Teleogryllus Oceanicus Research Articles

Sex differences in nutrient intake can reduce the potential for sexual conflict over fitness maximization by female and male crickets.

As females and males have different roles in reproduction, they are expected to require different nutrients for the expression of reproductive traits. However, due to their shared genome, both sexes may be constrained in the regulation of nutrient intake that maximizes sex-specific fitness. Here, we used the Geometric Framework for nutrition to examine the effect of macronutrient and micronutrient intakes on lifespan, fecundity and cuticular hydrocarbons (CHCs) that signal mate quality to prospective mates in female field crickets, Teleogryllus oceanicus. In addition, we contrasted nutritional effects on life-history traits between males and females to determine how sex differences influence nutrient regulation. We found that carbohydrate intake maximized female lifespan and protein intake influenced CHC expression, while early life fecundity (cumulative fecundity at day 21) and lifetime fecundity were dependent on both macronutrient and micronutrient intakes. Fecundity required different nutrient blends to those required to optimize sperm viability in males, generating the potential for sexual conflict over macronutrient intake. The regulation of protein (P) and carbohydrate (C) intakes by virgin and mated females initially matched that of males, but females adjusted their intake to a higher P:C ratio, 1P:2C, that maximized fecundity as they aged. This suggests that a sex-specific, age-dependent change in intake target for sexually mature females, regardless of their mating status, adjusts protein consumption in preparation for oviposition. Sex differences in the regulation of nutrient intake to optimize critical reproductive traits in female and male T.oceanicus provide an example of how sexual conflict over nutrition can shape differences in foraging between the sexes.

Nongenetic paternal effects via seminal fluid.

Mounting evidence suggests that nongenetic paternal effects on offspring may be widespread among animal taxa, but the mechanisms underlying this form of nongenetic inheritance are not yet fully understood. Here, we show that seminal fluids underlie paternal effects on early offspring survival in an insect, the cricket Teleogryllus oceanicus, and quantify the contribution of this paternal effect to the inheritance of this important fitness trait. We used castrated males within a full‐sib half‐sib experimental design to show that seminal fluid donors were responsible for variation in the survival of developing embryos to hatching, and in their subsequent survival to adulthood. Increased expression of two seminal fluid protein genes, previously found to be positively associated with sperm quality, was found to be negatively associated with embryo survival. These nongenetic paternal effects hold important implications for the evolution of adaptive maternal responses to sperm competition, and more broadly for the interpretation of sire effects from classic quantitative genetic breeding designs.

When Does Sexual Signal Exploitation Lead to Signal Loss?

Evolutionary loss of traits is common over evolutionary time and occurs in diverse taxa. Sexual signals and other non-signal traits should differ in their likelihood of becoming lost because they experience different selective pressures contributing to their diminution or persistence. In particular, conspicuous sexual signals are often exploited by natural enemies; this significant cost can favor signal reduction or loss. Yet sexual signals should also experience strong selection favoring their persistence because they facilitate communication during sexual encounters and their loss would involve changes in both the signaler and receiver. Most examples of sexual signal loss come from phylogenetic studies, so it is difficult to ascertain the context and key factors responsible for their loss. Here, we describe one of the best documented examples of evolutionary sexual signal loss in real time due to signal exploitation: Teleogryllus oceanicus (the Pacific field cricket) in Hawaii where many males have lost the ability to sing due to natural selection from a deadly, acoustically-orienting parasitoid fly. Using sexual signal loss in T. oceanicus as a model, we identify environmental, social, and genetic factors that appear generally important in driving sexual signal loss due to signal exploitation. We also discuss each putative factor contributing to signal loss more broadly within the context of non-signal trait loss. Overall, the factors that facilitate evolutionary loss of signals and other traits exhibit significant parallels. In general, a significant cost from the environment, weak selection for persistence, and alternative ways of accomplishing the former function appear critical to achieving evolutionary loss of both sexual signals and non-signal traits. However, because few empirical examples of sexual signal loss over contemporary timescales exist, we need more theory and empirical work to better understand the evolutionary dynamics of sexual signal loss.

Protein and carbohydrate intakes alter gut microbial community structure in crickets: a Geometric Framework approach.

