Decoupled evolution of the Sex Peptide gene family and Sex Peptide Receptor in Drosophilidae.

Across internally fertilising species, males transfer ejaculate proteins that trigger wide-ranging changes in female behaviour and physiology. Much theory has been developed to explore the drivers of ejaculate protein evolution. The accelerating availability of high-quality genomes now allows us to test how these proteins are evolving at fine taxonomic scales. Here, we use genomes from 264 species to chart the evolutionary history of Sex Peptide (SP), a potent regulator of female post-mating responses in Drosophila melanogaster. We infer that SP first evolved in the Drosophilinae subfamily and has since followed markedly different evolutionary trajectories in different lineages. Outside of the Sophophora-Lordiphosa, SP exists largely as a single-copy gene with independent losses in several lineages. Within the Sophophora-Lordiphosa, the SP gene family has repeatedly and independently expanded. Up to seven copies, collectively displaying extensive sequence variation, are present in some species. Despite these changes, SP expression remains restricted to the male reproductive tract. Alongside, we document considerable interspecific variation in the presence and morphology of seminal microcarriers that, despite the critical role SP plays in microcarrier assembly in D. melanogaster, appears to be independent of changes in the presence/absence or sequence of SP. We end by providing evidence that SP's evolution is decoupled from that of its receptor, Sex Peptide Receptor, in which we detect no evidence of correlated diversifying selection. Collectively, our work describes the divergent evolutionary trajectories that a novel gene has taken following its origin and finds a surprisingly weak coevolutionary signal between a supposedly sexually antagonistic protein and its receptor.

An evolutionary innovation for mating facilitates ecological niche expansion and buffers species against climate change.

One of the drivers of life's diversification has been the emergence of "evolutionary innovations": The evolution of traits that grant access to underused ecological niches. Since ecological interactions can occur separately from mating, mating-related traits have not traditionally been considered factors in niche evolution. However, in order to persist in their environment, animals need to successfully mate just as much as they need to survive. Innovations that facilitate mating activity may therefore be an overlooked determinant of species' ecological limits. Here, we show that species' historical niches and responses to contemporary climate change are shaped by an innovation involved in mating-a waxy, ultra-violet-reflective pruinescence produced by male dragonflies. Physiological experiments in two species demonstrate that pruinescence reduces heating and water loss. Phylogenetic analyses show that pruinescence is gained after taxa begin adopting a thermohydrically stressful mating behavior. Further comparative analyses reveal that pruinose species are more likely to breed in exposed, open-canopy microhabitats. Biogeographic analyses uncover that pruinose species occupy warmer and drier regions in North America. Citizen-science observations of Pachydiplax longipennis suggest that the extent of pruinescence can be optimized to match the local conditions. Finally, temporal analyses indicate that pruinose species have been buffered against contemporary climate change. Overall, these historical and contemporary patterns show that successful mating can shape species' niche limits in the same way as growth and survival.

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.

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.

Male harm offsets the demographic benefits of good genes.

Sexual conflict can arise when males evolve traits that improve their mating success but in doing so harm females. By reducing female fitness, male harm can diminish offspring production in a population and even drive extinction. Current theory on harm is based on the assumption that an individual's phenotype is solely determined by its genotype. But the expression of most sexually selected traits is also influenced by variation in biological condition (condition-dependent expression), such that individuals in better condition can express more extreme phenotypes. Here, we developed demographically explicit models of sexual conflict evolution where individuals vary in their condition. Because condition-dependent expression readily evolves for traits underlying sexual conflict, we show that conflict is more intense in populations where individuals are in better condition. Such intensified conflict reduces mean fitness and can thus generate a negative association between condition and population size. The impact of condition on demography is especially likely to be detrimental when the genetic basis of condition coevolves with sexual conflict. This occurs because sexual selection favors alleles that improve condition (the so-called good genes effect), producing feedback between condition and sexual conflict that drives the evolution of intense male harm. Our results indicate that in presence of male harm, the good genes effect in fact easily becomes detrimental to populations.

