Meta-analytical evidence that males prefer virgin females.

Males are often predicted to prefer virgin over non-virgin females because of the reduced risk of sperm competition. Does this prediction hold across studies? Our systematic meta-analysis of 138 studies, mainly conducted in invertebrates, confirms that males generally prefer virgin females. However, males preferred virgin females even in species with last male sperm precedence, suggesting that sperm competition alone does not drive male preferences. Furthermore, our results suggest that males may reject mated females even when no alternative exists. Preference for virgins is unlikely to influence female reproductive success since virginity cannot be selected for, but strong preference for virgin females could swamp or reinforce selection on other traits. Our results add to growing evidence that males are not indiscriminate in mating. However, given the unexplained heterogeneity in effect sizes, we urge caution in assuming that males will prefer virgins and recommend considering the natural context of mating decisions.

Rethinking same-sex sexual behaviour: male field crickets have broad mating filters.

Same-sex sexual behaviour (SSB) occurs in many animals and is often treated as an anomaly requiring special explanation. One common explanation for SSB is mistaken identity. However, animals make similar 'mistakes' in other contexts-such as attempting to mate with immature individuals or inanimate objects. Framing such behaviours as 'mistakes' risks misinterpreting how animals make flexible mating decisions. Here we make a case for an alternative approach to thinking about SSB by instead considering an individual's mating filter. A broad filter means directing courtship toward anything that resembles a potential mate, whilst a narrow filter means only courting with receptive targets. We illustrate this approach by examining the mating filters of male Pacific field crickets (Teleogryllus oceanicus). We find that males engage in SSB but also misdirect courtship toward juveniles (but not plastic crickets). This finding suggests that SSB is not an anomaly and is better considered alongside other misdirected behaviours. We argue that by viewing misdirected behaviours through the lens of mating filters rather than as 'mistakes' we can build a more nuanced understanding of reproductive behaviour and begin to determine when having a broader mating filter can be advantageous.

Living with plague: Lessons from the Soviet Union's antiplague system.

Zoonoses, such as plague, are primarily animal diseases that spill over into human populations. While the goal of eradicating such diseases is enticing, historical experience validates abandoning eradication in favor of ecologically based control strategies (which reduce morbidity and mortality to a locally accepted risk level). During the 20th century, one of the most extensive plague-eradication efforts in recorded history was undertaken to enable large-scale changes in land use in the former Soviet Union (including vast areas of central Asia). Despite expending tremendous resources in its attempt to eradicate plague, the Soviet antiplague response gradually abandoned the goal of eradication in favor of plague control linked with developing basic knowledge of plague ecology. Drawing from this experience, we combine new gray-literature sources, historical and recent research, and fieldwork to outline best practices for the control of spillover from zoonoses while minimally disrupting wildlife ecosystems, and we briefly compare the Soviet case with that of endemic plague in the western United States. We argue for the allocation of sufficient resources to maintain ongoing local surveillance, education, and targeted control measures; to incorporate novel technologies selectively; and to use ecological research to inform developing landscape-based models for transmission interruption. We conclude that living with emergent and reemergent zoonotic diseases-switching to control-opens wider possibilities for interrupting spillover while preserving natural ecosystems, encouraging adaptation to local conditions, and using technological tools judiciously and in a cost-effective way.

Sex-specific associations between life-history traits and a novel reproductive polymorphism in the Pacific field cricket.

Associations between heritable polymorphisms and life-history traits, such as development time or reproductive investment, may play an underappreciated role in maintaining polymorphic systems. This is because selection acting on a particular morph could be bolstered or disrupted by correlated changes in life history or vice versa. In a Hawaiian population of the Pacific field cricket (Teleogryllus oceanicus), a novel mutation (flatwing) on the X-chromosome is responsible for a heritable polymorphism in male wing structure. We used laboratory cricket colonies fixed for male wing morph to investigate whether males and females bearing the flatwing or normal-wing (wild-type) allele differed in their life-history traits. We found that flatwing males developed faster and had heavier testes than normal-wings, whereas flatwing homozygous females developed slower and had lighter reproductive tissues than normal-wing homozygous females. Our results advance our understanding of the evolution of polymorphisms by demonstrating that the genetic change responsible for a reproductive polymorphism can also have consequences for fundamental life-history traits in both males and females.

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.