Proteins and carbohydrates have profound impacts on the ecology of gut microbiota, but disentangling the single and interactive effects of different dietary constituents is challenging. Here, we used a multidimensional approach, the Geometric Framework, to study the interactions between nutrition and bacterial abundances with respect to protein and carbohydrate intakes in field cricket, Teleogryllus oceanicus. Our study revealed that species richness decreased as crickets consumed more macronutrients, and species evenness peaked at high intake of protein-rich diets. Sex and protein:carbohydrate (P:C) ratios in diets were the primary factors influencing the gut bacterial community, but most of the microbial operational taxonomic units (OTUs) that were significantly different between males and females were present in low abundance. In contrast, protein intake had a greater influence than carbohydrate consumption on the relative abundances of the core bacterial taxa, as an increase in dietary protein availability could remove the growth constraint imposed by limited nitrogen. Taken together, the use of the Geometric Framework provides a deeper insight into how nutritional intakes influence the relative abundances of gut microbes, and could be a useful tool to integrate the study of gut microbiome and fitness traits in a host.

Obligately silent males sire more offspring than singers in a rapidly evolving cricket population.

How sexual traits are gained and lost in the wild remains an important question in evolutionary biology. Pacific field crickets (Teleogryllus oceanicus) in Hawaii provide an unprecedented opportunity to investigate the factors facilitating evolutionary loss of a sexual signal in real time. Natural selection from an acoustically orienting parasitoid fly drove rapid evolution of a novel, silent male morph. While silent (flatwing) males enjoy protection from the fly, they face difficulty attracting mates. We tested how offspring production varies in association with three male attributes affected by the spread of flatwing: wing morph (flatwing or normal-wing), age (flatwings should survive longer than singers) and exposure to calling song during rearing (wild populations with many flatwings lack ambient calling song). Per mating event, flatwings sired more offspring than singers and older males were mounted more quickly by females when presented with standard courtship song. Despite prior work showing that male age and acoustic experience influence sperm characteristics associated with fertilization, age and song exposure had no influence on male offspring production per mating. This represents the first evidence that the silent male morph possesses a reproductive advantage that may help compensate for precopulatory barriers to mate attraction.

Sexual signal loss in field crickets maintained despite strong sexual selection favoring singing males.

Evolutionary biologists commonly seek explanations for how selection drives the emergence of novel traits. Although trait loss is also predicted to occur frequently, few contemporary examples exist. In Hawaii, the Pacific field cricket (Teleogryllus oceanicus) is undergoing adaptive sexual signal loss due to natural selection imposed by eavesdropping parasitoids. Mutant male crickets ("flatwings") cannot sing. We measured the intensity of sexual selection on wing phenotype in a wild population. First, we surveyed the relative abundance of flatwings and "normal-wings" (nonmutants) on Oahu. Then, we bred wild-mated females' offspring to determine both female genotype with respect to the flatwing mutation and the proportion of flatwing males that sired their offspring. We found evidence of strong sexual selection favoring the production of song: females were predominantly homozygous normal-wing, their offspring were sired disproportionately by singing males, and at the population level, flatwing males became less common following a single sexual selection event. We report a selection coefficient describing the total (pre- and postcopulatory) sexual selection favoring normal-wing males in nature. Given the maintenance of the flatwing phenotype in Hawaii in recent years, this substantial sexual selection additionally suggests an approximate strength of opposing natural selection that favors silent males.

Natural and sexual selection on cuticular hydrocarbons: a quantitative genetic analysis.

While the reproductive benefits of sexual displays have been widely studied, we have relatively limited evidence of the fitness costs associated with most display traits. Insect cuticular hydrocarbon (CHC) profiles are sexually selected traits that also protect against desiccation. These two functions are thought to oppose each other, with investment in particular compounds believed to increase attractiveness at the expense of compounds that protect against water loss. We investigated this potential trade-off in a quantitative genetic framework using the Australian field cricket, Teleogryllus oceanicus. Several compounds were significantly genetically correlated with either attractiveness or desiccation resistance. Of these compounds, one was negatively genetically correlated with attractiveness but positively genetically correlated with desiccation resistance. Furthermore, scoring each individual's overall CHC profile for its level of attractiveness and desiccation resistance indicated a negative genetic correlation between these multivariate phenotypes. Together, our results provide evidence for a genetic trade-off between sexually and naturally selected functions of the CHC profile. We suggest that the production of an attractive CHC profile may be costly for males, but highlight the need for further work to support this finding experimentally. Genetic covariation between the CHC profile and attractiveness suggests that females can gain attractive sons through female choice.