Parasite effects on receivers in animal communication: Hidden impacts on behavior, ecology, and evolution.

Parasites exert a profound effect on biological processes. In animal communication, parasite effects on signalers are well-known drivers of the evolution of communication systems. Receiver behavior is also likely to be altered when they are parasitized or at risk of parasitism, but these effects have received much less attention. Here, we present a broad framework for understanding the consequences of parasitism on receivers for behavioral, ecological, and evolutionary processes. First, we outline the different kinds of effects parasites can have on receivers, including effects on signal processing from the many parasites that inhabit, occlude, or damage the sensory periphery and the central nervous system or that affect physiological processes that support these organs, and effects on receiver response strategies. We then demonstrate how understanding parasite effects on receivers could answer important questions about the mechanistic causes and functional consequences of variation in animal communication systems. Variation in parasitism levels is a likely source of among-individual differences in response to signals, which can affect receiver fitness and, through effects on signaler fitness, impact population levels of signal variability. The prevalence of parasitic effects on specific sensory organs may be an important selective force for the evolution of elaborate and multimodal signals. Finally, host-parasite coevolution across heterogeneous landscapes will generate geographic variation in communication systems, which could ultimately lead to evolutionary divergence. We discuss applications of experimental techniques to manipulate parasitism levels and point the way forward by calling for integrative research collaborations between parasitologists, neurobiologists, and behavioral and evolutionary ecologists.

Evolutionary predictors of the specific colors of birds.

Animal coloration is one of the most conspicuous aspects of human-perceived organismal diversity, yet also one of the least understood. In particular, explaining why species have specific colors (e.g., blue vs. red) has proven elusive. Here, we quantify for nearly all bird species, the proportion of the body covered by each of 12 human-visible color categories, and test whether existing theory can predict the direction of color evolution. The most common colors are black, white, gray and brown, while the rarest are green, blue, purple, and red. Males have more blue, purple, red, or black, whereas females have more yellow, brown, or gray. Sexual dichromatism is partly due to sexual selection favoring ornamental colors in males but not in females. However, sexual selection also correlated positively with brown in both sexes. Strong social selection favors red and black, colors used in agonistic signaling, with the strongest effects in females. Reduced predation risk selects against cryptic colors (e.g., brown) and favors specific ornamental colors (e.g., black). Nocturnality is mainly associated with brown. The effects of habitat use support the sensory drive theory for camouflage and signaling. Darker colors are more common in species living in wet and cold climates, matching ecogeographical rules. Our study unambiguously supports existing theories of color evolution across an entire class of vertebrates, but much variation remains unexplained.

No neonates without adults: A review of adult black soldier fly biology, Hermetia illucens (Diptera: Stratiomyidae): A review of adult black soldier fly biology, Hermetia illucens (Diptera: Stratiomyidae).

With the potential to process the world's agricultural and food waste, provide sustainable fodder for livestock, aquaculture, and pet animals, as well as act as a source of novel biomolecules, the black soldier fly, Hermetia illucens, has been launched into the leading position within the insects as feed industry. Fulfilment of these goals, however, requires mass-rearing facilities to have a steady supply of neonate larvae, which in-turn requires an efficient mating process to yield fertile eggs; yet, little is known about adult reproductive behavior, nor what physiological factors lead to its emergence. Moreover, fertile egg production tends to be highly variable in colony. Therefore, this review brings together what is currently known of the organismal biology of H. illucens, compiling information on adult morphology, physiology, biogeography, genomics, and behavioral ecology. As a holistic synthesis, it highlights several directions of interest for research to follow.

Molecular parallelism in signaling function across different sexually selected ornaments in a warbler.