Direct and indirect effects of sexual signal loss on female reproduction in the Pacific field cricket (Teleogryllus oceanicus).

Sexual signal evolution may present fitness consequences for the non-signaling sex due to shared genes and altered social conditions, but this is rarely studied in natural populations. On the Hawaiian Island of Kauai, most male Teleogryllus oceanicus (Pacific field crickets) lack the ability to sing because of a novel wing mutation (flatwing) that arose and spread in <20 generations. Obligately silent flatwing males have been highly successful because they avoid detection by a deadly, acoustically-orienting parasitoid fly. Little is known about how the flatwing mutation and resulting song-less acoustic environment affects female fitness. We found that Kauai females carrying the flatwing allele invested less in reproductive tissues and experienced more instances of mating failure than normal-wing-carrying females, though total offspring production did not differ between female genotypes. Females from Oahu (HI, where the parasitoid and flatwing also occur) and Mangaia (an island in the Cook Islands which harbors neither the parasitoid nor flatwing) invested less in reproductive tissues when reared in a song-less acoustic environment. Kauai females did not exhibit this plasticity, perhaps because they have experienced nearly song-less conditions for the past ~15 years following the establishment of flatwing. We show that female T. oceanicus experience a mix of costly and beneficial effects of sexual signal loss, which should help maintain the wing polymorphism in the wild. Our results demonstrate that the non-signaling sex can experience a nuanced set of phenotypic consequences resulting from signal evolution, which can further shape dynamics of sexual signal evolution.

Host migration strategy is shaped by forms of parasite transmission and infection cost.

Most studies on the evolution of migration focus on food, mates and/or climate as factors influencing these movements, whereas negative species interactions such as predators, parasites and pathogens are often ignored. Although infection and its associated costs clearly have the potential to influence migration, thoroughly studying these interactions is challenging without a solid theoretical framework from which to develop testable predictions in natural systems. Here, we aim to understand when parasites favour the evolution of migration. We develop a general model which enables us to explore a broad range of biological conditions and to capture population and infection dynamics over both ecological and evolutionary time-scales. We show that when migration evolves depends on whether the costs of migration and infection are paid in reduced fecundity or survival. Also important are the parasite transmission mode and spatiotemporal dynamics of infection and recovery (if it occurs). Finally, we find that partial migration (where only a fraction of the population migrates) can evolve but only when parasite transmission is density-dependent. Our results highlight the critical, if overlooked, role of parasites in shaping long-distance movement patterns, and suggest that infection should be considered alongside more traditional drivers of migration in both empirical and theoretical studies.

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.

Increased socially mediated plasticity in gene expression accompanies rapid adaptive evolution.

Recent theory predicts that increased phenotypic plasticity can facilitate adaptation as traits respond to selection. When genetic adaptation alters the social environment, socially mediated plasticity could cause co-evolutionary feedback dynamics that increase adaptive potential. We tested this by asking whether neural gene expression in a recently arisen, adaptive morph of the field cricket Teleogryllus oceanicus is more responsive to the social environment than the ancestral morph. Silent males (flatwings) rapidly spread in a Hawaiian population subject to acoustically orienting parasitoids, changing the population's acoustic environment. Experimental altering crickets' acoustic environments during rearing revealed broad, plastic changes in gene expression. However, flatwing genotypes showed increased socially mediated plasticity, whereas normal-wing genotypes exhibited negligible expression plasticity. Increased plasticity in flatwing crickets suggests a coevolutionary process coupling socially flexible gene expression with the abrupt spread of flatwing. Our results support predictions that phenotypic plasticity should rapidly evolve to be more pronounced during early phases of adaptation.

Models on the Runway: How Do We Make Replicas of the World?

Models are universal in science, both as theoretical formulations of reality and as model systems, representatives of other organisms. A recent paper on how scientists view the world divides our work into the mind, the lab, and the field and suggests that models must not be conflated with reality. But in practice, these distinctions are blurred. For example, are flour beetles a model system for other insects when their natural habitat is the same as the way they live in the lab? In addition, models can become restrictive when they are viewed as archetypes, making us overgeneralize about the world and ignoring meaningful variation. The study of sexual conflict in insects illustrates some of the pitfalls of relying on Drosophila as a model system for sexual selection. Microbes can be used as models for populations and communities and are essential parts of larger biological systems. Finally, some models are not meant to replicate the world but are worlds unto themselves in which diverse possibilities can be directly observed.

