Oliver M. Beckers

Mate sampling strategy in a field cricket: evidence for a fixed threshold strategy with last chance option

The strategy females use to sample potential mates can influence mate choice and thus sexual selection. We examined the mate sampling strategy of the cricket Gryllus lineaticeps. In our first set of experiments, we simultaneously presented three different chirp rates to females. The set consisted of three trials, each covering a different range of chirp rates. Independent of chirp rate range, female G. lineaticeps preferred rates that were above 3.0 chirps/s to rates that were below 3.0 chirps/s. Females did not discriminate among chirp rates that were below this threshold and did not discriminate among chirp rates that were above this threshold, suggesting that they express a fixed threshold sampling strategy. In our second experiment, females were presented sequentially with a fast chirp rate and then a slow chirp rate. When the interval between presentations was 20 min, females showed significantly weaker responses to the slow rate than to the fast rate. However, when the interval between presentations was 24 h, female responses to the slow and fast rate did not significantly differ. The latter result suggests that females lower their threshold of acceptance when they have not recently experienced highly attractive song types. This lower acceptance threshold is probably adaptive, as it would allow females to avoid paying high search costs, and to reproduce, only when low-quality males are available. Our results are consistent with a rarely considered sampling strategy (fixed threshold with last chance option strategy) and highlights the importance of the timing of social experience for mate sampling.

Developmental plasticity of mating calls enables acoustic communication in diverse environments

Male calls of the katydid Neoconocephalus triops exhibit substantial developmental plasticity in two parameters: (i) calls of winter males are continuous and lack the verse structure of summer calls and (ii) at equal temperatures, summer males produce calls with a substantially higher pulse rate than winter males. We raised female N. triops under conditions that reliably induced either summer or winter phenotype and tested their preferences for the call parameters that differ between summer and winter males. Neither generation was selective for the presence of verses, but females had strong preferences for pulse rates: only a narrow range of pulse rates was attractive. The attractive ranges did not differ between summer and winter females. Both male pulse rate and female preference for pulse rate changed with ambient temperature, but female preference changed more than the male calls. As a result, the summer call was attractive only at 25°C, whereas the slower winter call was attractive only at 20°C. Thus, developmental plasticity of male calls compensates for differences in temperature dependency between calls and preferences and enables the communication system to function in heterogeneous environments. The potential role of call plasticity during the invasion of new habitats is discussed.

A complex mechanism of call recognition in the katydid Neoconocephalus affinis (Orthoptera: Tettigoniidae)

SUMMARY Acoustic pattern recognition is important for bringing together males and females in many insect species. We used phonotaxis experiments on a walking compensator to study call recognition in the katydid Neoconocephalus affinis, a species with a double-pulsed call and an atypically slow pulse rate for the genus. Call recognition in this species is unusual because females require the presence of two alternating pulse amplitudes in the signal. A Fourier analysis of the stimulus-envelopes revealed that females respond only when both the first and second harmonics of the AM spectrum are of similar amplitude. The second harmonic is generated by the amplitude difference between the two pulses making up a pulse-pair. Females respond to double pulses that have been merged into a single pulse only if this amplitude modulation is preserved. Further experiments suggest that females use a resonance mechanism to recognize the pulse rate of the call, supporting a neural model of rate recognition in which periodic oscillations in membrane potential are used to filter the pulse rate of the signal. Our results illustrate how a reduction in pulse rate extends the opportunities for females to evaluate fine-scale temporal properties of calls, and provide further evidence for the importance of oscillatory membrane properties in temporal processing. The results are discussed with regard to evolutionary changes in call recognition mechanisms within the genus.

