Eviction-driven infanticide and sexually selected adoption and infanticide in a neotropical parrot.

Infanticide and adoption have been attributed to sexual selection, where an individual later reproduces with the parent whose offspring it killed or adopted. While sexually selected infanticide is well known, evidence for sexually selected adoption is anecdotal. We report on both behaviors at 346 nests over 27 y in green-rumped parrotlets (Forpus passerinus) in Venezuela. Parrotlets are monogamous with long-term pair bonds, exhibit a strongly male-biased adult sex ratio, and nest in cavities that are in short supply, creating intense competition for nest sites and mates. Infanticide attacks occurred at 256 nests in two distinct contexts: 1) Attacks were primarily committed by nonbreeding pairs (69%) attempting to evict parents from the cavity. Infanticide attacks per nest were positively correlated with population size and evicting pairs never adopted abandoned offspring. Competition for limited nest sites was a primary cause of eviction-driven infanticide, and 2) attacks occurred less frequently at nests where one mate died (31%), was perpetrated primarily by stepparents of both sexes, and was independent of population size. Thus, within a single species and mating system, infanticide occurred in multiple contexts due to multiple drivers. Nevertheless, 48% of stepparents of both sexes adopted offspring, and another 23% of stepfathers exhibited both infanticide and long-term care. Stepfathers were often young males who subsequently nested with widows, reaching earlier ages of first breeding than competitors and demonstrating sexually selected adoption. Adoption and infanticide conferred similar fitness benefits to stepfathers and appeared to be equivalent strategies driven by limited breeding opportunities, male-biased sex ratios, and long-term monogamy.

Divergence in Reproductive Behaviors Is Associated with the Evolutionary Loss of Parental Care.

AbstractThe mechanisms underlying the divergence of reproductive strategies between closely related species are still poorly understood. Additionally, it is unclear which selective factors drive the evolution of reproductive behavioral variation and how these traits coevolve, particularly during early divergence. To address these questions, we quantified behavioral differences in a recently diverged pair of Nova Scotian three-spined stickleback (Gasterosteus aculeatus) populations, which vary in parental care, with one population displaying paternal care and the other lacking this. We compared both populations, and a full reciprocal F1 hybrid cross, across four major reproductive stages: territoriality, nesting, courtship, and parenting. We identified significant divergence in a suite of heritable behaviors. Importantly, F1 hybrids exhibited a mix of behavioral patterns, some of which suggest sex linkage. This system offers fresh insights into the coevolutionary dynamics of reproductive behaviors during early divergence and offers support for the hypothesis that coevolutionary feedback between sexual selection and parental care can drive rapid evolution of reproductive strategies.

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.

Filling the gaps in ecology of tropical tiger beetles (Coleoptera: Cicindelidae): first quantitative data of sexual dimorphism in semi-arboreal Therates from the Philippine biodiversity hotspot.

Background: Sexual dimorphism, driven by sexual selection, leads to varied morphological distinctions in male and female insects, providing insights into selection pressures across species. However, research on the morphometric variability within specific taxa of tiger beetles (Coleoptera: Cicindelidae), particularly arboreal and semi-arboreal species, remains very limited. Methods: We investigate sexual dimorphism in six semi-arboreal Therates tiger beetle taxa from the Philippines, focusing on morphological traits. We employed morphometric measurements and multivariate analyses to reveal patterns of sexual dimorphism between sexes within the taxa. Results: Our results indicate significant sexual dimorphism in elytra width, with females consistently displaying broader elytra, potentially enhancing fecundity. Notable sexual size dimorphism was observed in Therates fulvipennis bidentatus and T. coracinus coracinus, suggesting heightened sexual selection pressures on male body size. Ecological factors, mating behavior, and female mate choice might contribute to the observed morphological variation. These findings emphasize the need for further studies to comprehend mating dynamics, mate choice, and ecological influences on morphological variations in semi-arboreal and arboreal tiger beetles.

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.

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.

Fossil evidence sheds light on sexual selection during the early evolution of birds.

The impact of sexual selection on the evolution of birds has been widely acknowledged. Although sexual selection has been hypothesized as a driving force in the occurrences of numerous morphological features across theropod evolution, this hypothesis has yet to be comprehensively tested due to challenges in identifying the sex of fossils and by the limited sample size. Confuciusornis sanctus is arguably the best-known early avialan and is represented by thousands of well-preserved specimens from the Early Cretaceous Jehol lagerstätte, which provides us with a chance to decipher the strength of sexual selection on extinct vertebrates. Herein, we present a morphometric study of C. sanctus based on the largest sample size of this taxon collected up to now. Our results indicate that the characteristic elongated paired rectrices is a sexually dimorphic trait and statistically robust inferences of the sexual dimorphism in size, shape, and allometry that have been established, providing the earliest known sexual dimorphism in avian evolution. Our findings suggest that sexual selection, in conjunction with natural selection, does act upon body size and limb length ratio in early birds, thereby promoting a deeper understanding of the role of sexual selection in large-scale phylogenetic evolution.

