Nathan W. Bailey

Same-sex sexual behavior and evolution

Same-sex sexual behavior has been extensively documented in non-human animals. Here we review the contexts in which it has been studied, focusing on case studies that have tested both adaptive and non-adaptive explanations for the persistence of same-sex sexual behavior. Researchers have begun to make headway unraveling possible evolutionary origins of these behaviors and reasons for their maintenance in populations, and we advocate expanding these approaches to examine their role as agents of evolutionary change. Future research employing theoretical, comparative and experimental approaches could provide a greater understanding not only of how selection might have driven the evolution of same-sex sexual behaviors but also ways in which such behaviors act as selective forces that shape social, morphological and behavioral evolution.

Field crickets change mating preferences using remembered social information

Plasticity in female mate choice can fundamentally alter selection on male ornaments, but surprisingly few studies have examined the role of social learning in shaping female mating decisions in invertebrates. We used the field cricket Teleogryllus oceanicus to show that females retain information about the attractiveness of available males based on previous social experience, compare that information with incoming signals and then dramatically reverse their preferences to produce final, predictable, mating decisions. Male ornament evolution in the wild may depend much more on the social environment and behavioural flexibility through learning than was previously thought for non-social invertebrates. The predictive power of these results points to a pressing need for theoretical models of sexual selection that incorporate effects of social experience.

RUNAWAY SEXUAL SELECTION WITHOUT GENETIC CORRELATIONS: SOCIAL ENVIRONMENTS AND FLEXIBLE MATE CHOICE INITIATE AND ENHANCE THE FISHER PROCESS

Female mating preferences are often flexible, reflecting the social environment in which they are expressed. Associated indirect genetic effects (IGEs) can affect the rate and direction of evolutionary change, but sexual selection models do not capture these dynamics. We incorporate IGEs into quantitative genetic models to explore how variation in social environments and mate choice flexibility influence Fisherian sexual selection. The importance of IGEs is that runaway sexual selection can occur in the absence of a genetic correlation between male traits and female preferences. Social influences can facilitate the initiation of the runaway process and increase the rate of trait elaboration. Incorporating costs to choice do not alter the main findings. Our model provides testable predictions: (1) genetic covariances between male traits and female preferences may not exist, (2) social flexibility in female choice will be common in populations experiencing strong sexual selection, (3) variation in social environments should be associated with rapid sexual trait divergence, and (4) secondary sexual traits will be more elaborate than previously predicted. Allowing feedback from the social environment resolves discrepancies between theoretical predictions and empirical data, such as why indirect selection on female preferences, theoretically weak, might be sufficient for preferences to become elaborated.

Does signalling mitigate the cost of agonistic interactions? A test in a cricket that has lost its song

Prevailing models of animal communication assume that signalling during aggressive conflict mitigates the costs of fighting. We tested this assumption by staging dyadic encounters between male field crickets, Teleogryllus oceanicus, under three conditions: (i) both males could sing aggressive songs, (ii) neither male could sing, and (iii) one male could sing but the other could not. We conducted experiments on males from a Hawaiian population from Kauai that has recently evolved signal loss, and males from a Hawaiian population from the Big Island that has not. Among both populations, interactions between two silent males were characterized by higher levels of aggression than interactions involving one or two singing males. Because the level of aggression is strongly related to the cost of fighting, these data demonstrate that signalling mitigates the cost of fighting. In mixed trials, we found no statistically significant differences between the behaviour of calling and non-calling males in either population. We conclude that there is no evidence that the Kauai population exhibits special adaptations to alleviate the costs of signal loss. Finally, we found that males were much more likely to signal after their opponents retreat than after their own retreat. Aggressive song therefore meets the definition of a ‘victory display’.

Rapid Convergent Evolution in Wild Crickets

The earliest stages of convergent evolution are difficult to observe in the wild, limiting our understanding of the incipient genomic architecture underlying convergent phenotypes. To address this, we capitalized on a novel trait, flatwing, that arose and proliferated at the start of the 21st century in a population of field crickets (Teleogryllus oceanicus) on the Hawaiian island of Kauai. Flatwing erases sound-producing structures on male forewings. Mutant males cannot sing to attract females, but they are protected from fatal attack by an acoustically orienting parasitoid fly (Ormia ochracea). Two years later, the silent morph appeared on the neighboring island of Oahu. We tested two hypotheses for the evolutionary origin of flatwings in Hawaii: (1) that the silent morph originated on Kauai and subsequently introgressed into Oahu and (2) that flatwing originated independently on each island. Morphometric analysis of male wings revealed that Kauai flatwings almost completely lack typical derived structures, whereas Oahu flatwings retain noticeably more wild-type wing venation. Using standard genetic crosses, we confirmed that the mutation segregates as a single-locus, sex-linked Mendelian trait on both islands. However, genome-wide scans using RAD-seq recovered almost completely distinct markers linked with flatwing on each island. The patterns of allelic association with flatwing on either island reveal different genomic architectures consistent with the timing of two mutational events on the X chromosome. Divergent wing morphologies linked to different loci thus cause identical behavioral outcomes--silence--illustrating the power of selection to rapidly shape convergent adaptations from distinct genomic starting points.

Evolutionary models of extended phenotypes

A variety of theoretical models incorporate phenotypes expressed in the external environment, but a core question is whether such traits generate dynamics that alter evolution. This has proven to be a challenging and controversial proposition. However, several recent modelling frameworks provide insight: indirect genetic effect (IGE) models, niche construction models, and evolutionary feedback models. These distinct approaches converge upon the observation that gene action at a distance generates feedback that expands the range of trait values and evolutionary rates that we should expect to observe in empirical studies. Such conceptual replication provides solid evidence that traits with extended effects have important evolutionary consequences, but more empirical work is needed to evaluate the predictive power of different modelling approaches.