Metrics matter: the effect of parasite richness, intensity and prevalence on the evolution of host migration.

Parasites have long been thought to influence the evolution of migration, but precisely determining the conditions under which this occurs by quantifying costs of infection remains a challenge. Here we developed a model that demonstrates how the metric used to describe infection (richness/diversity, prevalence or intensity) shapes the prediction of whether migration will evolve. The model shows that predictions based on minimizing richness yield opposite results compared to those based on minimizing prevalence, with migration only selected for when minimizing prevalence. Consistent with these findings, empirical studies that measure parasite diversity typically find that migrants are worse off than residents, while those measuring prevalence or intensity find the opposite. Our own empirical analysis of fish parasite data finds that migrants (of all types) have higher parasite richness than residents, but with no significant difference in either prevalence or intensity.

Sexual signal loss: The link between behaviour and rapid evolutionary dynamics in a field cricket.

Sexual signals may be acquired or lost over evolutionary time, and are tempered in their exaggeration by natural selection. In the Pacific field cricket, Teleogryllus oceanicus, a mutation ("flatwing") causing loss of the sexual signal, the song, spread in <20 generations in two of three Hawaiian islands where the crickets have been introduced. Flatwing (as well as some normal-wing) males behave as satellites, moving towards and settling near calling males to intercept phonotactic females. From 2005 to 2012, we surveyed crickets and their responses to conspecific song, noting the morph and number of males and females before and after experimental playbacks. The three Hawaiian islands consistently contained different proportions of flatwing crickets, ranging from about 90% of males on Kauai to 50% on Oahu to rare on the Big Island of Hawaii. Flatwing and normal-wing males do not appear to differ in responsiveness to playback, a behaviour that should influence the likelihood of a male encountering a phonotactic female. Instead, male and female crickets from populations in which little to no calling song is perceptible during development tended to seek out callers more readily than crickets that developed in noisier environments. Such increased phonotaxis makes females more likely to find either the caller to which they are responding or to encounter a flatwing (or normal male satellite) that has also been attracted to the song. Our evidence suggests that pre-existing behavioural plasticity (manifest as flexible responses to social-particularly acoustic-information in the environment) is associated with the rapid spread of the flatwing trait. Different social environments select for differential success of flatwing or normal-wing males, which in turn alters the social environment itself.

Temperate Assumptions: How Where We Work Influences How We Think.

Scientists have been observing the natural world for centuries and have long been intrigued by the high biodiversity and complexity of the tropics. They also usually had North American or European-in other words, outsider-perspectives and frequently concluded that the tropics were qualitatively different from the temperate regions in their ecology, evolution, and behavior. In particular, the tropics were seen as having a more benign abiotic environment, which in turn fostered more complex biotic relationships, with increased competition and other interactions. This may or may not be the case. Regardless, these ideas establish the temperate regions of the world as a kind of model system, a norm to which the tropics are compared and seen as different or unusual. The tropics are warmer or more diverse, rather than the temperate zone being cooler or less diverse. Such an attitude makes it difficult both to appreciate the scope of variation in nature and to develop accurate and general models for ecological and evolutionary processes.

Alternative Reproductive Tactics in Context: How Demography, Ecology, and Behavior Affect Male Mating Success.

Exploitation of sexual signals by predators or parasites increases costs to signalers, creating opportunities for establishment of alternative reproductive tactics (ARTs). In field crickets, males calling may attract acoustically orienting parasitoid flies. Alternatively, males behaving as satellites forgo calling and attempt to intercept females attracted to callers. We modeled the contribution of calling versus satellite behavior to male reproductive success in the larger context of variation in ecology (parasitism rate, background mortality), demography (density, sex ratio), and female behavior (phonotaxis, mating choosiness). Male mating success was most influenced by number of females (standardized effect size 0.42), followed by female choosiness (0.33), background mortality (-0.31), number of males (-0.28), and parasitism rate (-0.21). The smallest effects were phonotaxis (0.10) and satellite behavior (-0.09). Although satellite behavior ameliorated negative effects of parasitism, its comparative effect was slight. ARTs seem most likely to evolve and persist when a single selection pressure on signaling is particularly strong.