Extravagant ornaments are thought to signal male quality to females choosing mates, but the evidence linking ornament size to male quality is controversial, particularly in cases in which females prefer different ornaments in different populations. Here, we use whole-genome sequencing and transcriptomics to determine the genetic basis of ornament size in two populations of a widespread warbler, the common yellowthroat (Geothlypis trichas). Within a single subspecies, females in a Wisconsin population prefer males with larger black masks as mates, while females in a New York population prefer males with larger yellow bibs. Despite being produced by different pigments in different patches on the body, the size of the ornament preferred by females in each population was linked to numerous genes that function in many of the same core aspects of male quality (e.g., immunity and oxidative balance). These relationships confirm recent hypotheses linking the signaling function of ornaments to male quality. Furthermore, the parallelism in signaling function provides the flexibility for different types of ornaments to be used as signals of similar aspects of male quality. This could facilitate switches in female preference for different ornaments, a potentially important step in the early stages of divergence among populations.

The evolution of mating preferences for genetic attractiveness and quality in the presence of sensory bias.

The aesthetic preferences of potential mates have driven the evolution of a baffling diversity of elaborate ornaments. Which fitness benefit-if any-choosers gain from expressing such preferences is controversial, however. Here, we simulate the evolution of preferences for multiple ornament types (e.g., "Fisherian," "handicap," and "indicator" ornaments) that differ in their associations with genes for attractiveness and other components of fitness. We model the costs of preference expression in a biologically plausible way, which decouples costly mate search from cost-free preferences. Ornaments of all types evolved in our model, but their occurrence was far from random. Females typically preferred ornaments that carried information about a male's quality, defined here as his ability to acquire and metabolize resources. Highly salient ornaments, which key into preexisting perceptual biases, were also more likely to evolve. When males expressed quality-dependent ornaments, females invested readily in costly mate search to locate preferred males. In contrast, the genetic benefits associated with purely arbitrary ornaments were insufficient to sustain highly costly mate search. Arbitrary ornaments could nonetheless "piggyback" on mate-search effort favored by other, quality-dependent ornaments. We further show that the potential to produce attractive male offspring ("sexy sons") can be as important as producing offspring of high general quality ("good genes") in shaping female preferences, even when preferred ornaments are quality dependent. Our model highlights the importance of mate-search effort as a driver of aesthetic coevolution.

Assortative mating enhances postzygotic barriers to gene flow via ancestry bundling.

Hybridization and subsequent genetic introgression are now known to be common features of the histories of many species, including our own. Following hybridization, selection often purges introgressed DNA genome-wide. While assortative mating can limit hybridization in the first place, it is also known to play an important role in postzygotic selection against hybrids and, thus, the purging of introgressed DNA. However, this role is usually thought of as a direct one: a tendency for mates to be conspecific reduces the sexual fitness of hybrids, reducing the transmission of introgressed ancestry. Here, we explore a second, indirect role of assortative mating as a postzygotic barrier to gene flow. Under assortative mating, parents covary in their ancestry, causing ancestry to be "bundled" in their offspring and later generations. This bundling effect increases ancestry variance in the population, enhancing the efficiency with which postzygotic selection purges introgressed DNA. Using whole-genome simulations, we show that the bundling effect can comprise a substantial portion of mate choice's overall effect as a postzygotic barrier to gene flow. We then derive a simple method for estimating the impact of the bundling effect from standard metrics of assortative mating. Applying this method to data from a diverse set of hybrid zones, we find that the bundling effect increases the purging of introgressed DNA by between 1.2-fold (in a baboon system with weak assortative mating) and 14-fold (in a swordtail system with strong assortative mating). Thus, assortative mating's bundling effect contributes substantially to the genetic isolation of species.

Sexual repurposing of juvenile aposematism in locusts.

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

Concerted evolution of metabolic rate, economics of mating, ecology, and pace of life across seed beetles.