A silent orchestra: convergent song loss in Hawaiian crickets is repeated, morphologically varied, and widespread.

Host-parasite interactions are predicted to drive the evolution of defences and counter-defences, but the ability of either partner to adapt depends on new and advantageous traits arising. The loss of male song in Hawaiian field crickets (Teleogryllus oceanicus) subject to fatal parasitism by eavesdropping flies (Ormia ochracea) is a textbook example of rapid evolution in one such arms race. Male crickets ordinarily sing to attract females by rubbing their forewings together, which produces sound by exciting acoustic resonating structures formed from modified wing veins (‘normal-wing’). The resulting song is the target of strong sexual selection by conspecific females. However, male song also attracts female flies that squirt larvae onto males or nearby female crickets; the larvae then burrow into, consume, and ultimately kill the host. The flies thus impose strong natural selection on male song, producing silent males, which have spread rapidly in populations on two islands – Kauai and Oahu. On both islands, song loss is caused by genetic mutations that drastically reduce or eliminate sound-producing structures on the male forewing by feminising wing venation – these males are called ‘flatwing’. On recent visits to parasitized cricket populations, we discovered two additional wing phenotypes – ‘small-wing’ and ‘curly-wing’. These two phenotypes differ noticeably from flatwing, and from each other, but all have the effect of eliminating or reducing acoustic signals that attract the parasitoid fly. These discoveries illustrate how the evolutionary process can repeatedly, and through a remarkable variety of independent mechanisms, drive adaptation to the same selection pressure.

Sex-specific pace-of-life syndromes

Abstract The pace-of-life syndrome (POLS) hypothesis considers an animal’s behavior, physiology, and life history as nonindependent components of a single integrated phenotype. However, frequent deviations from the expected correlations between POLS traits suggest that these relationships may be context, and potentially, sex dependent. To determine whether the sexes express distinct POLS trait covariance structures, we observed the behavior (mobility, latency to emerge from a shelter), physiology (mass-specific metabolic rate), and life history (life span, development time) of male and female Australian field crickets (Teleogryllus oceanicus). Path analysis modeling suggested that POLS trait covariation differed between the sexes. Although neither sex displayed the complete integration of traits predicted by the POLS hypothesis, females did display greater overall integration with a significant negative correlation between metabolic rate and risk-taking behavior but with life-history traits varying independently. In males, however, there was no clear association between traits. These results suggest that T. oceanicus do indeed display sex-specific trait covariance structures, emphasizing the importance of acknowledging sex in assessments of POLS.

Release from intralocus sexual conflict? Evolved loss of a male sexual trait demasculinizes female gene expression.

The loss of sexual ornaments is observed across taxa, and pleiotropic effects of such losses provide an opportunity to gain insight into underlying dynamics of sex-biased gene expression and intralocus sexual conflict (IASC). We investigated this in a Hawaiian field cricket, Teleogryllus oceanicus, in which an X-linked genotype ( flatwing) feminizes males' wings and eliminates their ability to produce sexually selected songs. We profiled adult gene expression across somatic and reproductive tissues of both sexes. Despite the feminizing effect of flatwing on male wings, we found no evidence of feminized gene expression in males. Instead, female transcriptomes were more strongly affected by flatwing than males', and exhibited demasculinized gene expression. These findings are consistent with a relaxation of IASC constraining female gene expression through loss of a male sexual ornament. In a follow-up experiment, we found reduced testes mass in flatwing males, whereas female carriers showed no reduction in egg production. By contrast, female carriers exhibited greater measures of body condition. Our results suggest sex-limited phenotypic expression offers only partial resolution to IASC, owing to pleiotropic effects of the loci involved. Benefits conferred by release from intralocus conflict could help explain widespread loss of sexual ornaments across taxa.

