Mating Signals Research Articles

Developmental transcriptomics of Chinese cordyceps reveals gene regulatory network and expression profiles of sexual development-related genes

BackgroundChinese cordyceps, also known as Chinese caterpillar fungus (Ophiocordyceps sinensis, syn. Cordyceps sinensis), is of particular interest for its cryptic life cycle and economic and ecological importance. The large-scale artificial cultivation was succeeded recently after several decades of efforts and attempts. However, the induction of primordium, sexual development of O. sinensis and the molecular basis of its lifestyle still remain cryptic.ResultsThe developmental transcriptomes were analyzed for six stages covering the whole developmental process, including hyphae (HY), sclerotium (ST), primordium (PR), young fruiting body (YF), developed fruiting body (DF) and mature fruiting body (MF), with a focus on the expression of sexual development-related genes. Principal component analysis revealed that the gene expression profiles at the stages of primordium formation and fruiting body development are more similar than those of the undifferentiated HY stage. The PR and MF stages grouped together, suggesting that primordium differentiation and sexual maturation have similar expression patterns. Many more DEGs were identified between the ST and HY stages, covering 47.5% of the O. sinensis genome, followed by the comparisons between the ST and PR stages. Using pairwise comparisons and weighted gene coexpression network analysis, modules of coexpressed genes and candidate hub genes for each developmental stage were identified. The four mating type loci genes expressed during primordium differentiation and sexual maturation; however, spatiotemporal specificity of gene expression indicated that they also expressed during the anamorphic HY stage. The four mating type genes were not coordinately expressed, suggesting they may have divergent roles. The expression of the four mating type genes was highest in the fertile part and lowest in the sclerotium of the MF stage, indicating that there is tissue specificity. Half of genes related to mating signaling showed as the highest expression in the ST stage, indicating fruiting was initiated in the ST stage.ConclusionsThese results provide a new perspective to understanding of the key pathways and hub genes, and sexual development-related gene profile in the development of Chinese cordyceps. It will be helpful for underlying sexual reproduction, and add new information to existing models of fruiting body development in edible fungi.

Toward Testing for Multimodal Perception of Mating Signals

Many mating signals consist of multimodal components that need decoding by several sensory modalities on the receiver’s side. For methodological and conceptual reasons, the communicative functions of these signals are often investigated only one at a time. Likewise, variation of single signal traits are frequently correlated by researchers with senders’ quality or receivers’ behavioural responses. Consequently, the two classic and still dominating hypotheses regarding the communicative meaning of multimodal mating signals postulate that different components either serve as back-up messages or provide multiple meanings. Here we discuss how this conceptual dichotomy might have hampered a more integrative, perception encompassing understanding of multimodal communication: neither the multiple message nor the back-up signal hypotheses address the possibility that multimodal signals are integrated neurally into one percept. Therefore when studying multimodal mating signals, we should be aware that multimodal signals can give rise to multimodal percepts, meaning that receivers can gain access to additional information inherent to only combined signal components (‘the whole is something different than the sum of its parts’). We review the evidence for the importance of multimodal percepts and outline potential avenues for discovery of multimodal percepts in animal communication.

Environmental heterogeneity alters mate choice behavior for multimodal signals

Animals frequently experience changes in their environment, including diel and seasonal shifts in abiotic and biotic factors. In addition to physiological and morphological changes, animals alter their behavior in response to environmental variation. This study examined the impacts of heterogeneous environments on mating behaviors. We examined both male and female tungara frog phonotactic responses to multimodal (audiovisual) and unimodal (acoustic) stimuli. We altered aspects of the physical environment by changing substrate (terrestrial and aquatic) and ambient light levels. Females demonstrated a similar preference for the audiovisual stimulus regardless of substrate but decreased latency to choose in an aquatic environment. When ambient light levels were increased (relative to darker control), females reversed their preference, avoiding the multimodal stimulus, but the latency to choose was unchanged. Males demonstrated no preference for the multimodal signal on either substrate, but like females, male latency was reduced in an aquatic environment. Different environments carry their own associated costs, including varying levels of predation risk. Increased light levels and an aquatic environment likely carry higher predation risk and therefore should lead to changes in female and male responses. Interestingly, these two environments do not cause uniform changes in female responses. The addition of an aquatic environment led to a reduction in latency, whereas an increase in ambient light levels induced a change in female mate preference. These findings demonstrate the importance of the environment on mating responses to multimodal signals. Responses to conspecific mating signals (e.g., mate preferences) have often been assumed to be static. In this study, we tested responses of both male and female tungara frogs to a multimodal (visual + vocal) advertisement signal under varying environmental conditions. Elevated light levels changed female responses to mating signals. When both sexes were required to swim, rather than walk to a signal, their choices did not change. They did respond faster, however. These results indicate that measuring the strength of sexual selection should be considered as a function of both innate preferences and the environmental conditions experienced by the animals.

