Gerlind U. C. Lehmann

Spermatophore characteristics in bushcrickets vary with parasitism and remating interval

Abstract Male bushcrickets provide females with a nuptial gift, a spermatophore, which is transferred to females at mating. The spermatophore consists of a gelatinous mass, the spermatophylax, and the sperm-containing ampulla. Male spermatophore size is positively correlated with insemination rate and female refractory period and therefore with male reproductive success. In this study, we examined spermatophylax weight, ampulla weight and sperm number in males of Poecilimon mariannae parasitized by the acoustically orienting fly Therobia leonidei. We show that in parasitized males, spermatophylax weight decreases with the level of parasitism. In line with the hypothesis that parasitism is a cost to reproduction, we found that spermatophylax weight was reduced at remating. In contrast, the replenishment of the spermatophylax in unparasitized males was complete after 2 days and was increased no further after 3 days. Both sperm number and ampulla weight showed an increase over time since last mating and sperm production was estimated at a constant rate of 500,000 per day in all individuals, regardless of parasitism. The allocation of investment in components of the spermatophore varies greatly with parasitism and remating. Both factors had rather independent effects on spermatophore constitution, revealing functional constraints acting on spermatophore characteristics in bushcrickets, which are important for understanding the selection pressures working on its components.

Review of Biogeography, Host Range and Evolution of Acoustic Hunting in Ormiini (Insecta, Diptera, Tachinidae), Parasitoids of Night-calling Bushcrickets and Crickets (Insecta, Orthoptera, Ensifera)

Abstract Interest in parasitoids has grown with the recognition that host-parasitoid systems offer opportunities to examine fundamental questions in behavioural and evolutionary ecology. Tachinid flies of the Ormiini possess a conspicuously inflated prosternal region, enabling them to detect the mating songs of their hosts. This speciality makes them a highly suitable group for studies of adaptive radiation. To emphasise further research in this important group of parasitoids, their biogeography and host species are summarised. The Ormiini are a particularly small group, containing only 68 described species of predominantly tropical, especially neotropical forms. A table of host-parasitoid relations reveals that predominant parasitism is of bushcrickets. The exploitation of cricket songs appears to be a derived pattern that evolved as a host switch some time after the Eocene. Hypotheses concerning fly-host coevolution and the reasons for the development of hearing are discussed, and include the question of mate finding and avoidance of bats as predators.

Weighing costs and benefits of mating in bushcrickets (Insecta: Orthoptera: Tettigoniidae), with an emphasis on nuptial gifts, protandry and mate density.

Sexual selection is a major force driving evolution and is intertwined with ecological factors. Differential allocation of limited resources has a central role in the cost of reproduction. In this paper, I review the costs and benefits of mating in tettigoniids, focussing on nuptial gifts, their trade-off with male calling songs, protandry and how mate density influences mate choice. Tettigoniids have been widely used as model systems for studies of mating costs and benefits; they can provide useful general insights. The production and exchange of large nuptial gifts by males for mating is an important reproductive strategy in tettigoniids. As predicted by sexual selection theory spermatophylax size is condition dependent and is constrained by the need to invest in calling to attract mates also. Under some circumstances, females benefit directly from the nuptial gifts by an increase in reproductive output. However, compounds in the nuptial gift can also benefit the male by prolonging the period before the female remates. There is also a trade-off between adult male maturation and mating success. Where males mature before females (protandry) the level of protandry varies in the direction predicted by sperm competition theory; namely, early male maturation is correlated with a high level of first inseminations being reproductively successful. Lastly, mate density in bushcrickets is an important environmental factor influencing the behavioural decisions of individuals. Where mates are abundant, individuals are more choosey of mates; when they are scarce, individuals are less choosey. This review reinforces the view that tettigoniids provide excellent models to test and understand the economics of matings in both sexes.

Bushcricket song as a clue for spermatophore size

Bushcricket males of Poecilimon zimmeri transfer large and protein-rich spermatophores during mating, which females directly ingest. There is correlational evidence that heavier males transfer larger nuptial gifts. In no-choice mating trials, females mated randomly with respect to male’s body weight. In contrast, in two-choice mating trials, female bushcrickets exhibit clear choice for the heavier male. This heavier male advantage was also found in pre-mating choice during phonotaxis. With manipulated mute males, females mated at random with regard to body weight of the competitors. The number of physical encounters between a female and males was low in all tests with a single male (no choice) and greater in choice-tests with two competing males. The latencies to mate also differed significantly between treatments. The time mating pairs spent in precopula was short in experiments where the males could hear rivals and significantly longer in all other tests using either a single male or mute males. Thus, acoustic signalling in male bushcrickets seems to signal male body weight. A preference for heavier males may reflect a female’s preference for a larger spermatophore and therefore a greater direct benefit.

Emerging issues in the evolution of animal nuptial gifts.

Uniquely positioned at the intersection of sexual selection, nutritional ecology and life-history theory, nuptial gifts are widespread and diverse. Despite extensive empirical study, we still have only a rudimentary understanding of gift evolution because we lack a unified conceptual framework for considering these traits. In this opinion piece, we tackle several issues that we believe have substantively hindered progress in this area. Here, we: (i) present a comprehensive definition and classification scheme for nuptial gifts (including those transferred by simultaneous hermaphrodites), (ii) outline evolutionary predictions for different gift types, and (iii) highlight some research directions to help facilitate progress in this field.

