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Title: Chronobiology as compensation: can biological rhythms compensate for sexual signals?
Conspicuous sexual signals come with costs and benefits. Such signals increase reproductive success but may also reduce survival or viability. It has recently been suggested that non-signal traits may alleviate some of those costs (termed “compensatory traits”). In this perspective piece, we argue that biological rhythms should be considered in the milieu of compensatory traits, as they can reduce the natural selection burden of signaling. This may be particularly true for the many sexual signals that are ephemeral (i.e., only periodically present like a courtship dance). Biological rhythms (e.g., circadian and circannual rhythms) are ubiquitous in nature and help organisms perform the right activity at the right time—this includes the timing of many sexual signals and reproductive traits. Timing itself may, in fact, reduce the costs of such sexual signals. Here, we review sexual signals that are governed by biological rhythms and discuss how signal modality and type (ornament, weapon, dominance trait) account for differences in how chronobiology may act as a compensatory trait. We then consider how biologists might examine the untested role of chronobiology as a compensatory trait and set forth compelling questions for future work. more »« less
Westwood, Mary L; Geissmann, Quentin; O’Donnell, Aidan J; Rayner, Jack; Schneider, Will; Zuk, Marlene; Bailey, Nathan W; Reece, Sarah E
(, Behavioral Ecology)
Pinter-Wollman, Noa
(Ed.)
Abstract 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.
Abstract The process of reproductive character displacement involves divergence and/or the narrowing of variance in traits involved in species recognition, driven by interactions between taxa. However, stabilizing sexual selection may favor stasis and species similarity in these same traits if signals are optimized for transmission through the prevailing environment. Further, sexual selection may promote increased variability within species to facilitate individual recognition. Here we ask how the conflicting selection pressures of species recognition and sexual selection are resolved in a genus of Himalayan birds that sing exceptionally similar songs. We experimentally show that small differences in two traits (note shape and peak frequency) are both necessary and sufficient for species recognition. Song frequency shows remarkable clinal variation along the Himalayan elevational gradient, being most divergent where species co-occur, the classic signature of reproductive character displacement. Note shape shows no such clinal variation but varies more between individuals of an allopatric species than it does among individuals within species that co-occur. We argue that the different note shapes experience similar transmission constraints, and differences produced through species interactions spread back through the entire species range. Our results imply that reproductive character displacement is likely to be common.
Despite the well-known effects of sexual selection on phenotypes, links between this evolutionary process and reproductive isolation, genomic divergence, and speciation have been difficult to establish. We unravel the genetic basis of sexually selected plumage traits to investigate their effects on reproductive isolation in barn swallows. The genetic architecture of sexual traits is characterized by 12 loci on two autosomes and the Z chromosome. Sexual trait loci exhibit signatures of divergent selection in geographic isolation and barriers to gene flow in secondary contact. Linkage disequilibrium between these genes has been maintained by selection in hybrid zones beyond what would be expected under admixture alone. Our findings reveal that selection on coupled sexual trait loci promotes reproductive isolation, providing key empirical evidence for the role of sexual selection in speciation.
BACKGROUND Charles Darwin’s Descent of Man, and Selection in Relation to Sex tackled the two main controversies arising from the Origin of Species: the evolution of humans from animal ancestors and the evolution of sexual ornaments. Most of the book focuses on the latter, Darwin’s theory of sexual selection. Research since supports his conjecture that songs, perfumes, and intricate dances evolve because they help secure mating partners. Evidence is overwhelming for a primary role of both male and female mate choice in sexual selection—not only through premating courtship but also through intimate interactions during and long after mating. But what makes one prospective mate more enticing than another? Darwin, shaped by misogyny and sexual prudery, invoked a “taste for the beautiful” without speculating on the origin of the “taste.” How to explain when the “final marriage ceremony” is between two rams? What of oral sex in bats, cloacal rubbing in bonobos, or the sexual spectrum in humans, all observable in Darwin’s time? By explaining desire through the lens of those male traits that caught his eyes and those of his gender and culture, Darwin elided these data in his theory of sexual evolution. Work since Darwin has focused on how traits and preferences coevolve. Preferences can evolve even if attractive signals only predict offspring attractiveness, but most attention has gone to the intuitive but tenuous premise that mating with gorgeous partners yields vigorous offspring. By focusing on those aspects of mating preferences that coevolve with male traits, many of Darwin’s influential followers have followed the same narrow path. The sexual selection debate in the 1980s was framed as “good genes versus runaway”: Do preferences coevolve with traits because traits predict genetic benefits, or simply because they are beautiful? To the broader world this is still the conversation. ADVANCES Even as they evolve toward ever-more-beautiful signals and healthier offspring, mate-choice mechanisms and courter traits are locked in an arms race of coercion and resistance, persuasion and skepticism. Traits favored by sexual selection often do so at the expense of chooser fitness, creating sexual conflict. Choosers then evolve preferences in response to the costs imposed by courters. Often, though, the current traits of courters tell us little about how preferences arise. Sensory systems are often tuned to nonsexual cues like food, favoring mating signals resembling those cues. And preferences can emerge simply from selection on choosing conspecifics. Sexual selection can therefore arise from chooser biases that have nothing to do with ornaments. Choice