Within-population variability in a moth sex pheromone blend, part 2: selection towards fixation

To understand how variation in sexual communication systems evolves, the genetic architecture underlying sexual signals and responses needs to be identified. Especially in animals where mating signals are important for mate recognition, and signals and responses are governed by independently assorting genes, it is difficult to envision how signals and preferences can (co)evolve. Moths are a prime example of such animals. In the noctuid moth Heliothis virescens, we found within-population variation in the female pheromone. In previous selection experiments followed by quantitative trait locus (QTL) analysis and expression analysis of candidate desaturase genes, we developed a model involving a trans-acting repressor of the delta-11-desaturase. In our current study with new selection lines, we fixed the most extreme phenotype and found a single underlying mutation: a premature stop codon in the first coding exon of delta-11-desaturase, which we could trace back to its origin in the laboratory. Interestingly, we found no pleiotropic effects of this knock-out mutation on the male physiological or behavioural response, or on growth or fertility. This finding is in contrast to Drosophila melanogaster, where a single desaturase gene affects both female pheromone production and male behavioural response, but similar to other Lepidoptera where these traits are under independent genetic control. To our knowledge, this is the first time that a single point mutation has been identified that underlies the phenotypic variation in the pheromone signal of a moth.

MilR4 and milR16 Mediated Fruiting Body Development in the Medicinal Fungus Cordyceps militaris.

Cordyceps militaris readily performs sexual reproduction, thus providing a remarkably rich model for understanding the processes involved in sexual development. It could regulate expression of human genes by diet-derived miRNA-like RNAs (milRNAs). However, the study of miRNAs in C. militaris has been limited. In the present study, genes encoding Dicers, Argonautes, and RNA-dependent RNA polymerases were identified. Illumina deep sequencing was performed to characterize the milRNAs in C. militaris at asexual and sexual development stages. Total 38 milRNAs were identified and five milRNAs were validated by northern blot and qRT-PCR, out of which, 19 were specific for sexual development. Importantly, the fungi could not form fruiting bodies after disruption of milR4, while the perithecium was formed in advance after over-expression of milR4. Abnormal pale yellow fruiting body primordium, covered with abnormal primordium, was formed in the strain with miR16 disruption. Although no milR4 or milR16 target genes were identified, differential expression of many different genes involved in mycelium growth and sexual development (mating process, mating signaling, and fruiting body development) among these mutants were found. Overall, milRNAs play vital roles in sexual development in C. militaris.

Evolution of acoustic communication in European gobies (Gobius lineage) based on molecular markers

Evolution of acoustic communication in European gobies (Gobius lineage) based on molecular markers

Adaptive changes in sexual signalling in response to urbanization.

Urbanization can cause species to adjust their sexual displays, because the effectiveness of mating signals is influenced by environmental conditions. Despite many examples that show that mating signals in urban conditions differ from those in rural conditions, we do not know whether these differences provide a combined reproductive and survival benefit to the urban phenotype. Here we show that male túngara frogs have increased the conspicuousness of their calls, which is under strong sexual and natural selection by signal receivers, as an adaptive response to city life. The urban phenotype consequently attracts more females than the forest phenotype, while avoiding the costs that are imposed by eavesdropping bats and midges, which we show are rare in urban areas. Finally, we show in a translocation experiment that urban frogs can reduce risk of predation and parasitism when moved to the forest, but that forest frogs do not increase their sexual attractiveness when moved to the city. Our findings thus reveal that urbanization can rapidly drive adaptive signal change via changes in both natural and sexual selection pressures.

