Sexual signals are often transmitted through multiple modalities (e.g., visual and chemical) and under selection from both intended and unintended receivers. Each component of a multimodal signal may be more or less conspicuous to receivers, and signals may evolve to take advantage of available private channels. We recently documented percussive substrate-borne vibrations in the Pacific field cricket (Teleogryllus oceanicus), a species that uses airborne acoustic and chemical signals to attract and secure mates. The airborne signals of Hawaiian T. oceanicus are currently undergoing rapid evolution; at least five novel male morphs have arisen in the past 20 years. Nothing is yet known about the newly discovered percussive substrate-borne vibrations, so we ask “how” they are produced, “who” produces them (e.g., population, morph), “when” they produce them (e.g., whether they are plastic), and “why” (e.g., do they play a role in mating). We show that the vibrations are produced exclusively by males during courtship via foreleg drumming. One novel morph, purring, produces quieter airborne songs and is more likely to drum than the ancestral morph. However, drumming behavior is also contextually plastic for some males; when we removed the ability of males to produce airborne song, ancestral males became more likely to drum, whereas two novel morphs were equally likely to drum regardless of their ability to produce song. Opposite our prediction, females were less likely to mate with males who drummed. We discuss why that might be and describe what we can learn about complex signal evolution from this newly discovered behavior.
- Award ID(s):
- 1846520
- NSF-PAR ID:
- 10379187
- Editor(s):
- Jennions, Michael D
- Date Published:
- Journal Name:
- Behavioral Ecology
- Volume:
- 33
- Issue:
- 4
- ISSN:
- 1045-2249
- Page Range / eLocation ID:
- 859 to 867
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract -
While thought to be widely used for animal communication, substrate-borne vibration is relatively unexplored compared to other modes of communication. Substrate-borne vibrations are important for mating decisions in many orthopteran species, yet substrate-borne vibration has not been documented in the Pacific field cricket Teleogryllus oceanicus . Male T. oceanicus use wing stridulation to produce airborne calling songs to attract females and courtship songs to entice females to mate. A new male morph has been discovered, purring crickets, which produce much quieter airborne calling and courtship songs than typical males. Purring males are largely protected from a deadly acoustically orienting parasitoid fly, and they are still able to attract female crickets for mating though typical calling song is more effective for attracting mates. Here, we document the first record of substrate-borne vibration in both typical and purring male morphs of T. oceanicus . We used a paired microphone and accelerometer to simultaneously record airborne and substrate-borne sounds produced during one-on-one courtship trials in the field. Both typical and purring males produced substrate-borne vibrations during courtship that temporally matched the airborne acoustic signal, suggesting that the same mechanism (wing movement) produces both sounds. As previously established, in the airborne channel, purring males produce lower amplitude but higher peak frequency songs than typical males. In the vibrational channel, purring crickets produce songs that are higher in peak frequency than typical males, but there is no difference in amplitude between morphs. Because louder songs (airborne) are preferred by females in this species, the lack of difference in amplitude between morphs in the substrate-borne channel could have implications for mating decisions. This work lays the groundwork for investigating variation in substrate-borne vibrations in T. oceanicus , intended and unintended receiver responses to these vibrations, and the evolution of substrate-borne vibrations over time in conjunction with rapid evolutionary shifts in the airborne acoustic signal.more » « less
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Abstract Divergence of sexual signals between populations can lead to speciation, yet opportunities to study the immediate aftermath of novel signal evolution are rare. The recent emergence and spread of a new mating song, purring, in Hawaiian populations of the Pacific field cricket (
Teleogryllus oceanicus ) allows us to investigate population divergence soon after the origin of a new signal. Male crickets produce songs with specialized wing structures to attract mates from afar (calling) and entice them to mate when found (courtship). However, in Hawaii, these songs also attract an eavesdropping parasitoid fly (Ormia ochracea ) that kills singing males. The novel purring song, produced with heavily modified wing morphology, attracts female crickets but not the parasitoid fly, acting as a solution to this conflict between natural and sexual selection. We've recently observed increasing numbers of purring males across Hawaii. In this integrative field study, we investigated the distribution of purring and the proportion of purring males relative to other morphs in six populations on four islands and compared a suite of phenotypic traits (wing morphology, calling song and courtship song) that make up this novel signal across populations of purring males. We show that purring is found in varying proportions across five, and is locally dominant in four, Hawaiian populations. We also show that calling songs, courtship songs and wing morphology of purring males differ geographically. Our findings demonstrate the rapid pace of evolution in island populations and provide insights into the emergence and divergence of new sexual signals over time. -
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/ SCIENCEmore » « less
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Abstract Animals often communicate in complex, heterogeneous environments, leading to hypothesized selection for increased detectability or discriminability in signaling traits. The extent to which secondary sexual ornaments have evolved to overcome the challenges of signaling in complex environments, however, remains understudied, especially in comparison to their role as indicator traits. This study tested the hypothesis that the condition-dependent secondary sexual ornamentation in the wolf spider Rabidosa rabida functions to increase detectability/discriminability in visually complex environments. We predicted that male ornamentation would interact with the complexity of the signaling environment to affect male mating success. In particular, we expected ornaments to confer a greater mating advantage when males courted in visually complex environments. To test this, we artificially manipulated male foreleg ornamentation (present/absent) and ran repeated-measures mating trials across laboratory microcosms that represented simple versus complex visual signaling environments. Microcosm visual complexity differed in their background pattern, grass stem color, and grass stem placement. We found that ornamented males mated more often and more quickly than unornamented males across both environments, but we found no support for an ornament-by-environment interaction. Male courtship rate, however, did interact with the signaling environment. Despite achieving the same level of mating success across signaling environments, ornamented males courted less rapidly in complex versus simple environments, although environmental complexity had no influence on unornamented male courtship rates. Our results suggest that the visual complexity of the signaling environment influences the interactive influence of ornamentation and dynamic visual courtship on female mate choice.
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/beheco/arac049