Tradeoffs limit the evolution of male traits that are attractive to females

Tradeoffs occur between a variety of traits in a diversity of organisms, and these tradeoffs can have major effects on ecological and evolutionary processes. Far less is known, however, about tradeoffs between male traits that affect mate attraction than about tradeoffs between other types of traits. Previous results indicate that females of the variable field cricket, Gryllus lineaticeps, prefer male songs with higher chirp rates and longer chirp durations. In the current study, we tested the hypothesis that a tradeoff between these traits affects the evolution of male song. The two traits were negatively correlated among full-sibling families, consistent with a genetically based tradeoff, and the tradeoff was stronger when nutrients were limiting. In addition, for males from 12 populations reared in a common environment, the traits were negatively correlated within populations, the strength of the tradeoff was largely invariant across populations, and the within-population tradeoff predicted how the traits have evolved among populations. A widespread tradeoff thus affects male trait evolution. Finally, for males from four populations assayed in the field, the traits were negatively correlated within and among populations. The tradeoff is thus robust to the presence of environmental factors that might mask its effects. Together, our results indicate there is a fundamental tradeoff between male traits that: (i) limits the ability of males to produce multiple attractive traits; (ii) limits how male traits evolve; and (iii) might favour plasticity in female mating preferences.

Beetle horns and horned beetles: emerging models in developmental evolution and ecology

Many important questions in developmental biology increasingly interface with related questions in other biological disciplines such as evolutionary biology and ecology. In this article, we review and summarize recent progress in the development of horned beetles and beetle horns as study systems amenable to the integration of a wide range of approaches, from gene function analysis in the laboratory to population ecological and behavioral studies in the field. Specifically, we focus on three key questions at the current interface of developmental biology, evolutionary biology and ecology: (1) the developmental mechanisms underlying the origin and diversification of novel, complex traits, (2) the relationship between phenotypic diversification and the diversification of genes and transcriptomes, and (3) the role of behavior as a leader or follower in developmental evolution. For each question we discuss how work on horned beetles is contributing to our current understanding of key issues, as well as highlight challenges and opportunities for future studies. WIREs Dev Biol 2013, 2:405–418. doi: 10.1002/wdev.81

Parasitoid infestation changes female mating preferences

Females often adjust their mating preference to environmental and social conditions. This plasticity of preference can be adaptive for females and can have important consequences for the evolution of male traits. While predation and parasitism are widespread, their effects on female preferences have rarely been investigated. Females of the cricket Gryllus lineaticeps are parasitized by the parasitoid fly Ormia ochracea. Infestation with fly larvae substantially reduces female life span and thus reproductive opportunities of the cricket. Both female G. lineaticeps and flies orient to male song and both prefer male songs with faster chirp rates to songs with slower chirp rates. We tested the effect of parasitic infestation on female responsiveness to male song and female chirp rate preferences. The proportion of individuals responding to male songs did not differ between infested and control females. Control females preferred intermediate chirp rates to slow chirp rates and did not discriminate between fast and intermediate chirp rates. In contrast, infested females showed no preferences in the choice trials, indicating reduced chirp rate selectivity. This plasticity in female preferences may be adaptive; parasitized females may have a higher probability of reproducing before they are killed by the parasitoids if they are less selective (i.e. there will be a larger pool of males considered acceptable). The change in preferences suggests relaxed selection on male chirp rate during times of parasitism.

Divergent Preferences for Song Structure between a Field Cricket and its Phonotactic Parasitoid

In many animals, males produce signals to attract females for mating. However, eavesdropping parasites may exploit these conspicuous signals to find their hosts. In these instances, the strength and direction of natural and sexual selection substantially influence song evolution. Male variable field crickets, Gryllus lineaticeps, produce chirped songs to attract mates. The eavesdropping parasitoid fly Ormia ochracea uses cricket songs to find its hosts. We tested female preferences for song structure (i.e., chirped song vs. trilled song) in crickets and flies using choice experiments. Female crickets from a parasitized and a non-parasitized population significantly preferred the species-typical chirped song, whereas flies significantly preferred a trilled song, which is expressed by other hosts in different regions. Sexual selection due to female choice and natural selection due to fly predation both appear to favor the chirped song structure of G. lineaticeps in the parasitized population, whereas sexual selection favors the chirped structure in the non-parasitized population.