Elevated temperatures reduce discrimination between conspecific and heterospecific sexual signals

Heat waves are rapidly increasing in frequency and length around the globe. These periods of elevated temperatures are inducing extreme thermal stress in many organisms. One dramatic result of heat waves is mass mortality events, notably in birds. Although much attention is given to lethal events, little is known about how more common sublethal temperatures affect behaviour, especially in endotherms. For example, male song sparrows, Melospiza melodia atlantica, sing at lower rates at higher temperatures. We hypothesized that simulated heat waves may also reduce the ability of females to discriminate between sexual signals. We tested this hypothesis by quantifying whether female zebra finches, Taeniopygia guttata, responded more to conspecific song or heterospecific song while at their typical housing temperature compared to temperatures above their upper critical temperature. We collected data on how often the birds selected conspecific over heterospecific songs and how much effort the birds invested in sampling those songs using a matched-pairs design. During housing temperature trials, females preferred conspecific song compared to heterospecific song. In contrast, females no longer showed a preference for conspecific song at temperatures above their upper critical limit, although the birds invested similar effort in sampling songs in both treatments. Our findings provide the first experimental evidence that high temperatures affect female preference for a mating signal in an endotherm. Our results highlight the need for future work to investigate this overlooked effect of climate change on endotherms. Because thermoregulatory processes are phylogenetically conserved, our results generate useful predictions for future studies of heat wave effects on mating behaviours in endotherms.

The influence of mate choice motivation on non-financial altruism

Several studies have found that individuals are more altruistic towards potential mates than others, suggesting altruistic behavior may be a mating signal. Much of the literature focuses on financial altruism using economic games, however altruism can also comprise of non-financial acts, which this experiment examined in an attempt to replicate and refine previous findings. A study was conducted with 199 participants, who viewed both high attractive and low attractive opposite-sex images and were asked how likely they would be to altruistically share their research credits with the person in the image, whilst controlling for self-rated attractiveness. The findings suggest that both men and women were more altruistic towards pictures of high attractive than low attractive potential mating partners (Cohen’s d = 0.37). This study therefore partially replicates previous research examining the role of mate choice effects when exploring non-financial altruism.

Behavioral Isolation and Incipient Speciation in Birds

Behavioral changes, such as those involved in mating, foraging, and migration, can generate reproductive barriers between populations. Birds, in particular, are known for their great diversity in these behaviors, and so behavioral isolation is often proposed to be the major driver of speciation. Here, we review empirical evidence to evaluate the importance of behavioral isolation in the early stages of avian speciation. Experimentally measured mating preferences indicate that changes in mating behavior can result in premating barriers, with their strength depending on the extent of divergence in mating signals. Differences in migratory and foraging behavior also can play important roles in generating reproductive barriers in the early stages of speciation. However, because premating behavioral isolation is imperfect, extrinsic postzygotic barriers, in the form of selection against hybrids having intermediate phenotypes, also play an important role in avian diversification, especially in completing the speciation process.

Multi-modal signal evolution in birds: re-examining a standard proxy for sexual selection.

Sexual selection is proposed to be an important driver of speciation and phenotypic diversification in animal systems. However, previous phylogenetic tests have produced conflicting results, perhaps because they have focused on a single signalling modality (visual ornaments), whereas sexual selection may act on alternative signalling modalities (e.g. acoustic ornaments). Here, we compile phenotypic data from 259 avian sister species pairs to assess the relationship between visible plumage dichromatism-a standard index of sexual selection in birds-and macroevolutionary divergence in the other major avian signalling modality: song. We find evidence for a strong negative relationship between the degree of plumage dichromatism and divergence in song traits, which remains significant even when accounting for other key factors, including habitat type, ecological divergence and interspecific interactions. This negative relationship is opposite to the pattern expected by a straightforward interpretation of the sexual selection-diversification hypothesis, whereby higher levels of dichromatism indicating strong sexual selection should be related to greater levels of mating signal divergence regardless of signalling modality. Our findings imply a 'trade-off' between the elaboration of visual ornaments and the diversification of acoustic mating signals, and suggest that the effects of sexual selection on diversification can only be determined by considering multiple alternative signalling modalities.

