Multi-Species Host Use by the Parasitoid Fly Ormia lineifrons.

Antagonistic species relationships such as parasitoid/host interactions lead to evolutionary arms races between species. Many parasitoids use more than one host species, requiring the parasitoid to adapt to multiple hosts, sometimes being the leader or the follower in the evolutionary back-and-forth between species. Thus, multi-species interactions are dynamic and show temporary evolutionary outcomes at a given point in time. We investigated the interactions of the multivoltine parasitoid fly Ormia lineifrons that uses different katydid hosts for each of its fly generations sequentially over time. We hypothesized that this fly is adapted to utilizing all hosts equally well for the population to persist. We quantified and compared the fly's development in each of the four Neoconocephalus hosts. Cumulative parasitism rates ranged between ~14% and 73%, but parasitoid load and development time did not differ across host species. Yet, pupal size was lowest for flies using N. velox as a host compared to N. triops and other host species. Successful development from pupa to adult fly differed across host species, with flies emerging from N. triops displaying a significantly lower development success rate than those emerging from N. velox and the other two hosts. Interestingly, N. triops and N. velox did not differ in size and were smaller than N. robustus and N. nebrascensis hosts. Thus, O. lineifrons utilized all hosts but displayed especially low ability to develop in N. triops, potentially due to differences in the nutritional status of the host. In the multi-species interactions between the fly and its hosts, the poor use of N. triops may currently affect the fly's evolution the most. Similarities and differences across host utilization and their evolutionary background are discussed.

doublesex alters aggressiveness as a function of social context and sex in the polyphenic beetle Onthophagus taurus.

Despite sharing nearly the same genome, individuals within the same species can vary drastically in both morphology and behaviour as a function of developmental stage, sex or developmental plasticity. Thus, regulatory processes must exist that enable the stage-, sex- or environment-specific expression of traits and their integration during ontogeny, yet exactly how trait complexes are co-regulated and integrated is poorly understood. In this study, we explore the developmental genetic basis of the regulation and integration of environment-dependent sexual dimorphism in behaviour and morphology in the horn-polyphenic dung beetle Onthophagus taurus through the experimental manipulation of the transcription factor doublesex (dsx). The gene dsx plays a profound role in the developmental regulation of morphological differences between sexes as well as alternative male morphs by inhibiting horn formation in females but enabling nutrition-responsive horn growth in males. Specifically, we investigated whether experimental downregulation of dsx expression affects male and female aggressive and courtship behaviours in two social contexts: interactions between individuals of the same sex and interactions between males and females. We find that dsx downregulation significantly alters aggressiveness in both males and females, yet does so differently for both sexes as a function of social context: dsxRNAi males exhibited elevated aggression towards males but showed reduced aggression towards females, whereas dsxRNAi females became more aggressive towards males, while their aggressiveness towards other females was unaffected. Moreover, we document unexpectedly high levels of female aggression independent of dsx treatment in both wild-type and control-injected individuals. Lastly, we found no effects of dsxRNAi on courtship and mating behaviours. We discuss the role of dsx in the regulation of sex-specific and plastic behaviours, the unexpectedly high levels of aggression of hornless dsxRNAi males in relation to the well-established description of the hornless sneaker phenotype and the potential ecological function of high female aggression.

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.

A combination of developmental plasticity, parental effects, and genetic differentiation mediates divergences in life history traits between dung beetle populations.

The dung beetle, Onthophagus taurus, was introduced <50 years ago from its native Mediterranean range into Western Australia (WA) and the Eastern United States (EUS). The intensity of intra- and interspecific competition for dung as a breeding resource is substantially higher in WA. First, we tested whether differential resource competition in the two exotic ranges is associated with divergences in life history traits, which impact on resource use. We predicted that high levels of resource competition in WA should favor females that produce brood balls more efficiently and of altered size, and produce offspring more readily when a breeding opportunity arises. Furthermore, we predicted that larvae from WA populations may have evolved more efficient development and thus exhibit higher eclosion success, shorter development time, and altered body size under standardized conditions. Second, we examined the likely developmental mechanisms underlying these divergences, that is, genetic differentiation, developmental plasticity, or parental effects in a common garden experiment. Field-collected EUS and WA populations significantly differed, as predicted, in most of the traits examined. However, these differences are facilitated by a complex combination of proximate mechanisms. Developmental plasticity and (grand) parental effects mediated differences related to reproductive performance, whereas genetic differentiation mediated differences in the duration of larval development. Our study highlights that population divergences can be the product of a patchwork of proximate mechanisms, with each mechanism adjusting different traits in a way that the resulting composite phenotype may be better suited to its competitive environment.

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.

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.

Eavesdropping parasitoids do not cause the evolution of less conspicuous signalling behaviour in a field cricket.

Males of many species produce conspicuous mating signals to attract females, but these signals can also attract eavesdropping predators and parasites. Males are thus expected to evolve signalling behaviours that balance the sexual selection benefits and the natural selection costs. In the variable field cricket, Gryllus lineaticeps, males sing to attract females, but these songs also attract the lethal parasitoid fly Ormia ochracea. The flies use male crickets as hosts for their larvae, primarily search for hosts during a 2 h period following sunset and prefer the same song types as female crickets. We tested whether males from high-risk populations reduce the risk of parasitism by singing less frequently or by shifting their singing activity to a time of the night when the risk of parasitism is low. We compared male singing activity and its temporal pattern between six high-risk and six low-risk populations that were reared in a common environment. There was no effect of parasitism risk on either total male singing activity or the temporal pattern of male singing activity. Males from high-risk populations thus sang as frequently as males from low-risk populations. These results suggest that sexual selection on male singing behaviour may be substantially stronger in high-risk populations than in low-risk populations. It is possible that other traits may have evolved to reduce parasitism risk without compromising mate attraction.

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

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.

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 degrees C, whereas the slower winter call was attractive only at 20 degrees 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.

Phonotaxis in Hyla versicolor (Anura, Hylidae): the effect of absolute call amplitude.

The influence of call amplitude on phonotaxis in female Hyla versicolor was studied using a no-choice paradigm. One set of experiments estimated effects of stimulus amplitude on phonotaxis toward a synthetic model of a conspecific call. The response strength increased with amplitude from the behavioral threshold (37-43 dB SPL) up to 79 dB SPL and then decreased at higher amplitudes. Females approached the loudspeaker with short walking bouts (approximately 1 s duration) occurring immediately after call presentations. Increase in response strength was attributed to an increasing proportion of calls that elicited such walking bouts, whereas the decrease at high amplitudes resulted from decreasing distance covered per bout. The quality of orientation remained constant for all above-threshold amplitudes. A second set of experiments tested the selectivity for interval duration and pulse duration at amplitudes of 55, 70, and 85 dB SPL. Selectivity for both parameters was similar at 70 and 85 dB SPL, but tended to increase at 55 dB SPL. The results suggest that selective phonotaxis in H. versicolor is not adapted for long-distance communication. This finding differs from those of comparable studies of acoustic insects.