Testing the role of trait reversal in evolutionary diversification using song loss in wild crickets

The mechanisms underlying rapid macroevolution are controversial. One largely untested hypothesis that could inform this debate is that evolutionary reversals might release variation in vestigial traits, which then facilitates subsequent diversification. We evaluated this idea by testing key predictions about vestigial traits arising from sexual trait reversal in wild field crickets. In Hawaiian Teleogryllus oceanicus, the recent genetic loss of sound-producing and -amplifying structures on male wings eliminates their acoustic signals. Silence protects these "flatwing" males from an acoustically orienting parasitoid and appears to have evolved independently more than once. Here, we report that flatwing males show enhanced variation in vestigial resonator morphology under varied genetic backgrounds. Using laser Doppler vibrometry, we found that these vestigial sound-producing wing features resonate at highly variable acoustic frequencies well outside the normal range for this species. These results satisfy two important criteria for a mechanism driving rapid evolutionary diversification: Sexual signal loss was accompanied by a release of vestigial morphological variants, and these could facilitate the rapid evolution of novel signal values. Widespread secondary trait losses have been inferred from fossil and phylogenetic evidence across numerous taxa, and our results suggest that such reversals could play a role in shaping historical patterns of diversification.

Life history consequences of developing in anthropogenic noise.

When environments change rapidly, adaptive phenotypic plasticity can ameliorate negative effects of environmental change on survival and reproduction. Recent evidence suggests, however, that plastic responses to human-induced environmental change are often maladaptive or insufficient to overcome novel selection pressures. Anthropogenic noise is a ubiquitous and expanding disturbance with demonstrated effects on fitness-related traits of animals like stress responses, foraging, vigilance, and pairing success. Elucidating the lifetime fitness effects of noise has been challenging because longer-lived vertebrate systems are typically studied in this context. Here, we follow noise-stressed invertebrates throughout their lives, assessing a comprehensive suite of life history traits, and ultimately, lifetime number of surviving offspring. We reared field crickets, Teleogryllus oceanicus, in masking traffic noise, traffic noise from which we removed frequencies that spectrally overlap with the crickets' mate location song and peak hearing (nonmasking), or silence. We found that exposure to masking noise delayed maturity and reduced adult lifespan; crickets exposed to masking noise spent 23% more time in juvenile stages and 13% less time as reproductive adults than those exposed to no traffic noise. Chronic lifetime exposure to noise, however, did not affect lifetime reproductive output (number of eggs or surviving offspring), perhaps because mating provided females a substantial longevity benefit. Nevertheless, these results are concerning as they highlight multiple ways in which traffic noise may reduce invertebrate fitness. We encourage researchers to consider effects of anthropogenic disturbance on growth, survival, and reproductive traits simultaneously because changes in these traits may amplify or nullify one another.

Female cuticular hydrocarbons can signal indirect fecundity benefits in an insect.

Male choosiness of prospective female mating partners provides an increasingly recognized pathway through which males can increase their fitness. For example, males may increase their number of offspring by targeting more fecund females as mating partners. If fecundity is heritable, males that mate with more fecund females can also receive the indirect benefit of more fecund daughters. In species where female fecundity is not directly assessable, female ornaments may act as signals of fecundity. However, whether female ornaments reliably signal the indirect benefit of more fecund daughters is not well understood. We investigated this question using the field cricket, Teleogryllus oceanicus. Previous work had identified the cuticular hydrocarbon (CHC) profile as a female sexual display trait in T. oceanicus. To examine whether CHCs can provide a reliable signal of fecundity, we tested whether individual CHC compounds and the first principal axis of CHC variation (PC1) are genetically correlated with ovary mass, a reliable proxy for fecundity in this species. We found significant genetic correlations between ovary mass and three individual CHC compounds, as well as PC1. This result indicates that by targeting females as mating partners based on their CHC profile, males can sire more fecund daughters.

Social cues affect quantitative genetic variation and covariation in animal personality traits.

