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.

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.

Thermal Plasticity in Behavioral Traits Mediates Mating and Reproductive Dynamics in an Ectotherm.

AbstractEnvironmental temperatures potentially influence reproductive performance and sexual selection by restricting opportunities for activity. However, explicit tests of the behavioral mechanisms linking thermal variation to mating and reproductive performance are rare. We address this gap in a temperate lizard by combining social network analysis with molecular pedigree reconstruction in a large-scale thermal manipulation experiment. Populations exposed to cool thermal regimes presented fewer high-activity days compared with populations exposed to a warmer regime. While plasticity in thermal activity responses in males masked overall differences in activity levels, prolonged restriction nevertheless affected the timing and consistency of male-female interactions. Females were less capable than males of compensating for lost activity time under cold stress, and less active females in this group were significantly less likely to reproduce. While sex-biased activity suppression appeared to limit male mating rates, this did not correspond to a heightened intensity of sexual selection or shifts in the targets of sexual selection. In many populations facing thermal activity restriction, sexual selection on males may play a limited role relative to other thermal performance traits in facilitating adaptation.

Morphology, nuclear SNPs and mate selection reveal that COI barcoding overestimates species diversity in a Mediterranean freshwater amphipod by an order of magnitude.

DNA sequence information has revealed many morphologically cryptic species worldwide. For animals, DNA-based assessments of species diversity usually rely on the mitochondrial cytochrome c oxidase subunit I (COI) gene. However, a growing amount of evidence indicate that mitochondrial markers alone can lead to misleading species diversity estimates due to mito-nuclear discordance. Therefore, reports of putative species based solely on mitochondrial DNA should be verified by other methods, especially in cases where COI sequences are identical for different morphospecies or where divergence within the same morphospecies is high. Freshwater amphipods are particularly interesting in this context because numerous putative cryptic species have been reported. Here, we investigated the species status of the numerous mitochondrial molecular operational taxonomic units (MOTUs) found within Echinogammarus sicilianus. We used an integrative approach combining DNA barcoding with mate selection observations, detailed morphometrics and genome-wide double digest restriction site-associated DNA sequencing (ddRAD-seq). Within a relatively small sampling area, we detected twelve COI MOTUs (divergence = 1.8-20.3%), co-occurring in syntopy at two-thirds of the investigated sites. We found that pair formation was random and there was extensive nuclear gene flow among the ten MOTUs co-occurring within the same river stretch. The four most common MOTUs were also indistinguishable with respect to functional morphology. Therefore, the evidence best fits the hypothesis of a single, yet genetically diverse, species within the main river system. The only two MOTUs sampled outside the focal area were genetically distinct at the nuclear level and may represent distinct species. Our study reveals that COI-based species delimitation can significantly overestimate species diversity, highlighting the importance of integrative taxonomy for species validation, especially in hyperdiverse complexes with syntopically occurring mitochondrial MOTUs.

2-D sex images elicit mate copying in fruit flies.

Although the environment is three-dimensional (3-D), humans are able to extract subtle information from two-dimensional (2-D) images, particularly in the domain of sex. However, whether animals with simpler nervous systems are capable of such information extraction remains to be demonstrated, as this ability would suggest a functional generalisation capacity. Here, we performed mate-copying experiments in Drosophila melanogaster using 2-D artificial stimuli. Mate copying occurs when naïve females observe the mating success of potential mates and use that social information to build their own mating preference. By replacing live demonstrations with (i) photos or (ii) simplified images of copulating pairs, we found that even crudely simplified images of sexual intercourse still elicit mate copying, suggesting that Drosophila is able to extract sex-related information even from a degraded image. This new method constitutes a powerful tool to further investigate mate copying in that species and sexual preferences in general.

Mate Sampling Behavior Determines the Density Dependence of Sexual Selection.

AbstractTheory predicts that the strength of sexual selection (i.e., how well a trait predicts mating or fertilization success) should increase with population density, yet empirical support remains mixed. We explore how this discrepancy might reflect a disconnect between current theory and our understanding of the strategies individuals use to choose mates. We demonstrate that the density dependence of sexual selection predicted by previous theory arises from the assumption that individuals automatically sample more potential mates at higher densities. We provide an updated theoretical framework for the density dependence of sexual selection by (1) developing models that clarify the mechanisms through which density-dependent mate sampling strategies might be favored by selection and (2) using simulations to determine how sexual selection changes with population density when individuals use those strategies. We find that sexual selection may increase strongly with density if sampling strategies change adaptively in response to density-dependent sampling costs, whereas within-individual plasticity in sampling over time (e.g., due to adaptation to increasing sampling costs as the breeding season progresses) produces weaker density-dependent sexual selection. Our findings suggest that density dependence of sexual selection depends on the ecological context in which mate sampling has evolved.

