Rafael L. Rodríguez

The Behavioral Ecology of Insect Vibrational Communication

Abstract Vibrational communication is widespread in insect social and ecological interactions. Of the insect species that communicate using sound, water surface ripples, or substrate vibrations, we estimate that 92% use substrate vibrations alone or with other forms of mechanical signaling. Vibrational signals differ dramatically from airborne insect sounds, often having low frequencies, pure tones, and combinations of contrasting acoustic elements. Plants are the most widely used substrate for transmitting vibrational signals. Plant species can vary in their signal transmission properties, and thus host plant use may influence signal divergence. Vibrational communication occurs in a complex environment containing noise from wind and rain, the signals of multiple individuals and species, and vibration-sensitive predators and parasitoids. We anticipate that many new examples and functions of vibrational communication will be discovered, and that study of this modality will continue to provide important insights into insect social behavior, ecology, and evolution.

Evidence that female preferences have shaped male signal evolution in a clade of specialized plant-feeding insects

Mate choice is considered an important influence in the evolution of mating signals and other sexual traits, and—since divergence in sexual traits causes reproductive isolation—it can be an agent of population divergence. The importance of mate choice in signal evolution can be evaluated by comparing male signal traits with female preference functions, taking into account the shape and strength of preferences. Specifically, when preferences are closed (favouring intermediate values), there should be a correlation between the preferred values and the trait means, and stronger preferences should be associated with greater preference–signal correspondence and lower signal variability. When preferences are open (favouring extreme values), signal traits are not only expected to be more variable, but should also be shifted towards the preferred values. We tested the role of female preferences in signal evolution in the Enchenopa binotata species complex of treehoppers, a clade of plant-feeding insects hypothesized to have speciated in sympatry. We found the expected relationship between signals and preferences, implicating mate choice as an agent of signal evolution. Because differences in sexual communication systems lead to reproductive isolation, the factors that promote divergence in female preferences—and, consequently, in male signals—may have an important role in the process of speciation.

Genotype–environment interaction and the reliability of mating signals

I t is a central tenet of animal communication theory that signals are reliable (Zahavi 1977). That is, the characteristics of a signal that are attended to by a receiver should be reasonably good predictors of the transmitter’s current physical ability, internal state or motivation, social status, or acquired information. Signal characteristics should also predict the future consequences that a receiver, responding in a particular way, is likely to experience. Whereas the range of signals that animals transmit between one another may certainly include some messages that are not fully honest (Hasson 1994; e.g. Backwell et al. 2000), and partially withholding information or identity can sometimes be in a transmitter’s best interest (Johnstone 1997), animal communications are generally expected to result in a net benefit to both signaller and receiver (see Hauser 1996; Bradbury & Vehrencamp 1998). This expectation rests on the reasoning that failure to meet the criterion of reliability, as when an ‘inferior’ individual broadcasts a ‘strong’ signal normally associated with superior physical prowess, should result in selection against receiver responses to the signal, which, in turn, would select against its continued transmission, without alteration, by the signaller. In terms of perfection, signal characteristics are expected to be reliable to the extent that an ‘ideal receiver’, one suffering no perceptual impairments, can respond in a manner that on average enhances its fitness (see Johnstone & Grafen 1993). Within the realm of sexual selection, animal mating signals are expected to indicate the signaller’s phenotype with some degree of reliability. Moreover, under the various coevolutionary mechanisms of sexual selection (wherein mate choice only yields indirect, genetic benefits), mating signals are also expected to indicate the signaller’s genotype and, more critically, the phenotype of offspring that the signaller would sire. This latter expectation is most apparent in those processes

VIBRATIONAL COMMUNICATION AND REPRODUCTIVE ISOLATION IN THE ENCHENOPA BINOTATA SPECIES COMPLEX OF TREEHOPPERS (HEMIPTERA: MEMBRACIDAE)