may occur before mating, as Darwin emphasized, but individuals mate multiple times and bias fertilization and offspring care toward favored partners. Mate choice can thus occur in myriad ways after mating, through behavioral, morphological, and physiological mechanisms. Like other biological traits, mating preferences vary among individuals and species along multiple dimensions. Some of this is likely adaptive, as different individuals will have different optimal mates. Indeed, mate choice may be more about choosing compatible partners than picking the “best” mate in the absolute sense. Compatibility-based choice can drive or reinforce genetic divergence and lead to speciation. The mechanisms underlying the “taste for the beautiful” determine whether mate choice accelerates or inhibits reproductive isolation. If preferences are learned from parents, or covary with ecological differences like the sensory environment, then choice can promote genetic divergence. If everyone shares preferences for attractive ornaments, then choice promotes gene flow between lineages. OUTLOOK Two major trends continue to shift the emphasis away from male “beauty” and toward how and why individuals make sexual choices. The first integrates neuroscience, genomics, and physiology. We need not limit ourselves to the feathers and dances that dazzled Darwin, which gives us a vastly richer picture of mate choice. The second is that despite persistent structural inequities in academia, a broader range of people study a broader range of questions. This new focus confirms Darwin’s insight that mate choice makes a primary contribution to sexual selection, but suggests that sexual selection is often tangential to mate choice. This conclusion challenges a persistent belief with sinister roots, whereby mate choice is all about male ornaments. Under this view, females evolve to prefer handsome males who provide healthy offspring, or alternatively, to express flighty whims for arbitrary traits. But mate-choice mechanisms also evolve for a host of other reasons Understanding mate choice mechanisms is key to understanding how sexual decisions underlie speciation and adaptation to environmental change. New theory and technology allow us to explicitly connect decision-making mechanisms with their evolutionary consequences. A century and a half after Darwin, we can shift our focus to females and males as choosers, rather than the gaudy by-products of mate choice. Mate choice mechanisms across domains of life. Sensory periphery for stimulus detection (yellow), brain for perceptual integration and evaluation (orange), and reproductive structures for postmating choice among pollen or sperm (teal). ILLUSTRATION: KELLIE HOLOSKI/ SCIENCE
Moehring, Amanda J.; Boughman, Janette W.
(, Biology Letters)
Males in many species have elaborated sexual traits that females strongly prefer, and these traits often conspicuously differ among species. How novel preferences and traits originate, however, is a challenging evolutionary problem because the initial appearance of only the female preference or only the male trait should reduce the ability to find a suitable mate, which could reduce fitness for individuals possessing those novel alleles. Here, we present a hypothesis for how novel preferences, as well as the novel male traits that females prefer, can originate, be favoured and spread in polyandrous species. Novel preference mutations can arise as ‘veiled preferences’ that are not expressed when the corresponding male trait is not present in the population, allowing preferences to be hidden from selection, and thus persist. In those cases when a male trait is present, veiled preferences provide a selective advantage, and females disproportionately produce offspring from preferred males through either mate choice or cryptic female choice. This tips the fitness advantage for novel males, allowing both preference and trait to spread, and limiting selection against them in the absence of the corresponding trait or preference.
Westwood, Mary L, Broder, E Dale, Welsh, Gabrielle T, and Tinghitella, Robin M. Chronobiology as compensation: can biological rhythms compensate for sexual signals?. Retrieved from https://par.nsf.gov/biblio/10569769. Frontiers in Ethology 3. Web. doi:10.3389/fetho.2024.1473358.
Westwood, Mary L, Broder, E Dale, Welsh, Gabrielle T, & Tinghitella, Robin M. Chronobiology as compensation: can biological rhythms compensate for sexual signals?. Frontiers in Ethology, 3 (). Retrieved from https://par.nsf.gov/biblio/10569769. https://doi.org/10.3389/fetho.2024.1473358
Westwood, Mary L, Broder, E Dale, Welsh, Gabrielle T, and Tinghitella, Robin M.
"Chronobiology as compensation: can biological rhythms compensate for sexual signals?". Frontiers in Ethology 3 (). Country unknown/Code not available: Frontiers. https://doi.org/10.3389/fetho.2024.1473358.https://par.nsf.gov/biblio/10569769.
@article{osti_10569769,
place = {Country unknown/Code not available},
title = {Chronobiology as compensation: can biological rhythms compensate for sexual signals?},
url = {https://par.nsf.gov/biblio/10569769},
DOI = {10.3389/fetho.2024.1473358},
abstractNote = {Conspicuous sexual signals come with costs and benefits. Such signals increase reproductive success but may also reduce survival or viability. It has recently been suggested that non-signal traits may alleviate some of those costs (termed “compensatory traits”). In this perspective piece, we argue that biological rhythms should be considered in the milieu of compensatory traits, as they can reduce the natural selection burden of signaling. This may be particularly true for the many sexual signals that are ephemeral (i.e., only periodically present like a courtship dance). Biological rhythms (e.g., circadian and circannual rhythms) are ubiquitous in nature and help organisms perform the right activity at the right time—this includes the timing of many sexual signals and reproductive traits. Timing itself may, in fact, reduce the costs of such sexual signals. Here, we review sexual signals that are governed by biological rhythms and discuss how signal modality and type (ornament, weapon, dominance trait) account for differences in how chronobiology may act as a compensatory trait. We then consider how biologists might examine the untested role of chronobiology as a compensatory trait and set forth compelling questions for future work.},
journal = {Frontiers in Ethology},
volume = {3},
publisher = {Frontiers},
author = {Westwood, Mary L and Broder, E Dale and Welsh, Gabrielle T and Tinghitella, Robin M},
}
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