Divergence in Potential Contact Pheromones and Genital Morphology Among Sympatric Song Types of the Bush Cricket Mecopoda elongata

A well-established route to speciation in animals is via the evolution of divergent male mating signals and female preferences within a species. However, an open question is how common it is for near complete isolation to be achieved through a single signal-receiver system or whether multiple aspects of the mate-recognition system diverge simultaneously. The five highly divergent song types of the bush cricket Mecopoda elongata, exemplify reproductive isolation in sympatry through long-distance mating signals. Female preference for their own song type has been established as a strong pre-mating reproductive barrier, but the potential existence of additional isolating mechanisms has not been investigated. We quantify divergence in cuticular lipid profiles and external genital structures between song types. These traits show significant divergence among species of Orthoptera and are known to be used in mate recognition following contact. We show that divergence among sympatric Mecopoda song types in both cuticular lipid profiles and two external genital structures is sufficiently extensive that either of them can be used to identify individual song type with 90% accuracy. Our findings suggest that multiple isolating mechanisms are likely to evolve simultaneously to facilitate a more robust reproductive isolation. This indicates a role for sexual selection in the divergence and potential future speciation of these populations and suggests that reproductive isolation may frequently evolve through simultaneous divergence across different aspects of mate recognition systems.

The roles of altruism, heroism, and physical attractiveness in female mate choice

The role of prosocial behaviour in female mate choice has been extensively explored, focusing on the desirability of altruism in potential mates, as well as altruism being a mating signal. However, little research has focused on the desirability of heroism and altruism in potential partners. Furthermore, the synergistic effect of attractiveness on the desirability of prosocial behavior has only recently been explored, and to our knowledge, has not been explored in relation to the desirability of heroism in a romantic partner. We explored the effect of prosociality and attractiveness on female desirability ratings (n = 198), and whether desirability was influenced by whether women were seeking a short-term or long-term relationship. We find that women are attracted to men who display heroism and altruism, and this preference is higher when the male is attractive compared to unattractive. Furthermore, preferences for prosocial traits were higher when seeking a long-term compared to a short-term partner. Our findings add to the literature on prosocial behaviour and matechoice. Data and materials [Open Science Framework Project A76P8].

Macrogeographic variation in song of the MacGillivray's Warbler (Geothlypis tolmiei)

ABSTRACT Geographic variation in mating signals is of interest to evolutionary biologists because the consequences of spatial divergence may lead to behavioral discrimination, assortative mating, and speciation. Birdsong is a mating signal of songbirds, and geographic variation in the form of small-scale dialects or large-scale regiolects has been documented in many species. We studied macrogeographic variation in song of the MacGillivray's Warbler (Geothlypis tolmiei) to determine the pattern of song variation in this species. Hypotheses used to explain the evolution of song divergence were also examined. We found extensive individual variation in the cultural units and physical parameters of song that overwhelmed differences among populations. We did not find dialects in the breeding range but did find a pattern of clinal variation with song differences increasing with increasing geographic distances among populations. Hypotheses that explain patterns of song divergence in other species did not apply to...

An Alternative to Adaptation by Sexual Selection: Habitat Choice

Adaptation in mating signals and preferences has generally been explained by sexual selection. We propose that adaptation in such mating traits might also arise via a non-mutually exclusive process wherein individuals preferentially disperse to habitats where they experience high mating performance. Here we explore the evolutionary implications of this process.

Call recognition and female choice in a treefrog with a multicomponent call

AbstractAcoustic mating signals are typically species‐specific, and often additionally are subject to directional female preferences. Male executioner treefrogs, Dendropsophus carnifex, produce a multicomponent advertisement call composed of an introductory screech note followed by two or more click notes. Here, we tested (i) call recognition by comparing female directed phonotaxis towards individual and combined call components: screech vs. clicks vs. screech + clicks, (ii) female preferences for greater numbers of click notes and (iii) female preferences for faster call rates. The results demonstrated that screeches and clicks, presented either separately or together as a complete call, evoke similar female responses, suggesting that either note was sufficient to elicit a mate‐recognition response. Additionally, females preferred calls with greater numbers of click notes and with faster call rates. We interpret these results within the context of female mate selection in natural choruses.

Ecological drivers of song evolution in birds: Disentangling the effects of habitat and morphology.