Abstract Sexual communication can contribute to population divergence and speciation because of its effect on assortative mating. We examined the role of communication in assortative mating in the Enchenopa binotata species complex of treehoppers. These plant‐feeding insects are a well studied case of sympatric speciation resulting from shifts to novel host‐plant species. Shifting to hosts with different phenologies causes changes in life‐history timing. In concert with high host fidelity, these changes reduce gene flow between populations on ancestral and novel hosts and facilitate a rapid response to divergent natural selection. However, some interbreeding can still occur because of partial overlap of mating periods. Additional behavioral mechanisms resulting in reproductive isolation may thus be important for divergence. In E. binotata, mating pairs form after an exchange of plant‐borne vibrational signals. We used playback experiments to examine the relevance of inter‐ and intraspecific variation in male advertisement signals for female mate choice in a member of the E. binotata species complex. Female signals given in response to male signals provided a simple and reliable assay. Male species and male individual identity were important determinants of female responses. Females failed to respond to the signals of the two most closely related species in the complex, but they responded strongly to the signals of conspecific males, as well as to those of the most basal species in the complex. Communication systems in the E. binotata species complex can therefore play a role in reproductive isolation. Female responses were influenced by among‐individual variation in male signals and females, suggesting the involvement of sexual selection in the evolution of these communication systems.

Contributions of natural and sexual selection to the evolution of premating reproductive isolation: a research agenda.

Speciation by divergent natural selection is well supported. However, the role of sexual selection in speciation is less well understood due to disagreement about whether sexual selection is a mechanism of evolution separate from natural selection, as well as confusion about various models and tests of sexual selection. Here, we outline how sexual selection and natural selection are different mechanisms of evolutionary change, and suggest that this distinction is critical when analyzing the role of sexual selection in speciation. Furthermore, we clarify models of sexual selection with respect to their interaction with ecology and natural selection. In doing so, we outline a research agenda for testing hypotheses about the relative significance of divergent sexual and natural selection in the evolution of reproductive isolation.

EXPERIENCE-MEDIATED PLASTICITY IN MATE PREFERENCES: MATING ASSURANCE IN A VARIABLE ENVIRONMENT

An individuals prior experience of sexual signals can result in variation in mate preferences, with important consequences for the course of sexual selection. We test two hypotheses about the evolution of experience‐mediated plasticity in mate preferences: mating assurance and mismating avoidance. We exposed female Enchenopa binotata treehoppers (Hemiptera: Membracidae) to treatments that varied their experience of signal frequency, the most divergent sexual signal trait in the E. binotata species complex. Treatments consisted of (1) signals matching the preferred frequency, (2–3) signals deviating either 100 Hz above or 100 Hz below the preferred frequency, and (4) no signals. Females experiencing preferred signals showed the greatest selectivity. However, experience had no effect on peak preference. These results support the hypothesis that selection has favored plasticity in mate preferences that ensures that mating takes place when preferred mates are rare or absent, while ensuring choice of preferred types when those are present. We consider how experience‐mediated plasticity may influence selection on sexual advertisement signals, patterns of reproductive isolation, and the maintenance of genetic variation. We suggest that the plasticity we describe may increase the likelihood of successful colonization of a novel environment, where preferred mating types may be rare.

Plant Host Specificity Among Flower-Feeding Neotropical Drosophila (Diptera: Drosophilidae)