On the function of a female-like signal type in the vibrational repertoire of Enchenopa male treehoppers (Hemiptera: Membracidae).

Animals often mimic the behaviours or signals of conspecifics of the opposite sex while courting. We explored the potential functions of a novel female-like signal type in the courtship displays of male Enchenopa treehoppers. In these plant-feeding insects, males produce plant-borne vibrational advertisement signals, to which females respond with their own duetting signals. Males also produce a signal type that resembles the female duetting responses. We experimentally tested whether this signal modifies the behaviour of receivers. First, we tested whether the female-like signal would increase the likelihood of a female response. However, females were as likely to respond to playbacks with or without them. Second, we tested whether the female-like signal would inhibit competing males, but males were as likely to produce displays after playbacks with or without them. Hence, we found no evidence that this signal has an adaptive function, despite its presence in the courtship display, where sexual selection affects signal features. Given these findings, we also explored whether the behavioural and morphological factors of the males were associated with the production of the female-like signal. Males that produced this signal had higher signalling effort (longer and more frequent signals) than males that did not produce it, despite being in worse body condition. Lastly, most males were consistent over time in producing the female-like signal or not. These findings suggest that condition-dependent or motivational factors explain the presence of the female-like signal. Alternatively, this signal might not bear an adaptive function, and it could be a way for males to warm up or practice signalling, or even be a by-product of how signals are transmitted through the plant. We suggest further work that might explain our puzzling finding that a signal in the reproductive context might not have an adaptive function.

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.

Host Plant Effects on Sexual Selection Dynamics in Phytophagous Insects.

Natural selection is notoriously dynamic in nature, and so, too, is sexual selection. The interactions between phytophagous insects and their host plants have provided valuable insights into the many ways in which ecological factors can influence sexual selection. In this review, we highlight recent discoveries and provide guidance for future work in this area. Importantly, host plants can affect both the agents of sexual selection (e.g., mate choice and male-male competition) and the traits under selection (e.g., ornaments and weapons). Furthermore, in our rapidly changing world, insects now routinely encounter new potential host plants. The process of adaptation to a new host may be hindered or accelerated by sexual selection, and the unexplored evolutionary trajectories that emerge from these dynamics are relevant to pest management and insect conservation strategies. Examining the effects of host plants on sexual selection has the potential to advance our fundamental understanding of sexual conflict, host range evolution, and speciation, with relevance across taxa.

Sexual selection buffers the negative consequences of population fragmentation on adaptive plastic responses to increasing temperatures.

Whether sexual selection facilitates or hampers the ability to plastically respond to novel environments might depend on population structure, via its effects on sexual interactions and associated fitness payoffs. Using experimentally evolved lines of the seed beetle Callosobruchus maculatus, we tested whether individuals evolving under different sexual selection (monogamy vs. polygamy) and population spatial structure (metapopulation vs. undivided populations) treatments differed in their response across developmental thermal conditions (control, hot, or stressful) in a range of fitness and fitness-associated traits. We found that individuals from subdivided populations had lower lifetime reproductive success at hot temperatures, but only in lines evolving under relaxed sexual selection, revealing a complex interaction between sexual selection, population structure, and thermal environmental stress on fitness. We also found an effect of population structure on several traits, including fertility and adult emergence success, under exposure to high thermal conditions. Finally, we found a strong negative effect of hot and stressful temperatures on fitness and associated traits. Our results show that population structure can exacerbate the impact of a warming climate, potentially leading to declines in population viability, but that sexual selection can buffer the negative influence of population subdivision on adaptation to warm temperatures.

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.

Convergent rates of protein evolution identify novel targets of sexual selection in primates.

Sexual selection is the differential reproductive success of individuals, resulting from competition for mates, mate choice, or success in fertilization. In primates, this selective pressure often leads to the development of exaggerated traits which play a role in sexual competition and successful reproduction. In order to gain insight into the mechanisms driving the development of sexually selected traits, we used an unbiased genome-wide approach across 21 primate species to correlate individual rates of protein evolution to relative testes size and sexual dimorphism in body size, 2 anatomical hallmarks of sexual selection in mammals. Among species with presumed high levels of sperm competition, we detected strong conservation of testes-specific proteins responsible for spermatogenesis and ciliary form and function. In contrast, we identified accelerated evolution of female reproductive proteins expressed in the vagina, cervix, and fallopian tubes in these same species. Additionally, we found accelerated protein evolution in lymphoid tissue, indicating that adaptive immune functions may also be influenced by sexual selection. This study demonstrates the distinct complexity of sexual selection in primates revealing contrasting patterns of protein evolution between male and female reproductive tissues.

Contrasting the form and strength of pre- and postcopulatory sexual selection in a flatworm.

