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• W2055904191 abstract "What is a stalk-eyed fly? Among the true flies (Diptera) are many examples of species with bizarre head projections such as antlers, eyes that project out of the head or eyes that are on stalks (Figure 1). In the Diopsid family, the exaggeration of eye-stalks can be extreme, with males having an eyespan greater than their body length. There are several hundred species in the Diopsid family, split into three genera: Diopsis, Diasemopsis and Teleopsis. Most species are found in the tropics of the Old World, though a European species was discovered recently in Hungary. Stalk-eyed flies are up to a centimetre long and have a largely terrestrial habit. Adults feed on microbes from decaying plants or animals and their larvae eat decaying vegetation. Many stalk-eyed flies exhibit sexual dimorphism for eyespan, with males having much greater eyespan than females, and this has evolved many times within the family. Members of dimorphic species tend to disperse in moist undergrowth and low vegetation during the day and roost together at night in nocturnal clusters on rootlets or leaves. In the highly dimorphic sister species Cyrtodiopsis dalmanni and C. whitei, males compete with each other to control these nocturnal aggregation sites, by literally ‘eyeing each other up’: rearing up, spreading their front legs alongside their eye stalks and trying to knock each other over. The winner takes control of rootlets where females aggregate. Most matings occur at dawn the following morning, before individuals disperse for the day. Why the interest? Stalk-eyed flies are a canonical example of sexual selection. This is because of the strong female preference for males with large eyespans, well-documented in sexually dimorphic species such as C. dalmanni and C. whitei. Females prefer to roost and to mate more frequently with large eyespan males. In contrast to many other invertebrate species, the basis of female choice is clear and amenable to experimental investigation. There is also evidence that eyespan is used as a signal in antagonistic interactions between males. Compared to a laboratory favourite such as Drosophila, stalk-eyed flies are slower growing and longer lived. But they adapt readily to laboratory culture and are ideal material for evolutionary and quantitative genetic studies. Experiments using artificial selection have revealed some very interesting findings, such as a genetic correlation between female preference and male eyespan, a pre-requisite for evolutionary change driven by sexual selection. Why large eyespan? It may seem a curious question, but why is it eyespan that is exaggerated in the stalk-eyed flies, rather than some other part of the anatomy? We don’t know the answer, but can make some suggestions. In all other Diptera, head projections are limited to males, which suggests a functional role in sexual selection. In contrast, Diopsid females also have eyestalks, and in the basal Sphyracephela group, eye-stalks are sexually monomorphic. This suggests that ecological factors specific to Diopsid flies originally drove natural selection in favour of lateral displacement of the eyes onto stalks. We don’t know the natural selective force, but it seems plausible that placing eyes on stalks may have given flies greater all round peripheral vision. Why then did sexual selection for increasing male eyespan occur? Again this is not well understood, but in the sexually monomorphic species Sphyracephela beccarii, the development of eyespan is more sensitive to environmental conditions than is true for other traits, and this elevated sensitivity may have pre-adapted eyespan to a role in signalling male condition or quality. What genetic mechanisms underlie exaggerated eyespan? Presumably the evolution of exaggerated eyespan involved changes in the action of genes or their targets that regulate head development and morphogenesis. Recent studies have shown that the expression of four key regulator genes — defective proventriculus, Distal-less, engrailed and wingless — in the imaginal discs that give rise to the head is remarkably similar in Drosophila and Diopsids during larval development. Of course, differences may arise later during metamorphosis, and this is the target for future research. What is signalled by male eyespan? There are three main ideas about what male eyespan reveals to females. The first is that it indicates male genetic quality. Male eyespan is highly condition-dependent, much more so than other traits or the unexaggerated eyespan of females, and this condition-dependence is heritable. Male genotypes of ‘high quality’ are able to express large eyespan even when resources (food available during the larval development phase) are limiting, but males with genotypes of a lower quality produce only small eyespans under such conditions. By choosing large eyespan males, females obtain males with stress-resistant genotypes, which confer heritable fitness benefits on their progeny through increased stress resistance and the elevated mating success of sons with large eyespans. The second idea is that the width of the male eyespan is genetically correlated in males with the strength of a suppressor of meiotic drive. Females of some natural populations harbour an X chromosome-linked meiotic driver, which causes all Y chromosome-bearing sperm to degenerate. Hence not only do these populations become female-biased, they may also suffer from sperm limitation. Females from such populations are presumed to benefit from the increased meiotic drive suppression conferred by males with large eyespan. These indirect genetic benefits make intuitive sense, as eyespan is fixed at eclosion and would not be predicted to be informative about adult fitness. Nevertheless, a third possibility is that large eyespan in males signals a potential direct benefit to females from elevated male fertility: there is evidence that males with large eyespan have a higher fertility than small eyespan males. Determining the relative importance of these rival explanations of the signal provided by male eyespan is a challenge for the future. Condition dependence of female mate preference? Laboratory studies have shown that the mate preference of female C. dalmanni varies according to their condition: well-fed or large females show strong preference for large eyespan males, while poorly fed or small females do not. In both experiments female fecundity was correlated with mate preference. These results have received relatively little attention. It will be important to see whether they are also true of other sexually dimorphic Diopsid species and to what extent they strengthen the force of sexual selection on male eyespan, as large eyespan males not only get more matings but also mate with the most fecund females. Why do stalk-eyed flies mate so often? Stalk-eyed flies are highly promiscuous. In C. dalmanni for example, both sexes are capable of mating extremely frequently (as often as 10 times in a morning) throughout most of their long lifespan. The reasons for this are unclear. If sperm displacement is strong — the last males to mate obtain a disproportionately high share of successful fertilisations — then males should mate often to increase their paternity. Females may tolerate frequent matings to minimise harassment (‘convenience polyandry’). This seems unlikely, however, as in at least one sexually dimorphic species (Diasemopsis meigenii) females are capable of overt and effective rejection of unwanted suitors. Another possibility is that females need to remate often to ensure adequate sperm supplies. Females of C. whitei actually store very few sperm (around 35) following a single mating, and female C. dalmanni require multiple matings to achieve high fertility. The fact that males transfer few sperm per mating is consistent with the notion that ejaculate production in males incurs significant costs. Males transfer sperm in spermatophores formed from products of the accessory glands. In C. dalmanni, the spermatophores are small relative to those of Diopsids that remate at lower frequencies. Further research on variation in both reproductive morphology and life history traits is essential. What determines male mating rate? New research is highlighting the potential importance of variation in reproductive organ size in determining the limits of male mating frequency and reproductive success. The accessory glands provide the material required to synthesise the spermatophore in which the sperm, produced by the testes, are packaged. Male mating rate is both phenotypically and genetically correlated with the size of male accessory glands, but not of the testes. Furthermore, mating causes a significant short-term decrease specifically in accessory gland size. In other Diptera, the accessory glands produce substances that alter female behaviour and physiology, as well as structural proteins that may correspond to those forming spermatophores. Current research with stalk-eyed flies is focussed on identification of accessory gland products and evaluating their role in mediating potential conflicts of interest between the sexes." @default.
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• W2055904191 date "2005-07-01" @default.
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• W2055904191 title "Stalk-eyed flies" @default.
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• W2055904191 doi "https://doi.org/10.1016/j.cub.2005.07.015" @default.
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