Environmental differences influence the evolutionary divergence of mating signals through selection acting either directly on signal transmission (“sensory drive”) or because morphological adaptation to different foraging niches causes divergence in “magic traits” associated with signal production, thus indirectly driving signal evolution. Sensory drive and magic traits both contribute to variation in signal structure, yet we have limited understanding of the relative role of these direct and indirect processes during signal evolution. Using phylogenetic analyses across 276 species of ovenbirds (Aves: Furnariidae), we compared the extent to which song evolution was related to the direct influence of habitat characteristics and the indirect effect of body size and beak size, two potential magic traits in birds. We find that indirect ecological selection, via diversification in putative magic traits, explains variation in temporal, spectral, and performance features of song. Body size influences song frequency, whereas beak size limits temporal and performance components of song. In comparison, direct ecological selection has weaker and more limited effects on song structure. Our results illustrate the importance of considering multiple deterministic processes in the evolution of mating signals.

Selfishness is attributed to men who help young women: Signaling function of male altruism

To investigate the function of altruism as a mating signal especially among males, the present study examined whether the motivation of a man who behaves altruistically toward a woman is more likely to be perceived as selfish by a third party. In two studies, participants read vignettes about one person helping a stranger, after which they rated the helpers’ perceived selfish motivation. We manipulated the sex of the recipient and helper (Study 1) and the recipient’s age (young vs. old; Study 2). In both studies, a man who helped a young woman was regarded as having a more selfish motivation than was an individual who helped the same sex. Conversely, although a woman who helped a man was viewed as more selfish than was a woman who helped another woman, the effect was smaller than when the helper was male (Study 1). Furthermore, a man who helped an old woman was not regarded as more selfish than was a man who helped another man (Study 2). These results support the notion that male altruism works as a courtship display.

Heterospecific mating between distantly related species of stink bugs and its evolutionary implications

ABSTRACTThe copulatory process in animals is preceded by a series of integrated communication processes which are often under selection to guarantee species-specific courtship and copula. However, individuals of species supposedly in reproductive isolation frequently copulate in nature, which has sparked the attention of evolutionary biologists for decades. While studies on this topic have strongly focused on recently diverged species or populations, few instances of heterospecific copula between distantly related species are known. Here we report an intriguing case of interspecific copula between two distantly related species of stink bugs in nature. We replicated this observation in laboratory conditions and revealed an asymmetric relation: males of Chinavia obstinata copulated with females of C. erythrocnemis but the reverse combination did not occur. We propose a series of hypotheses to explain our observations in the light of the current knowledge on mate recognition and reproductive isolation in stink bugs, considering the potential pre- and postcopulatory barriers involved. Once these two species have probably evolved in allopatry and contacted secondarily, the absence of directional selection against mating signals differentiation is a probable process. We argue that similarities in genital shape and size, most likely a result of convergent evolution, may have played a fundamental role in guaranteeing that these species achieved proper coupling.

The effect of temperature on male mating signals and female choice in the red mason bee, Osmia bicornis (L.).

Climate change and the resulting changes in air temperature are known to have a major influence on most animals, especially poikilothermic insects, because they depend on the high enough temperatures to function. Previous studies have shown that various signals can be affected by changes in temperature. However, research into the effect of temperature on mating signals and subsequently communication between mates and on female choice is still rare. In the red mason bee, Osmia bicornis, which emerges early in spring and is therefore subject to extensive temperature changes, females choose suitable males based on, among other criteria, their thorax vibrations and odor. So far there has been no research into the effect of temperature changes on these signals. We therefore investigated whether the environmental temperature has an influence on the male's mating signals by measuring vibrations using a laser vibrometer and collecting male and female odor at different temperatures. Furthermore, we performed behavioral experiments in order to show whether there is an effect of temperature‐induced changes and female choice. Our results showed that rejected males differed in their vibrations between the two temperature settings but accepted ones did not. Temperature changes therefore seem to have a stronger effect on those males that are rejected by the females, whereas the accepted males are the ones that can produce desirable signals despite temperature fluctuations. Furthermore, we found that the differences in odor profiles were greater between temperature settings than between the sexes and that females change their preference for odor with temperature. We conclude that temperature strongly influences the male mating signals and therefore may have a major impact on sexual selection in this species. This is an important aspect to consider, not only in future studies on mating behavior, but also in view of our ever raising temperatures.