Exposure to sexual signals during rearing increases immune defence in adult field crickets

Increased investment in immunity is expected to be beneficial under crowded conditions because of the greater risk of pathogen and parasite transmission, but the evolution of this facultative response relies on the ability to accurately assess social cues in the environment and adjust immune defences accordingly. Because of their highly conspicuous nature, long-range sexual signals are prime candidates to be used in evaluating the social conditions likely to be experienced upon adulthood in continuously breeding species; however, their role in mediating immune responses is unknown. We tested whether exposure to acoustic sexual signals in the field cricket Teleogryllus oceanicus affects immunity by manipulating male juvenile experience of acoustic signals, and measuring the effect on adult immunity. Adult males exposed to song during rearing showed stronger immune responses than males reared in silence: they were better able to encapsulate artificial nylon implants and showed higher levels of antimicrobial lysozyme-like activity in their haemolymph. Experience of sexual signals thus translates into increased immunity, which suggests that such signals may play a role in conveying information about population demography and shaping density-dependent responses in unintended receivers.

Mate choice plasticity in the field cricket Teleogryllus oceanicus: effects of social experience in multiple modalities

Social experience can elicit phenotypically plastic changes in mate choice, but little is known about the degree to which social information from one modality can influence mating decisions based on information from a different modality. I used the field cricket Teleogryllus oceanicus to test whether experience of chemical cues mimicking a high density of sexually mature males causes changes in mate choice based on acoustic signals. T. oceanicus males produce long-range calling songs to attract females for mating, but they also produce waxy, non-volatile hydrocarbons on their cuticle (CHCs) which, when deposited on a substrate, can be detected by females and may provide demographic information. I manipulated female experience of substrate-bound male CHCs and then performed acoustic mate choice trials. When CHCs were present on the substrate during trials, females showed greater motivation to respond to male calling song. This effect diminished with repeated exposure to male songs, demonstrating that the importance of olfactory cues in altering acoustic mate choice decreased with increasing exposure to acoustic signals. However, the temporal nature of CHC experience mattered: previous experience of CHCs did not alter subsequent female choice for male calling song traits. Exposure to male song increased the threshold of mate acceptance over time, and individuals varied considerably in overall levels of responsiveness. Taken together, the results demonstrate that mate choice is dependent on social context mediated by multiple modalities in T. oceanicus, but they do not support the idea that prior experience of social cues in one modality necessarily influences later mating decisions based on other signalling modalities.

Tissue-Specific Transcriptomics in the Field Cricket Teleogryllus oceanicus

Field crickets (family Gryllidae) frequently are used in studies of behavioral genetics, sexual selection, and sexual conflict, but there have been no studies of transcriptomic differences among different tissue types. We evaluated transcriptome variation among testis, accessory gland, and the remaining whole-body preparations from males of the field cricket, Teleogryllus oceanicus. Non-normalized cDNA libraries from each tissue were sequenced on the Roche 454 platform, and a master assembly was constructed using testis, accessory gland, and whole-body preparations. A total of 940,200 reads were assembled into 41,962 contigs, to which 36,856 singletons (reads not assembled into a contig) were added to provide a total of 78,818 sequences used in annotation analysis. A total of 59,072 sequences (75%) were unique to one of the three tissues. Testis tissue had the greatest proportion of tissue-specific sequences (62.6%), followed by general body (56.43%) and accessory gland tissue (44.16%). We tested the hypothesis that tissues expressing gene products expected to evolve rapidly as a result of sexual selection—testis and accessory gland—would yield a smaller proportion of BLASTx matches to homologous genes in the model organism Drosophila melanogaster compared with whole-body tissue. Uniquely expressed sequences in both testis and accessory gland showed a significantly lower rate of matching to annotated D. melanogaster genes compared with those from general body tissue. These results correspond with empirical evidence that genes expressed in testis and accessory gland tissue are rapidly evolving targets of selection.

Dispersal differences predict population genetic structure in Mormon crickets

Research investigating the geographical context of speciation has primarily focused on abiotic factors such as the role of Pleistocene glacial cycles, or geotectonic events. Few study systems allow a direct comparison of how biological differences, such as dispersal behaviour, affect population genetic structure of organisms that were subdivided during the Pleistocene. Mormon crickets exist in solitary and gregarious ‘phases’, which broadly correspond with an east–west mtDNA division across the Rocky Mountains. Gregarious individuals form bands that can move up to 2 km daily. This study assessed whether population genetic structure results mainly from deep Pleistocene vicariance or if we can also detect more recent genetic patterns due to phase and dispersal differences superimposed on the older, deeper divisions. We found that separation in refugia was a more important influence on genetic divergence than phase, with the Rockies acting as a barrier that separated Mormon cricket populations into eastern and western refugia during Pleistocene glacial cycles. However, patterns of isolation by distance differ between eastern and western clades for both mitochondrial and nuclear DNA, with greater divergence within the eastern, solitary clade. An mtDNA haplotype mismatch distribution is compatible with historical population expansion in the western clade but not in the eastern clade. A persistent (and possibly sex‐biased) difference in dispersal ability has most likely influenced the greater population genetic structure seen in the eastern clade, emphasizing the importance of the interaction of Quaternary climate fluctuations and geography with biotic factors in producing the patterns of genetic subdivision observed today.