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.

Animals eavesdrop on signals and cues generated by prey, predators, hosts, parasites, competing species, and conspecifics, and the conspicuousness of sexual signals makes them particularly susceptible. Yet, when sexual signals evolve, most attention is paid to impacts on intended receivers (potential mates) rather than fitness consequences for eavesdroppers. Using the rapidly evolving interaction between the Pacific field cricket, Teleogryllus oceanicus , and the parasitoid fly, Ormia ochracea , we asked how parasitoids initially respond to novel changes in host signals. We recently discovered a novel sexual signal, purring song, in Hawaiian populations of T. oceanicus that appears to have evolved because it protects the cricket from the parasitoid while still allowing males to attract female crickets for mating. In Hawaii, there are no known alternative hosts for the parasitoid, so we would expect flies to be under selection to detect and attend to the new purring song. We used complementary field and laboratory phonotaxis experiments to test fly responses to purring songs that varied in many dimensions, as well as to ancestral song. We found that flies strongly prefer ancestral song over purring songs in both the field and the lab, but we caught more flies to purring songs in the field than reported in previous work, indicating that flies may be exerting some selective pressure on the novel song. When played at realistic amplitudes, we found no preferences–flies responded equally to all purrs that varied in frequency, broadbandedness, and temporal measures. However, our lab experiment did reveal the first evidence of preference for purring song amplitude, as flies were more attracted to purrs played at amplitudes greater than naturally occurring purring songs. As purring becomes more common throughout Hawaii, flies that can use purring song to locate hosts should be favored by selection and increase in frequency.

No 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.

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.

In the original publication of the article, the author wanted to correct the typography errors in the acknowledgement text as well as in the text which were missed to notice before publishing. Now, the original article has been updated with those corrections.Publisher's Note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.