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.Why does same-sex sexual behavior matter? Same-sex sexual behavior in animals has long fascinated scientists as well as non-scientists. Previous work has emphasized the apparent paradox of selection acting on non-reproductive individuals [1,2], but little is known about the evolutionary consequences of such behavior, whether it occurs as exclusive life-long pairing or as a part of other sexual interactions. The variety and ubiquity of same-sex sexual behavior in animals is impressive; many thousands of instances of same-sex courtship, pair bonding and copulation have been observed in a wide range of species, including mammals, birds, reptiles, amphibians, insects, mollusks and nematodes (Table 1). These observations are likely to be underestimates of the frequency of such interactions, partly because researchers assume that pairs in sexually monomorphic species that are engaging in sexual behavior must be opposite sexes.From an evolutionary perspective, same-sex behavior has been viewed as a puzzle requiring a special explanation, rather like suicide or adoption of unrelated infants [3]. Why would animals engage in sexual behaviors that do not directly result in reproduction? It is clear that lifelong same-sex orientation is unlikely to evolve and, indeed, few examples of life-long pairings in wild animals exist, but the persistent and well-documented occurrence of same-sex sexual behaviors across nearly all taxonomic groups of animals is worth exploring.The purpose of this review is to expand our thinking about the evolutionary implications of same-sex behavior in animals. We suggest that the phenomenon needs to be Review Glossary Alternative reproductive behavior: different methods, mechanisms or strategies for attaining matings found within a single sex. Most often studied in males, alternative mating tactics might be purely behavioral, or might be associated with different morphologies. Cooperative breeding: social structure in which individuals forgo reproduction and provide care for others' offspring, such as feeding, grooming and protection from predation. Gay/lesbian: terms describing homosexual orientation in humans. In typical usage, implies a stereotyped set of lifestyle ch...
Developmental plasticity allows juvenile animals to assess environmental cues and adaptively shape behavioral and morphological traits to maximize fitness in their adult environment. Sexual signals are particularly conspicuous cues, making them likely candidates for mediating such responses. Plasticity in male reproductive traits is a common phenomenon, but empirical evidence for signal-mediated plasticity in males is lacking. We tested whether experience of acoustic sexual signals during juvenile stages influences the development of three adult traits in the continuously breeding field cricket Teleogryllus oceanicus: male mating tactics, reproductive investment, and condition. All three traits were affected by juvenile acoustic experience. Males of this species produce a long-range calling song to attract receptive females, but they can also behave as satellites by parasitizing other males' calls. Males reared in an environment mimicking a population with many calling males were less likely to exhibit satellite behavior, invested more in reproductive tissues, and attained higher condition than males reared in a silent environment. These results contrast with other studies and demonstrate how the effects of juvenile social experience on adult male morphology, reproductive investment, and behavior may subsequently influence sexual selection and phenotypic evolution.
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.
Behavior is rapidly flexible and highly context-dependent, which poses obvious challenges to researchers attempting to dissect its causes. However, over a century of unresolved debate has also focused on whether the very flexibility and context-dependence of behavior lends it a unique role in the evolutionary origins and patterns of diversity in the Animal Kingdom. Here, we propose that both challenges can benefit from studying how indirect genetic effects (IGEs: the effects of genes expressed in one individual on traits in another individual) shape behavioral phenotypes. We provide a sketch of the theoretical framework that grounds IGEs in behavioral ecology research and focus on recent advances made from studies of IGEs in areas of behavioral ecology such as sexual selection, sexual conflict, social dominance, and parent-offspring interactions. There is mounting evidence that IGEs have important influences on behavioral phenotypes associated with these processes, such as sexual signals and preferences and behaviors which function to manipulate interacting partners. IGEs can also influence both responses to selection and selection itself, and considering IGEs refines evolutionary predictions and provides new perspectives on the origins of seemingly perplexing behavioral traits. A key unresolved question, but one that has dominated the behavioral sciences for over a century, is whether behavior is more likely than other types of traits to contribute to evolutionary change and diversification. We advocate taking advantage of an IGE approach to outline falsifiable hypotheses and a general methodology to rigorously test this frequently proposed, yet still contentious, special role of behavior in evolution.
Female choice can drive the evolution of extravagant male traits. In invertebrates, the influence of prior social experience on female choice has only recently been considered. To better understand the evolutionary implications of experience-mediated plasticity in female choice, we investigated the effect of acoustic experience during rearing on female responsiveness to male song in the field cricket Teleogryllus oceanicus. Acoustic experience has unique biological relevance in this species: a morphological mutation has rendered over 90 per cent of males on the Hawaiian island of Kauai silent in fewer than 20 generations, impeding females' abilities to locate potential mates. Females reared in silent conditions mimicking Kauai were less discriminating of male calling song and more responsive to playbacks, compared with females that experienced song during rearing. Our results to our knowledge, are the first demonstration of longterm effects of acoustic experience in an arthropod, and suggest that female T. oceanicus may be able to compensate for the reduced availability of long-range male sexual signals by increasing their responsiveness to the few remaining signallers. Understanding the adaptive significance of experience-mediated plasticity in female choice provides insight into processes that facilitate rapid evolutionary change and shape sexual selection pressure in natural populations.
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