Male-female coevolution has taken different paths among closely related species, but our understanding of the factors that govern its direction is limited. While it is clear that ecological factors, life history, and the economics of reproduction are connected, the divergent links are often obscure. We propose that a complete understanding requires the conceptual integration of metabolic phenotypes. Metabolic rate, a nexus of life history evolution, is constrained by ecological factors and may exert important direct and indirect effects on the evolution of sexual dimorphism. We performed standardized experiments in 12 seed beetle species to gain a rich set of sex-specific measures of metabolic phenotypes, life history traits, and the economics of mating and analyzed our multivariate data using phylogenetic comparative methods. Resting metabolic rate (RMR) showed extensive evolution and evolved more rapidly in males than in females. The evolution of RMR was tightly coupled with a suite of life history traits, describing a pace-of-life syndrome (POLS), with indirect effects on the economics of mating. As predicted, high resource competition was associated with a low RMR and a slow POLS. The cost of mating showed sexually antagonistic coevolution, a hallmark of sexual conflict. The sex-specific costs and benefits of mating were predictably related to ecology, primarily through the evolution of male ejaculate size. Overall, our results support the tenet that resource competition affects metabolic processes that, in turn, have predictable effects on both life history evolution and reproduction, such that ecology shows both direct and indirect effects on male-female coevolution.

Drosophila females have an acoustic preference for symmetric males.

SignificanceTheoretically, symmetry in bilateral animals is subject to sexual selection, since it can serve as a proxy for genetic quality of competing mates during mate choice. Here, we report female preference for symmetric males in Drosophila, using a mate-choice paradigm where males with environmentally or genetically induced wing asymmetry were competed. Analysis of courtship songs revealed that males with asymmetric wings produced songs with asymmetric features that served as acoustic cues, facilitating this female preference. Females experimentally evolved in the absence of mate choice lost this preference for symmetry, suggesting that it is maintained by sexual selection.

The evolutionary history and spectral tuning of vertebrate visual opsins.

Many animals depend on the sense of vision for survival. In eumetazoans, vision requires specialized, light-sensitive cells called photoreceptors. Light reaches the photoreceptors and triggers the excitation of light-detecting proteins called opsins. Here, we describe the story of visual opsin evolution from the ancestral bilaterian to the extant vertebrate lineages. We explain the mechanisms determining color vision of extant vertebrates, focusing on opsin gene losses, duplications, and the expression regulation of vertebrate opsins. We describe the sequence variation both within and between species that has tweaked the sensitivities of opsin proteins towards different wavelengths of light. We provide an extensive resource of wavelength sensitivities and mutations that have diverged light sensitivity in many vertebrate species and predict how these mutations were accumulated in each lineage based on parsimony. We suggest possible natural and sexual selection mechanisms underlying these spectral differences. Understanding how molecular changes allow for functional adaptation of animals to different environments is a major goal in the field, and therefore identifying mutations affecting vision and their relationship to photic selection pressures is imperative. The goal of this review is to provide a comprehensive overview of our current understanding of opsin evolution in vertebrates.

Human-modified habitats imperil ornamented dragonflies less than their non-ornamented counterparts at local, regional, and continental scales.

Biologists have long wondered how sexual ornamentation influences a species' risk of extinction. Because the evolution of condition-dependent ornamentation can reduce intersexual conflict and accelerate the fixation of advantageous alleles, some theory predicts that ornamented taxa can be buffered against extinction in novel and/or stressful environments. Nevertheless, evidence from the wild remains limited. Here, we show that ornamented dragonflies are less vulnerable to extinction across multiple spatial scales. Population-occupancy models across the Western United States reveal that ornamented species have become more common relative to non-ornamented species over >100 years. Phylogenetic analyses indicate that ornamented species exhibit lower continent-wide extinction risk than non-ornamented species. Finally, spatial analyses of local dragonfly assemblages suggest that ornamented species possess advantages over non-ornamented taxa at living in habitats that have been converted to farms and cities. Together, these findings suggest that ornamented taxa are buffered against contemporary extinction at local, regional, and continental scales.