A comprehensive overview of the effects of urbanisation on sexual selection and sexual traits.

Urbanisation can affect mating opportunities and thereby alter inter- and intra-sexual selection pressures on sexual traits. Biotic and abiotic urban conditions can influence an individual's success in pre- and post-copulatory mating, for example through impacts on mate attraction and mate preference, fertilisation success, resource competition or rival interactions. Divergent sexual selection pressures can lead to differences in behavioural, physiological, morphological or life-history traits between urban and non-urban populations, ultimately driving adaptation and speciation. Most studies on urban sexual selection and mating interactions report differences between urban and non-urban populations or correlations between sexual traits and factors associated with increased urbanisation, such as pollution, food availability and risk of predation and parasitism. Here we review the literature on sexual selection and sexual traits in relation to urbanisation or urban-associated conditions. We provide an extensive list of abiotic and biotic factors that can influence processes involved in mating interactions, such as signal production and transmission, mate choice and mating opportunities. We discuss all relevant data through the lens of two, non-mutually exclusive theories on sexual selection, namely indicator and sensory models. Where possible, we indicate whether these models provide the same or different predictions regarding urban-adapted sexual signals and describe different experimental designs that can be useful for the different models as well as to investigate the drivers of sexual selection. We argue that we lack a good understanding of: (i) the factors driving urban sexual selection; (ii) whether reported changes in traits result in adaptive benefits; and (iii) whether these changes reflect a short-term ecological, or long-term evolutionary response. We highlight that urbanisation provides a unique opportunity to study the process and outcomes of sexual selection, but that this requires a highly integrative approach combining experimental and observational work.

Male and female developmental temperature modulate post-copulatory interactions in a beetle.

Sexual selection theory has proven to be fundamental to our understanding of the male-female (sperm-egg) interactions that characterise fertilisation. However, sexual selection does not operate in a void and abiotic environmental factors have been shown to modulate the outcome of pre-copularory sexual interactions. Environmental modulation of post-copulatory interactions are particularly likely because the form and function of primary reproductive traits appears to be acutely sensitive to temperature stress. Here we report the effects of developmental temperature on female reproductive architecture and the interaction between male and female developmental temperature on the outcome of sperm competition in the bruchid beetle Callosobruchus maculatus. When females were reared at developmental temperatures above and below typical temperatures the bursa copulatrix (site of spermatophore deposition) were smaller and, were either shorter and broader (high temperatures) or longer and thinner (low temperatures) than those reared at intermediate temperatures. Males and females reared at low developmental temperatures were less likely to mate than those reared at higher temperatures. Where copulation occurred, females reared at the highest temperature copulated for longest, whilst males reared at the lowest temperature spent longer in copula. Male developmental temperature had a significant impact on the outcome of sperm competition: males reared at 17 °C were largely unsuccessful in sperm competition against control (27 °C) males, although some of the variation in the outcome of sperm competition was a product of the interaction between male and female developmental temperature. Our results demonstrate that male-female interactions that characterise pre- and post-copulatory outcomes are sensitive to developmental temperature and that plasticity in cryptic female preferences could lead to heterogeneous selection on the male reproductive phenotype.

Positive-to-negative behavioural responses suggest hedonic evaluation in treefrog mate choice.

Sexual competition hinges on the ability to impress other conspecifics, to drive them away or attract them. In such cases, the selective environment may be hedonic or affective in nature, as it consists of the evaluations of the individuals making the decisions. This may contribute to the power of sexual selection because evaluations may range from positive to negative rather than simply from positive to neutral. Selection due to mate choice may therefore be stronger than currently appreciated. Further, change in preferred mate types can occur simply by changes (flips) in the evaluation of similar display features, adding to the dynamism of sexual selection as well as its strength. We tested the hypothesis of positive-to-negative behavioural responses in mate choice with a playback experiment using two treefrog species with 'mirror image' structures in their advertisement and aggressive calls. Female treefrog responses ranged from approach to evasion, and the presence of an aversive stimulus tainted evaluation of an attractive stimulus. Further, females in the two species showed flips in approach/evasion of stimuli with comparable signal structure. These results suggest that hedonic evaluation may have an important role in mate choice and showcase how mechanistic analysis can help understand evolutionary processes.