Sexual traits may be selected during multiple consecutive episodes of selection, occurring before, during, or after copulation. The overall strength and form of selection acting on traits may thus be determined by how selection (co-)varies along different episodes. However, it is challenging to measure pre- and postcopulatory phenotypic traits alongside variation in fitness components at each different episode. Here, we used a transgenic line of the transparent flatworm Macrostomum lignano expressing green fluorescent protein (GFP) in all cell types, including sperm cells, enabling in vivo sperm tracking. We assessed the mating success, sperm-transfer efficiency, and sperm fertilizing efficiency of GFP(+) focal worms in which we measured 13 morphological traits. We found linear selection on sperm production rate arising from pre- and postcopulatory components and on copulatory organ shape arising from sperm fertilizing efficiency. We further found nonlinear (mostly concave) selection on combinations of copulatory organ and sperm morphology traits arising mostly from sperm-transfer efficiency and sperm fertilizing efficiency. Our study provides a fine-scale quantification of sexual selection, showing that both the form and strength of selection can change across fitness components. Quantifying how sexual selection builds up along episodes of selection allows us to better understand the evolution of sexually selected traits.

Digest: Understanding the evolution of sexual dichromatism also requires a female perspective.

The study of sexual dichromatism has generally focused on sexual selection for conspicuous males, ignoring the potential role played by selection in females. To address this problem, Price et al. took into account evolutionary changes in both males and females when investigating the evolution of plumage dichromatism across the New World blackbirds (Icteridae). They found that sexual dichromatism was repeatedly and rapidly lost as females evolved male-like plumage traits. The evolutionary dynamics in plumage coloration were drastically different in males and females, highlighting the importance of considering both perspectives in trait evolution.

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.

The macroevolutionary dynamics of mammalian sexual size dimorphism.

Sexual size dimorphism (SSD) is a common phenomenon across the animal kingdom. Mammals are unusual in primarily displaying male-biased SSD, where males of a species are typically larger than females. The driving factors behind the evolution of this SSD have been much debated, with popular hypotheses invoking the influence of mating system and social organization via sexual selection, dietary niche divergence and broad-scale correlations with body size (Rensch's rule). Here, we investigate the macroevolutionary origins and maintenance of SSD among mammals, using phylogenetic general mixed linear models and a comprehensive global dataset to evaluate correlations of diet, body mass, seasonality, social organization and mating system with SSD type. We find that SSD as a whole is lost at a greater rate than it is gained, with female-biased SSD being particularly unstable. Non-monogamous mating systems, vertebrate prey consumption and temperature seasonality correlate with male-biased SSD, while polyandry correlates with female-biased SSD, and both types of SSD are positively correlated with body mass. This is in partial contrast to the predictions of Rensch's rule, which predicts that female-biased SSD would correlate negatively with body size. Taken together, our results highlight the importance of considering multiple ecological and social drivers when evaluating the macroevolutionary trajectory of sex differences in body size.

Sexes in sync: phenotypic plasticity, sexual selection and phenological synchrony between the sexes in a wild hibernator.

Desynchrony of phenological responses to climate change is a major concern for ecological communities. Potential uncoupling between one of the most fundamental divisions within populations, males and females, has not been well studied. To address this gap, we examined sex-specific plasticity in hibernation phenology in two populations of Columbian ground squirrels (Urocitellus columbianus). We find that both sexes display similar phenological plasticity to spring snowmelt dates in their timing of torpor termination and behavioural emergence from hibernation. As a result of this plasticity, the degree of protandry (i.e. males' emergences from hibernation preceding those of females) did not change significantly over the 27-year study. Earlier male behavioural emergence, relative to females, improved the likelihood of securing a breeding territory and increased annual reproductive success. Sexual selection favouring earlier male emergence from hibernation may maintain protandry in this population, but did not contribute to further advances in male phenology. Together, our results provide evidence that the sexes should remain synchronized, at least in response to the weather variation investigated here, and further support the role of sexual selection in the evolution of protandry in sexually reproducing organisms.

Sexual selection for extreme physical performance in a polygynous bird is associated with exceptional sex differences in oxygen carrying capacity.

In many animals, males compete for access to fertile females. The resulting sexual selection leads to sex differences in morphology and behaviour, but may also have consequences for physiology. Pectoral sandpipers are an arctic-breeding polygynous shorebird in which males perform elaborate displays around-the-clock and move over long distances to sample potential breeding sites, implying the need for physiological adaptations to cope with extreme endurance. We examined the oxygen carrying capacity of pectoral sandpipers, measured as the volume percentage of red blood cells in blood (haematocrit, Hct). We found a remarkable sex difference in Hct levels, with males having much higher values (58.9 ± 3.8 s.d.) than females (49.8 ± 5.3 s.d.). While Hct values of male pectoral sandpipers are notable for being among the highest recorded in birds, the sex difference we report is unprecedented and more than double that of any previously described. We also show that Hct values declined after arrival to the breeding grounds in females, but not in males, suggesting that males maintain an aerobic capacity during the mating period equivalent to that sustained during trans-hemispheric migration. We conclude that sexual selection for extreme physical performance in male pectoral sandpipers has led to exceptional sex differences in oxygen carrying capacity.