The social environment is expected to have substantial effects on behavior, and as a consequence, its heritability and evolvability. We investigated these effects by exposing Australian field crickets (Teleogryllus oceanicus) to either silence or recordings of male acoustic sexual signals. We used a combined pedigree and full-sib/half-sib breeding design to estimate the repeatability, heritability, and evolvability of behaviors related to boldness, exploration, and activity. All behaviors measured were significantly repeatable in both social environments. Additionally, most behaviors showed significant heritabilities in the two environments. We found no difference in repeatabilities between the silent and the acoustic environment but did find significant differences in the heritabilities and evolvabilities between these environments. There was a high degree of similarity between the phenotypic covariance matrices across the two environments, while the genotypic covariance matrices were highly dissimilar. Reflecting this, we found significant genotype-by-environment interactions for most of the behaviors. Lastly, we found that the repeatable aspect of behavior ("personality") was significantly heritable for most behaviors, but that these heritabilities were higher in the acoustic than in the silent environment. We conclude that the social environment can have a significant impact on the heritability and evolvability of behavior, and argue that evolutionary inferences from phenotypic studies should be made with caution.

Behavioural mechanisms of sexual isolation involving multiple modalities and their inheritance.

Speciation research dissects the genetics and evolution of reproductive barriers between parental species. Hybrids are the "gatekeepers" of gene flow, so it is also important to understand the behavioural mechanisms and genetics of any potential isolation from their parental species. We tested the role of multiple behavioural barriers in reproductive isolation among closely related field crickets and their hybrids (Teleogryllus oceanicus and Teleogryllus commodus). These species hybridize in the laboratory, but the behaviour of hybrids is unusual and there is little evidence for gene flow in the wild. We found that heterospecific pairs exhibited reduced rates of courtship behaviour due to discrimination by both sexes, and that this behavioural isolation was symmetrical. However, hybrids were not sexually selected against and exhibited high rates of courtship behaviour even though hybrid females are sterile. Using reciprocal hybrid crosses, we characterized patterns of interspecific divergence and inheritance in key sexual traits that might underlie the mating patterns we found: calling song, courtship song and cuticular hydrocarbons (CHCs). Song traits exhibited both sex linkage and transgressive segregation, whereas CHCs exhibited only the latter. Calculations of the strength of isolation exerted by these sexual traits suggest that close-range signals are as important as long-distance signals in contributing to interspecific sexual isolation. The surprisingly weak mating barriers observed between hybrids and parental species highlight the need to examine reproductive isolating mechanisms and their genetic bases across different potential stages of introgressive hybridization.

When virginity matters: age and mating status affect female responsiveness in crickets

Behavioural assays in which animals recognize, localize or discriminate among signals are broadly useful for answering an array of biological questions, but results can be sensitive to the characteristics of individuals, including age and mating status. Researchers may prefer to use young, unmated individuals in experiments both to control for the effects of mating and because younger and unmated individuals may respond more often or more quickly. In natural contexts, virgin females are likely to behave differently than mated females, especially in animals that store sperm for future use, because the costs and benefits of mating are different for these two groups. In species in which multiple mating is common, individuals are much more likely to have mated at least once at the time of any given mating event than they are to be virgins, suggesting the use of virgin subjects in experiments is not reflective of most natural mating decisions. We conducted a literature review to sample the methods employed in empirical studies that use crickets in phonotaxis assays. Many studies draw conclusions based only on virgins, and methods vary widely with respect to the age of individual subjects. We then conducted an empirical study of the effect of mating status and age on female phonotaxis behaviour in Teleogryllus oceanicus, the Pacific field cricket. Our results show that both age and mating status affect some commonly used measures of female responsiveness in phonotaxis assays: older females begin moving more quickly in phonotaxis tests, while virgins have shorter response latencies. These findings are consistent with the idea that the cost of remaining unmated increases with age, and that virgin females benefit from an initial mating more than mated females benefit from additional matings.

Purring Crickets: The Evolution of a Novel Sexual Signal.