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.

Natural variation in sexual traits and gene expression between selfing and outcrossing Arabidopsis lyrata suggests sexual selection at work.

Flowering plants show significant diversity in sexual strategies, profoundly impacting the evolution of sexual traits and associated genes. Sexual selection is one of the primary evolutionary forces driving sexual trait variation, particularly evident during pollen-pistil interactions, where pollen grains compete for fertilization and females select mating partners. Multiple mating may intensify competition among pollen donors for siring, while in contrast, self-fertilization reduces sire-sire competition, relaxing the sexual selection pressure. Traits involved in male-male competition and female choice are well described, and molecular mechanisms underlying pollen development and pollen-pistil interactions have been extensively studied in the model species Arabidopsis thaliana. However, whether these molecular mechanisms are involved in sexual selection in nature remains unclear. To address this gap, we measured intrinsic pollen performance and its interaction with female choice, and investigated the associated gene expression patterns in a selfing and an outcrossing population of Arabidopsis lyrata. We found that pollen germination and pollen tube growth were significantly higher in outcrossers than selfers, and this difference was accompanied by changes in expression of genes involved in vesicle transport and cytoskeleton. Outcrosser mother plants showed a negative impact on pollen tube growth compared to selfer mother plants, together with a difference of expression for genes involved in auxin and stress response, suggesting a potential mechanism for female choice through molecular crosstalk at the post-pollination stage. Our study provides insight on the impact of sexual selection on the evolution of sexual gene expression in plants.

Female Preferences for More Elaborate Signals Are an Emergent Outcome of Male Chorusing Interactions in Túngara Frogs.

AbstractIn chorusing species, conspecific interference exerts strong selection on signal form and timing to maximize conspicuousness and attractiveness within the signaling milieu. We investigated how túngara frog calling strategies were influenced by varied social environments and male phenotypes and how calling interactions influenced female preferences. When chorusing, túngara frog calls consist of a whine typically followed by one to three chucks. In experimental choruses we saw that as chorus size increased, calls increasingly had their chucks overlapped by the high-amplitude beginning section of other callers' whines. Playback experiments revealed that such overlap reduced the attractiveness of calls to females but that appending additional chucks mitigated this effect. Thus, more elaborate calls were preferred when calls suffered overlap, although they were not preferred when overlap was absent. In response to increasing risk of overlap in larger choruses, males increased call elaboration. However, males overwhelmingly produced two-chuck calls in even the largest choruses, despite our results suggesting that additional chucks would more effectively safeguard calls. Furthermore, aspects of male phenotypes predicted to limit call elaboration had negligible or uncertain effects, suggesting that other constraints are operating. These results highlight how complex interrelations among signal form, signaling interactions, and the social environment shape the evolution of communication in social species.

Anisogamy Does Not Always Promote the Evolution of Mating Competition Traits in Males.

AbstractAnisogamy has evolved in most sexually reproducing multicellular organisms allowing the definition of male and female sexes, producing small and large gametes. Anisogamy, as the initial sexual dimorphism, is a good starting point to understand the evolution of further sexual dimorphisms. For instance, it is generally accepted that anisogamy sets the stage for more intense mating competition in males than in females. We argue that this idea stems from a restrictive assumption on the conditions under which anisogamy evolved in the first place: the absence of sperm limitation (assuming that all female gametes are fertilized). Here, we relax this assumption and present a model that considers the coevolution of gamete size with a mating competition trait, starting in a population without dimorphism. We vary gamete density to produce different scenarios of gamete limitation. We show that while at high gamete density the evolution of anisogamy always results in male investment in competition, gamete limitation at intermediate gamete densities allows for either females or males to invest more into mating competition. Our results thus suggest that anisogamy does not always promote mating competition among males. The conditions under which anisogamy evolves matter, as does the competition trait.