Social Plasticity Enhances Signal-Preference Codivergence.

AbstractThe social environment is often the most dynamic and fitness-relevant environment animals experience. Here we tested whether plasticity arising from variation in social environments can promote signal-preference divergence-a key prediction of recent speciation theory but one that has proven difficult to test in natural systems. Interactions in mixed social aggregations could reduce, create, or enhance signal-preference differences. In the latter case, social plasticity could establish or increase assortative mating. We tested this by rearing two recently diverged species of Enchenopa treehoppers-sap-feeding insects that communicate with plant-borne vibrational signals-in treatments consisting of mixed-species versus own-species aggregations. Social experience with heterospecifics (in the mixed-species treatment) resulted in enhanced signal-preference species differences. For one of the two species, we tested but found no differences in the plastic response between sympatric and allopatric sites, suggesting the absence of reinforcement in the signals and preferences and their plastic response. Our results support the hypothesis that social plasticity can create or enhance signal-preference differences and that this might occur in the absence of long-term selection against hybridization on plastic responses themselves. Such social plasticity may facilitate rapid bursts of diversification.

Combinatorial Signal Processing in an Insect.

AbstractHuman language is combinatorial: phonemes are grouped into syllables, syllables are grouped into words, and so on. The capacity for combinatorial processing is present, in different degrees, in some mammals and birds. We used vibrational insects, Enchenopa treehoppers, to test the hypothesis of basic combinatorial processing against two competing hypotheses: beginning rule (where the early signal portions play a stronger role in acceptability) and no ordering rule (where the order of signal elements plays no role in signal acceptability). Enchenopa males use plant-borne vibrational signals that consist of a whine followed by pulses. We tested the above hypotheses with vibrational playback experiments in which we presented Enchenopa females with stimuli varying in signal element combinations. We monitored female responses to these playbacks with laser vibrometry. We found strong support for combinatorial processing in Enchenopa: in brief, females preferred natural-combination signals regardless of the beginning element and discriminated against reverse-order signals or individual elements. Finding support for the combinatorial rule hypothesis in insects suggests that this capability represents a common solution to the problems presented by complex communication.

The relationship between a combinatorial processing rule and a continuous mate preference function in an insect.

Mate choice involves processing signals that can reach high levels of complexity and feature multiple components, even in small animals with tiny brains. This raises the question of whether and how such organisms deal with this complexity. One solution involves combinatorial processing, whereby different signal elements are processed as single units. Combinatorial processing has been described in several mammals and birds, and recently in a vibrationally signalling insect, Enchenopa treehoppers. Here, we ask about the relationship between combinatorial rules and mate preferences for continuously varying signal features. Enchenopa male advertisement signals are composed of two elements: a 'whine' followed by a set of pulses. The dominant frequency of the whine and element combination both matter to females. We presented synthetic signals varying in element order (natural [whine-pulses], reverse [pulses-whine]) and in frequency to Enchenopa females and recorded their responses. The reverse combination resulted in a decrease in attractiveness of the signals, and also slightly changed the shape of the preference for frequency. We found that females could be classified into three 'types': females with both a strong preference and a strong combinatorial rule, females with both a weak preference and weak rule, and females with a strong preference but a weak rule. Our results suggest that in Enchenopa signal processing, the mate preference for a continuous signal feature 'takes precedence' over, but also interacts with, the combinatorial rule. The relationship between the preference and the rule could evolve to take different forms according to selection on mate choice decisions. We suggest that exploring the relationship between such preferences and rules in species with more complex signals will bring insight into the evolution of the multi-component communication systems.

Signalling interactions during ontogeny are a cause of social plasticity in Enchenopa treehoppers (Hemiptera: Membracidae).

We recently discovered that there is a social ontogeny of signals and preferences in Enchenopa treehoppers. Nymphs signalled throughout their development; some signal features changed gradually and in sexually dimorphic ways throughout ontogeny; and some adult male signal features and female mate preferences differed between individuals reared in isolation or groups. In this paper, we investigate whether signalling interactions during ontogeny are a cause of plasticity in mating signals and preferences. We subjected Enchenopa nymphs to treatments of either: rearing in aggregations (the natural condition), in isolation, or in isolation with playbacks of nymph signals. We then described variation in the signals and mating preferences of individuals that developed in those conditions. The playback treatments partially "rescued" the signal and preference phenotypes, resulting in phenotypes either similar to those that result from rearing in aggregations, or intermediate between those that result from rearing in isolation or in aggregations. These results pin-point signalling interactions during ontogeny as an important cause of plasticity in signals and mate preferences.