Opportunities to observe contemporary signal change are incredibly rare but critical for understanding how diversity is created and maintained. We discovered a population of the Pacific field cricket (Teleogryllus oceanicus) with a newly evolved song (purring), different from any known cricket. Male crickets use song to attract females from afar and to court females once near. Teleogryllus oceanicus is well known for sexual signal evolution, as exemplified by a recent signal loss. In this study, we characterized the new purring sound and investigated the role of the purr in long-distance and short-distance communication. The purring sound differed from typical ancestral calls in peak frequency, amplitude, and bandwidth. Further, the long-distance purring song facilitated mate location, though the role of courtship purring song is less clear. Our discovery of purring male crickets is an unprecedented opportunity to watch the emergence of a newly evolved sexual signal unfold in real time and has potential to illuminate the mechanisms by which evolutionary novelties arise and coevolve between the sexes.

Obligate, but not facultative, satellite males prefer the same male sexual signal characteristics as females

Signalling is energetically expensive and increases the risk of predation and parasite infection. To balance the costs and benefits of mate attraction, individuals may adopt an alternative mating strategy such as satellite behaviour, in which nonsignalling males will settle near signalling males and attempt to intercept approaching females. While many suggest that alternative strategies are ‘making the best of a bad job’, little research has examined whether satellites, particularly obligate satellites, have the potential to increase their mating success by preferentially targeting more attractive signallers. Using the Pacific field cricket, Teleogryllus oceanicus, we tested the hypothesis that males are more likely to act as satellites to signalling males with particularly attractive songs, as these callers are likely to attract the most females. In this species, a novel male wing mutation, ‘flatwing’, renders some males unable to call. Flatwings are obligate satellites, while nonmutated, normal-wing males switch between calling and satellite strategies. We presented males with calling song models varying in the percentage of long-to-short chirps, a characteristic important in female choice. As was shown for females in previous work, flatwings exhibited a strong preference for calling songs composed of 60% long chirp. Normal wing males did not prefer any particular calling song model. Our results lead to the paradoxical conclusion that males with highly attractive songs may not have the highest mating success. Such male preference for male sexual signals may oppose selection by females and increase competition between signalling and satellite males. This could potentially slow the rate of male trait evolution and influence the evolution of male competition.

Is it the Song or the Singers? Acoustic and Social Experiences Shape Adult Reproductive Tactics and Condition

When sexual signals are perceived during growth and development they can provide information regarding the social conditions likely to be encountered as an adult. Perception of cues related to the presence and density of future mates and potential competitors can result in altered adult phenotypes. Previous studies have shown that adult male Teleogryllus oceanicus field crickets from a Kauai, Hawaii population reared alone and without hearing conspecific song are more phonotactic than those reared with song. These naive males also reduce investment in body size and immunity. Here we examined whether another source of population density information, the presence of other males, affects behavior, size, and immunity. Specifically, we examined satellite behavior as evidenced by strength of phonotaxis, body condition, and immune response in males reared singly and in groups in the presence and absence of conspecific song. Body condition did not vary with rearing density, and immune response did not vary with either acoustic environment or rearing density. Interestingly, group-housed males were more phonotactic than singly-housed males. This pattern was largely driven by the low levels of phonotaxis exhibited by males that were singly-housed in the presence of conspecific song. These findings suggest that males respond to social cues in addition to conspecific song, but that these cues do not necessarily provide concordant information.

State-dependent changes in risk-taking behaviour as a result of age and residual reproductive value

Animals are able to modify their behaviour in response to changes in their internal and environmental state. The asset protection principle predicts that an animal's risk-taking behaviour should vary as a result of its residual reproductive value (RRV); animals with greater RRV would incur a greater cost if injured or killed and should therefore take fewer risks than those with low RRV. Despite the intuitive appeal of this hypothesis, few studies have effectively separated the effects of RRV on behaviour from those of age. We addressed this weakness in the widely invoked hypothesis by measuring the risk-taking behaviour of female Australian field crickets, Teleogryllus oceanicus, at various points in the animal's lifetime. We found significant effects of age on risk-taking behaviour: older females emerged from a shelter sooner after a simulated predation threat and exhibited greater mobility in an open arena. Importantly, there was also a significant marginal effect of RRV on risk-taking behaviour. Females with lower RRV displayed greater levels of risk taking than females with high RRV. Our results thereby offer support for the asset protection principle as an explanation for state-dependent variation in risk-taking behaviour.