A study has been made of plant host specificity of flower-feeding Drosophila collected in western, central, and eastern Panama, the west coast of Colombia, Trinidad, W. I., and Leticia, Colombia, on the headwaters of the Amazon River. Three and four species of single host flower-feeding Drosophila species were found in each of two collecting areas, respectively, in central Panama. These flies were bred only from flowers of their special hosts and never from other plants in the vicinity. A fluctuation of population numbers of the drosophilid is correlated with the period of blossoming of the plant species. Monophagous flower-feeding Drosophila occupy plants with long blossoming periods of four to nine months. Other adaptations of monophagous drosophilids to the host plant concern body color and structural details of the ovipositor and egg filaments. About 5% of flies bred from flowers of plants serving monophagous Drosophila are polyphagous drosophilids; i.e., flower-feeders, ground-feeders, or fungus feeders, No evidence was found of larval competition between a monophagous Drosophila species and a polyphagous drosophilid sharing the same plant. Polyphagous flower-feeding drosophilids use a variety of host plants which generally have a short blossoming period of one to three months. These more versatile species have a wide range of distribution and include the cosmopolitan Drosophila busckii. Preferences for one plant host but tolerance for another have been found in the case of two sibling species of Drosophila using, respectively, two different members of the genus Calathea as primary hosts and each having as secondary host the primary host of its sibling Drosophila species. In addition, two monophagous flower-feeders belonging to the same species group use two different Heliconia species in the same area. In different geographical areas, a monophagous Drosophila species depends either on the same plant host or on plant species very closely related within the genus. An association of the same two distantly related host specific drosophilids in different geographical areas is presumed to have been established in the Pliocene at least, antedating the differentiation of the ancestral Heliconia into five closely related plant species. A number of polyphagous flower-feeding Drosophila species can be cultured on laboratory medium. With one exception monophagous flower-feeders on this medium either (1) refuse to oviposit, or (2) undergo a prolonged larval and pupal state and fail to eclose. It has been possible to adapt one host specific Drosophila species to laboratory culture medium.

The evolution and evolutionary consequences of social plasticity in mate preferences

In many animals, experience modifies behaviour in a variety of ways and contexts. Here we focus on experience of social environments and phenotypic plasticity in mate preferences. We first review adaptive hypotheses about the evolution of social plasticity in mate preferences, finding support for all of them across different species. We suggest that future work should assess which patterns of variation in social environments select for which forms of plasticity in mate preferences. We then highlight that social plasticity in mate preferences creates feedback loops between the role of social environments as causes of variation in phenotypes and the role of social environments as causes of selection on phenotypes. Fully understanding the consequences of these feedbacks will involve assessing both how selection shapes the plastic response to variation in social environments and how individuals in social environments are selected to influence the mate preferences of others. This task is just beginning, but we review evidence of genetic variation in both of these aspects of social plasticity in mate preferences.

Diversification under sexual selection: the relative roles of mate preference strength and the degree of divergence in mate preferences

The contribution of sexual selection to diversification remains poorly understood after decades of research. This may be in part because studies have focused predominantly on the strength of sexual selection, which offers an incomplete view of selection regimes. By contrast, students of natural selection focus on environmental differences that help compare selection regimes across populations. To ask how this disparity in focus may affect the conclusions of evolutionary research, we relate the amount of diversification in mating displays to quantitative descriptions of the strength and the amount of divergence in mate preferences across a diverse set of case studies of mate choice. We find that display diversification is better explained by preference divergence rather than preference strength; the effect of the latter is more subtle, and is best revealed as an interaction with the former. Our findings cast the action of sexual selection (and selection in general) in a novel light: the strength of selection influences the rate of evolution, and how divergent selection is determines how much diversification can occur. Adopting this view will enhance tests of the relative role of natural and sexual selection in processes such as speciation.

The evolution of experience‐mediated plasticity in mate preferences

Experience of sexual signals can alter mate preferences and influence the course of sexual selection. Here, we examine the patterns of experience‐mediated plasticity in mate preferences that can arise in response to variation in the composition of mates in the environment. We use these patterns to test hypotheses about potential sources of selection favouring experience‐mediated plasticity. We manipulated signal experience of female Enchenopa treehoppers (Hemiptera: Membracidae) in a vibrational playback experiment with the following treatments: silence; two types of non‐preferred signals; preferred signals; and a mixture of preferred and non‐preferred signals. This experiment revealed plasticity in mate preference selectivity, with greatest selectivity in the mixed signal treatment, followed by the preferred signal treatment. We found no plasticity in peak preference. These results suggest that females have been selected to adjust preference selectivity according to the variability of potential mates in their social environment, as well as to the presence/absence of preferred mates. We discuss how experience‐mediated plasticity in mate preferences can influence the strength of selection on male signals and can result in evolutionary dynamics between variation in preferences and signals that either promote the maintenance of variation or facilitate rapid trait fixation.