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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.
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Decoupling of sexual signals and their underlying morphology facilitates rapid phenotypic diversification
How novel phenotypes evolve is challenging to imagine because traits are often underlain by numerous integrated phenotypic components, and changes to any one form can disrupt the function of the entire module. Yet novel phenotypes do emerge, and research on adaptive phenotypic evolution suggests that complex traits can diverge while either maintaining existing form–function relationships or through innovations that alter form–function relationships. How these alternate routes contribute to sexual signal evolution is poorly understood, despite the role of sexual signals in generating biodiversity. In Hawaiian populations of the Pacific field cricket, male song attracts both female crickets and a deadly acoustically orienting parasitoid fly. In response to this conflict between natural and sexual selection, male crickets have evolved altered wing morphologies multiple times, resulting in loss and dramatic alteration of sexual signals. More recently, we and others have observed a radical increase in sexual signal variation and the underlying morphological structures that produce song. We conducted the first combined analysis of form (wing morphology), function (emergent signal), and receiver responses to characterize novel variation, test alternative hypotheses about form–function relationships (Form–Function Continuity vs. Form–Function Decoupling), and investigate underlying mechanistic changes and fitness consequences of novel signals. We identified three sound-producing male morphs (one previously undescribed, named “rattling”) and found that relationships between morphology and signals have been rewired (Form–Function Decoupling), rapidly and repeatedly, through the gain, loss, and alteration of morphological structures, facilitating the production of signals that exist in novel phenotypic space. By integrating across a hierarchy of phenotypes, we uncovered divergent morphs with unique solutions to the challenge of attracting mates while evading fatal parasitism.
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- Award ID(s):
- 1846520
- PAR ID:
- 10482583
- Publisher / Repository:
- Wiley
- Date Published:
- Journal Name:
- Evolution Letters
- ISSN:
- 2056-3744
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Understanding how the early stages of sexual signal diversification proceed is critically important because these microevolutionary dynamics directly shape species trajectories and impact macroevolutionary patterns. Unfortunately, studying this is challenging because signals involve complex interactions between behavior, morphology, and physiology, much of which can only be measured in real-time. In Hawaii, male Pacific field cricket song attracts both females and a deadly parasitoid fly. Over the past two decades, there has been a marked increase in signal variation in Hawaiian populations of these crickets, including novel male morphs with distinct mating songs. We capitalize on this rare opportunity to track changes in morph composition over time in a population with three novel morphs, investigating how mate and parasitoid attraction (components of sexual and natural selection) may shape signal evolution. We find dramatic fluctuation in morph proportions over the three years of the study, including the arrival and rapid increase of one novel morph. Natural and sexual selection pressures act differently among morphs, with some more attractive to mates and others more protected from parasitism. Collectively, our results suggest that differential protection from parasitism among morphs, rather than mate attraction, aligns with recent patterns of phenotypic change in the wild.more » « less
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Abstract Inadvertent cues can be refined into signals through coevolution between signalers and receivers, yet the earliest steps in this process remain elusive. In Hawaiian populations of the Pacific field cricket, a new morph producing a novel and incredibly variable song (purring) has spread across islands. Here we characterize the current sexual and natural selection landscape acting on the novel signal by (1) determining fitness advantages of purring through attraction to mates and protection from a prominent deadly natural enemy, and (2) testing alternative hypotheses about the strength and form of selection acting on the novel signal. In field studies, female crickets respond positively to purrs, but eavesdropping parasitoid flies do not, suggesting purring may allow private communication among crickets. Contrary to the sensory bias and preference for novelty hypotheses, preference functions (selective pressure) are nearly flat, driven by extreme inter-individual variation in function shape. Our study offers a rare empirical test of the roles of natural and sexual selection in the earliest stages of signal evolution.more » « less
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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
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1002/evl3.302