Differentiation of ovarian development and the evolution of fecundity in rapidly diverging exotic beetle populations

Fecundity is a fundamental determinant of fitness, yet the proximate developmental and physiological mechanisms that enable its often rapid evolution in natural populations are poorly understood. Here, we investigated two populations of the dung beetle Onthophagus taurus that were established in exotic ranges in the early 1970s. These populations are subject to drastically different levels of resource competition in the field, and have diverged dramatically in female fecundity. Specifically, Western Australian O. taurus experience high levels of resource competition, and exhibit greatly elevated reproductive output compared to beetles from the Eastern US, where resource competition is minimal and female fecundity is low. We compared patterns of ovarian maturation, relative investment into and timing of egg production, and potential trade-offs between ovarian investment and the duration of larval development and adult body size between populations representative of both exotic ranges. We found that the rapid divergence in fecundity between exotic populations is associated with striking differences in several aspects of ovarian development: (1) Western Australian females exhibit accelerated ovarian development, (2) produce more eggs, (3) bigger eggs, and (4) start laying eggs earlier compared to their Eastern US counterparts. At the same time, divergence in ovarian maturation patterns occurred alongside changes in (5) larval developmental time, and (6) adult body size, and (7) mass. Western Australian females take longer to complete larval development and, surprisingly, emerge into smaller yet heavier adults than size-matched Eastern US females. We discuss our results in the context of the evolutionary developmental biology of fecundity in exotic populations.

Male field crickets infested by parasitoid flies express phenotypes that may benefit the parasitoids

Parasites can cause changes in the phenotypes of their hosts that may benefit the parasite, the host, or both. To understand the evolutionary dynamics of host–parasite interactions it is necessary to first examine the effect of parasitic infestation on the host phenotype and whether the host or parasite benefits from these changes. The fly Ormia ochracea parasitizes the variable field cricket, Gryllus lineaticeps, and it uses male song to locate hosts for its lethal larvae. Adult flies preferentially orient to male songs with faster and longer chirps. We tested the effect of larval infestation on two types of host traits. First, we tested whether infestation affects male singing activity and song characters. Infested males were significantly less likely to sing than noninfested males, and when they did sing, they sang less frequently. Infestation thus reduced a male’s ability to attract mates, which may benefit the parasitoid if mating activity increases predation, superparasitism and/or energetic costs for their hosts. No song character we measured, however, differed between infested and noninfested males. Second, we tested whether infestation affects host mass. Infested males gained more mass than noninfested males, which was not explained by the reduced singing of infested males. Importantly, parasitoids that developed in males that gained more mass were heavier as pupae, which may increase their viability and reproductive success as adults. These changes in the host may be beneficial side-effects of the pathology of parasitism, the result of a host-compensatory response, or the result of host manipulation by the parasitoid.

Female adaptation to developmental plasticity in male calling behavior

The katydid Neoconocephalus triops exhibits in North America substantial developmental plasticity of male mating calls. The AM rate of the summer calls is significantly faster than that of the winter calls at the same temperature. In the tropics, where N. triops originated, males express only the fast summer-call phenotype. We tested two alternative hypotheses: (1) call plasticity in the population from North America evolved in response to selection by female preference after N. triops colonized North America, or (2) call plasticity evolved before N. triops expanded into North America and its expression in the novel environment led to adaptive change of female preferences. First, we tested whether call plasticity was present in tropical populations of N. triops. Tropical males expressed the winter-call phenotype when reared under winter conditions, indicating that call plasticity did not evolve in response to temperate climates. Second, we compared female preferences among temperate and tropical populations. We found that the temperature dependence of preferred AM rate was significantly steeper in temperate N. triops than in a tropical population of N. triops. Third, we compared temperature dependence of female preference of the N. triops populations to three Neoconocephalus species without call plasticity. Only temperate N. triops had significantly steeper temperature dependence than the other species. This steeper temperature dependence matched female preference to the fast summer call at high temperatures and to the slow winter call at low temperatures in temperate populations. These results support the hypothesis that female preference changed in N. triops in North America to compensate for the plasticity of male calls.