Female bushcrickets fuel their metabolism with male nuptial gifts

In many arthropods, such as bushcrickets, males donate protein-rich nuptial gifts—so-called spermatophores—to females, which females ingest while the sperm enter the females reproductive tract. Previously, it was shown that females route spermatophore nutrients over the course of hours and days to egg production or body synthesis. We investigated whether female bushcrickets fuel their metabolism with spermatophores immediately after consumption. We fed two male groups diets that were either enriched or depleted in 13C, and then tracked the isotopic changes in exhaled breath in female bushcrickets after spermatophore consumption. Within 3 hours, the stable carbon isotope ratio (δ13C) of female breath converged on the ratio of the male donor of the nuptial gift. This supports the idea that females quickly routed nutrients to metabolism, receiving immediate benefits from spermatophore feeding.

Listening when there is no sexual signalling? Maintenance of hearing in the asexual bushcricket Poecilimon intermedius.

Unisexual reproduction is a widespread phenomenon in invertebrates and lower vertebrates. If a former sexual reproducing species becomes parthenogenetic, we expect traits that were subject to sexual selection to diminish. The bushcricket Poecilimon intermedius is one of the few insect species with obligate but diploid parthenogenetic reproduction. We contrasted characters that are involved in mating in a sexually sibling species with the identical structures in the parthenogenetic P. intermedius. Central for sexual communication are male songs, while receptive females approach the males phonotactically. Compared to its sister-species P. ampliatus, the morphology of the hearing organs (acoustic spiracle, crista acustica) and the function of hearing (acoustic threshold) are reduced in P. intermedius. Nonetheless, hearing is clearly maintained in the parthenogenetic females. Natural selection by acoustic hunting bats, pleiotropy or a developmental trap may explain the well maintained hearing function.

Variation in body size among populations of the bushcricket Poecilimon thessalicus (Orthoptera: Phaneropteridae): an ecological adaptation

Abstract We analyzed geographical variation in body size in males and females of nine Greek populations of the bushcricket Poecilimon thessalicus Brunner von Wattenwyl, 1891. We found significant geographic variability in P. thessalicus, with all three morphometric body-size characters (hind femur, front tibia, and pronotum) highly correlated within populations. Populations differed in mean size between three mountain ranges, and were larger on moist eastern, than on dry western slopes. We suggest that the observed smaller size of the bushcrickets on western slopes is mainly the consequence of a shorter growing season due to summer drying on western slopes. Sex-specific growth rates might contribute to the observed smaller body size in males in all populations. Renschs rule that sexual size dimorphism (SSD) decreases as body size increases is supported, with males growing relatively larger compared to females in populations with larger body sizes. This pattern might be sexually selected, as males that produce larger nuptial gifts are favored as mates in Poecilimon bushcrickets.

Spatial organization of tettigoniid auditory receptors: Insights from neuronal tracing

The auditory sense organ of Tettigoniidae (Insecta, Orthoptera) is located in the foreleg tibia and consists of scolopidial sensilla which form a row termed crista acustica. The crista acustica is associated with the tympana and the auditory trachea. This ear is a highly ordered, tonotopic sensory system. As the neuroanatomy of the crista acustica has been documented for several species, the most distal somata and dendrites of receptor neurons have occasionally been described as forming an alternating or double row. We investigate the spatial arrangement of receptor cell bodies and dendrites by retrograde tracing with cobalt chloride solution. In six tettigoniid species studied, distal receptor neurons are consistently arranged in double‐rows of somata rather than a linear sequence. This arrangement of neurons is shown to affect 30–50% of the overall auditory receptors. No strict correlation of somata positions between the anterio‐posterior and dorso‐ventral axis was evident within the distal crista acustica. Dendrites of distal receptors occasionally also occur in a double row or are even massed without clear order. Thus, a substantial part of auditory receptors can deviate from a strictly straight organization into a more complex morphology. The linear organization of dendrites is not a morphological criterion that allows hearing organs to be distinguished from nonhearing sense organs serially homologous to ears in all species. Both the crowded arrangement of receptor somata and dendrites may result from functional constraints relating to frequency discrimination, or from developmental constraints of auditory morphogenesis in postembryonic development. J. Morphol.

Potential lifetime reproductive success of male bushcrickets parasitized by a phonotactic fly

Males of the bushcricket Poecilimon mariannae are parasitized by the acoustically orienting fly Therobia leonidei. Developing fly larvae reduce male bushcricket survival and reproductive effort. We estimated potential lifetime reproductive success (PLRS) of male bushcrickets to investigate the likely costs of this parasitism. Our analysis explored the relative reduction in PLRS caused by parasitoid infection by examining effects on survival, calling attractiveness and spermatophylax size. We also incorporated nonparasitoid-related mortality. Parasitized males lost 42% of their PLRS compared to nonparasitized males. The shortened life span after parasitism accounted for half of the PLRS reduction. Decreased spermatophylax production also had a major effect on PLRS, while decreased calling attractiveness had a smaller effect. This fitness loss was context dependent and changed with extrinsic nonparasitoid-related mortality. If nonparasitoid-related mortality was high, the selection on host males to avoid parasitism was weak; if it was low, parasitized males lost a considerable amount of reproductive opportunities compared with unparasitized males.