Male coloration affects female gestation period and timing of fertilization in the guppy (Poecilia reticulata).

The trade-up hypothesis is a female behavioral strategy related to mating with multiple males. In this hypothesis, females can produce high-quality offspring while avoiding the risk of losing reproductive opportunities by non-selective mating with males at first mating and then re-mating with more attractive males. As an internal mechanism to realize this behavioral strategy, we predicted that females would immediately fertilize their eggs when they mated with attractive males, whereas females would delay fertilization when they mated with unattractive males to trade-up sires of offspring. The guppy (Poecilia reticulata) is an ovoviviparous fish with internal fertilization, and females show a clear mate preference based on the area of orange coloration on the bodies of males. In addition, it is known that females show a re-mating strategy consistent with the trade-up hypothesis. We tested whether the attractiveness of mated males affected the gestation period and the timing of fertilization. Females were paired with either colorful males or drab males, and the gestation periods (the number of days from mating to parturition) were compared. In addition, we dissected the abdomens of the females at intervals of several days after mating and observed whether the eggs were fertilized. The gestation period in females that were paired with attractive colorful males was significantly shorter than that in females that were paired with drab males. We found that females that mated with colorful males also had their eggs fertilized earlier than those that mated with drab males. Our findings show that differences in the timing of fertilization according to attractiveness of the mate increase the opportunity for cryptic female choice and trading up.

Fitness costs of female choosiness are low in a socially monogamous songbird.

Female mate choice is thought to be responsible for the evolution of many extravagant male ornaments and displays, but the costs of being too selective may hinder the evolution of choosiness. Selection against choosiness may be particularly strong in socially monogamous mating systems, because females may end up without a partner and forego reproduction, especially when many females prefer the same few partners (frequency-dependent selection). Here, we quantify the fitness costs of having mating preferences that are difficult to satisfy, by manipulating the availability of preferred males. We capitalize on the recent discovery that female zebra finches (Taeniopygia guttata) prefer males of familiar song dialect. We measured female fitness in captive breeding colonies in which one-third of females were given ample opportunity to choose a mate of their preferred dialect (two-thirds of all males; "relaxed competition"), while two-thirds of the females had to compete over a limited pool of mates they preferred (one-third of all males; "high competition"). As expected, social pairings were strongly assortative with regard to song dialect. In the high-competition group, 26% of the females remained unpaired, yet they still obtained relatively high fitness by using brood parasitism as an alternative reproductive tactic. Another 31% of high-competition females paired disassortatively for song dialect. These females showed increased levels of extra-pair paternity, mostly with same-dialect males as sires, suggesting that preferences were not abolished after social pairing. However, females that paired disassortatively for song dialect did not have lower reproductive success. Overall, females in the high-competition group reached equal fitness to those that experienced relaxed competition. Our study suggests that alternative reproductive tactics such as egg dumping can help overcome the frequency-dependent costs of being selective in a monogamous mating system, thereby facilitating the evolution of female choosiness.

Kisspeptin signaling and nNOS neurons in the VMHvl modulate lordosis behavior but not mate preference in female mice.

It was recently shown that kisspeptin neurons in the anteroventral periventricular area (AVPV) orchestrate female sexual behavior, including lordosis behavior and mate preference. A potential target of AVPV kisspeptin signaling could be neurons expressing the neuronal form of nitric oxide synthase (nNOS) in the ventrolateral part of the ventromedial hypothalamus (VMHvl). Therefore, in the present study, we further refined the role of the VHMvl in female sexual behavior. Adult female mice received a bilateral cannula aimed at the VMHvl. A single injection with kisspeptin (Kp-10) or SNAP/BAY, a nitric oxide donor, significantly increased lordosis, whereas the nNOS inhibitor l-NAME decreased it. None of these drugs affected mate preference. Interestingly, administration of GnRH into the VMHvl had no effect on lordosis or mate preference. To determine whether the stimulatory effect of Kp-10 on lordosis was specific to the VMHvl, an additional group of females received Kp-10 directly into the paraventricular nucleus (PVN). No effect was found on lordosis and mate preference. These results suggest that kisspeptin most likely modulates lordosis behavior through nNOS neurons in the VMHvl whereas mate preference is modulated by kisspeptin through a separate neuronal circuit not including the VMHvl.