Alternative Reproductive Tactics Arising from a Continuous Behavioral Trait: Callers versus Satellites in Field Crickets.

Alternative reproductive tactics may arise when natural enemies use sexual signals to locate the signaler. In field crickets, elevated costs to male calling due to acoustically orienting parasitoid flies create opportunity for an alternative tactic, satellite behavior, where noncalling males intercept females attracted to callers. Although the caller-satellite system in crickets that risk detection by parasitoids resembles distinct behavioral phenotypes, a male's propensity to behave as caller or satellite can be a continuously variable trait over several temporal scales, and an individual may pursue alternate tactics at different times. We modeled a caller-satellite-parasitoid system as a spatially explicit interaction among male and female crickets using individual-based simulation. Males varied in their propensity to call versus behave as a satellite from one night to the next. We varied mortality, density, sex ratio, and female mating behavior, and recorded lifetime number of mates as a function of a male's probability of calling (vs. acting as a satellite) along a gradient in parasitism risk. Frequently, the optimal behavior switched abruptly from being pure caller (call every night) to pure satellite (never call) as parasitism rate increased. However, mixed strategies prevailed even with high parasitism risk under conditions of higher background mortality rate, decreasing density, increasing female-biased sex ratio, and increasing female choosiness. In natural populations, high parasitoid pressure alone would be unlikely to yield fixation of pure satellite behavior.

Model systems, taxonomic bias, and sexual selection: beyond Drosophila.

Although model systems are useful in entomology, allowing generalizations based on a few well-known species, they also have drawbacks. It can be difficult to know how far to generalize from information in a few species: Are all flies like Drosophila? The use of model systems is particularly problematic in studying sexual selection, where variability among taxa is key to the evolution of different behaviors. A bias toward the use of a few insect species, particularly from the genus Drosophila, is evident in the sexual selection and sexual conflict literature over the past several decades, although the diversity of study organisms has increased more recently. As the number of model systems used to study sexual conflict increased, support for the idea that sexual interactions resulted in harm to females decreased. Future work should choose model systems thoughtfully, combining well-known species with those that can add to the variation that allows us to make more meaningful generalizations.

Reproductive biology of Hawaiian lava crickets.

Insects have spread across diverse ecological niches, including extreme environments requiring specialized traits for survival. However, little is understood about the reproductive traits required to facilitate persistence in such environments. Here, we report on the reproductive biology of two species of endemic Hawaiian lava crickets (Caconemobius fori and Caconemobius anahulu) that inhabit barren lava flows on the Big Island. We examine traits that reflect investment into reproduction for both male and female lava crickets and compare them to the non-extremophile Allard's ground cricket (Allonemobius allardi) in the same sub-family. Lava cricket females possessed fewer, but much larger eggs than ground crickets, while males do not provide the costly nuptial gifts that are characteristic of the Nemobiinae subfamily. Lava crickets also have longer ovipositors relative to their body length than related Caconemobius species that occupy cave habitats on the Hawaiian islands. The differences in reproduction we report reveal how these little-known cricket species may increase survival of their offspring in the resource-deprived conditions of their hot, dry environments.

Machine learning reveals singing rhythms of male Pacific field crickets are clock controlled.

Circadian rhythms are ubiquitous in nature and endogenous circadian clocks drive the daily expression of many fitness-related behaviors. However, little is known about whether such traits are targets of selection imposed by natural enemies. In Hawaiian populations of the nocturnally active Pacific field cricket (Teleogryllus oceanicus), males sing to attract mates, yet sexually selected singing rhythms are also subject to natural selection from the acoustically orienting and deadly parasitoid fly, Ormia ochracea. Here, we use T. oceanicus to test whether singing rhythms are endogenous and scheduled by circadian clocks, making them possible targets of selection imposed by flies. We also develop a novel audio-to-circadian analysis pipeline, capable of extracting useful parameters from which to train machine learning algorithms and process large quantities of audio data. Singing rhythms fulfilled all criteria for endogenous circadian clock control, including being driven by photoschedule, self-sustained periodicity of approximately 24 h, and being robust to variation in temperature. Furthermore, singing rhythms varied across individuals, which might suggest genetic variation on which natural and sexual selection pressures can act. Sexual signals and ornaments are well-known targets of selection by natural enemies, but our findings indicate that the circadian timing of those traits' expression may also determine fitness.