negatively, and the largest covariance was at the among-individual level. There was extensive plasticity in calling with changes in social competition, and we found some evidence for among-individual variance in call rate plasticity. The significant negative among-individual covariance in trait values is perpendicular to the primary direction of sexual selection in this species, indicating potential limits on the response to selection.

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.

A genetic cause of male mate preference.

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

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.

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.

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.

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.