No water, no mating: Connecting dots from behaviour to pathways.

Insects hold considerable ecological and agricultural importance making it vital to understand the factors impacting their reproductive output. Environmental stressors are examples of such factors which have a substantial and significant influence on insect reproductive fitness. Insects are also ectothermic and small in size which makes them even more susceptible to environmental stresses. The present study assesses the consequence of desiccation on the mating latency and copulations duration in tropical Drosophila melanogaster. We tested flies for these reproductive behavioral parameters at varying body water levels and with whole metabolome analysis in order to gain a further understanding of the physiological response to desiccation. Our results showed that the duration of desiccation is positively correlated with mating latency and mating failure, while having no influence on the copulation duration. The metabolomic analysis revealed three biological pathways highly affected by desiccation: starch and sucrose metabolism, galactose metabolism, and phenylalanine, tyrosine and tryptophan biosynthesis. These results are consistent with carbohydrate metabolism providing an energy source in desiccated flies and also suggests that the phenylalanine biosynthesis pathway plays a role in the reproductive fitness of the flies. Desiccation is a common issue with smaller insects, like Drosophila and other tropical insects, and our findings indicate that this lack of ambient water can immediately and drastically affect the insect reproductive behaviour, which becomes more crucial because of unpredictable and dynamic weather conditions.

Reproductive Character Displacement Drives Diversification of Male Courtship Songs in Drosophila.

AbstractMale secondary sexual traits are one of the most striking and diverse features of the animal kingdom. While these traits are often thought to evolve via sexual selection, many questions remain about their patterns of diversification and their role in speciation. To address these questions, I performed a comparative study of precopulatory male courtship songs of 119 Drosophila species across 10 distinct species groups. I related song divergence to genetic distances, geographic relationships, and sexual isolation between species. On the basis of pairwise Euclidean song distances, species groups typically retained their phylogenetic signal while species within groups diverged five times more in sympatry relative to allopatry, producing a pattern of reproductive character displacement. This occurred despite similar genetic distances in allopatry and sympatry, was exaggerated among younger species pairs, and was driven primarily by the parameter interpulse interval. While sexual isolation in sympatry was high even with low song divergence, these variables were correlated with each other and with increased divergence of female mating preferences in sympatry. The widespread pattern of character displacement implies that allopatric divergence due to processes like sexual selection are very slow relative to sympatric processes such as reinforcement and reproductive interference in driving song diversification across Drosophila.

bric à brac controls sex pheromone choice by male European corn borer moths.

The sex pheromone system of ~160,000 moth species acts as a powerful form of assortative mating whereby females attract conspecific males with a species-specific blend of volatile compounds. Understanding how female pheromone production and male preference coevolve to produce this diversity requires knowledge of the genes underlying change in both traits. In the European corn borer moth, pheromone blend variation is controlled by two alleles of an autosomal fatty-acyl reductase gene expressed in the female pheromone gland (pgFAR). Here we show that asymmetric male preference is controlled by cis-acting variation in a sex-linked transcription factor expressed in the developing male antenna, bric à brac (bab). A genome-wide association study of preference using pheromone-trapped males implicates variation in the 293 kb bab intron 1, rather than the coding sequence. Linkage disequilibrium between bab intron 1 and pgFAR further validates bab as the preference locus, and demonstrates that the two genes interact to contribute to assortative mating. Thus, lack of physical linkage is not a constraint for coevolutionary divergence of female pheromone production and male behavioral response genes, in contrast to what is often predicted by evolutionary theory.

An amygdala circuit that suppresses social engagement.

Innate social behaviours, such as mating and fighting, are fundamental to animal reproduction and survival1. However, social engagements can also put an individual at risk2. Little is known about the neural mechanisms that enable appropriate risk assessment and the suppression of hazardous social interactions. Here we identify the posteromedial nucleus of the cortical amygdala (COApm) as a locus required for the suppression of male mating when a female mouse is unhealthy. Using anatomical tracing, functional imaging and circuit-level epistatic analyses, we show that suppression of mating with an unhealthy female is mediated by the COApm projections onto the glutamatergic population of the medial amygdalar nucleus (MEA). We further show that the role of the COApm-to-MEA connection in regulating male mating behaviour relies on the neuromodulator thyrotropin-releasing hormone (TRH). TRH is expressed in the COApm, whereas the TRH receptor (TRHR) is found in the postsynaptic MEA glutamatergic neurons. Manipulating neural activity of TRH-expressing neurons in the COApm modulated male mating behaviour. In the MEA, activation of the TRHR pathway by ligand infusion inhibited mating even towards healthy female mice, whereas genetic ablation of TRHR facilitated mating with unhealthy individuals. In summary, we reveal a neural pathway that relies on the neuromodulator TRH to modulate social interactions according to the health status of the reciprocating individual. Individuals must balance the cost of social interactions relative to the benefit, as deficits in the ability to select healthy mates may lead to the spread of disease.

The influence of male dominance in female Anastrepha curvicauda mate selection.

Males of the papaya fruit fly, Anastrepha curvicauda Gerstaecker (former Toxotrypana curvicauda), defend a papaya fruit from rivals and males release their sex pheromone to attract and mate with females and offer them an oviposition site. While some aspects of the biology of A. curvicauda are known, such as its reproductive biology, its sex pheromone, and host selection, there is currently no information on the species mate selection process. This paper describes the precopulatory mating behavior of A. curvicauda and elucidates how intrasexual selection affects the mate selection process. We studied the precopulatory mating behavior of dominant and subordinate males and ethograms were devised. The effect of hierarchy was studied in non-choice and choice experiments. Male's repertoire includes 15 behavioral elements, 12 precopulatory, one mating, and two postcopulatory (tandem and encounter). In non-choice experiments, dominant and subordinate males were accepted by females, but when females had the opportunity to choose among males, dominant males were significantly preferred over subordinate ones. The presence of a rival male modified the courting behavior of males and agonistic behavior among males was observed before and during mating.

Responses of intended and unintended receivers to a novel sexual signal suggest clandestine communication.

Inadvertent cues can be refined into signals through coevolution between signalers and receivers, yet the earliest steps in this process remain elusive. In Hawaiian populations of the Pacific field cricket, a new morph producing a novel and incredibly variable song (purring) has spread across islands. Here we characterize the current sexual and natural selection landscape acting on the novel signal by (1) determining fitness advantages of purring through attraction to mates and protection from a prominent deadly natural enemy, and (2) testing alternative hypotheses about the strength and form of selection acting on the novel signal. In field studies, female crickets respond positively to purrs, but eavesdropping parasitoid flies do not, suggesting purring may allow private communication among crickets. Contrary to the sensory bias and preference for novelty hypotheses, preference functions (selective pressure) are nearly flat, driven by extreme inter-individual variation in function shape. Our study offers a rare empirical test of the roles of natural and sexual selection in the earliest stages of signal evolution.

Darwin, sexual selection, and the brain.

One hundred fifty years ago Darwin published The Descent of Man, and Selection in Relation to Sex, in which he presented his theory of sexual selection with its emphasis on sexual beauty. However, it was not until 50 y ago that there was a renewed interest in Darwin's theory in general, and specifically the potency of mate choice. Darwin suggested that in many cases female preferences for elaborately ornamented males derived from a female's taste for the beautiful, the notion that females were attracted to sexual beauty for its own sake. Initially, female mate choice attracted the interest of behavioral ecologists focusing on the fitness advantages accrued through mate choice. Subsequent studies focused on sensory ecology and signal design, often showing how sensory end organs influenced the types of traits females found attractive. Eventually, investigations of neural circuits, neurogenetics, and neurochemistry uncovered a more complete scaffolding underlying sexual attraction. More recently, research inspired by human studies in psychophysics, behavioral economics, and neuroaesthetics have provided some notion of its higher-order mechanisms. In this paper, I review progress in our understanding of Darwin's conjecture of "a taste for the beautiful" by considering research from these diverse fields that have conspired to provide unparalleled insight into the chooser's mate choices.

Mosquito Sexual Selection and Reproductive Control Programs.

The field of mosquito mating biology has experienced a considerable expansion in the past decade. Recent work has generated many key insights about specific aspects of mating behavior and physiology. Here, we synthesize these findings and classify swarming mosquito systems as polygynous. Male mating success is highly variable in swarms and evidence suggests that it is likely determined by both scramble competition between males and female choice. Incorporating this new understanding will improve both implementation and long-term stability of reproductive control tools.