A fungal parasite selects against body size but not fluctuating asymmetry in Swiss subalpine yellow dung flies

Evidence for selective disadvantages of large body size remains scarce in general. Previous studies of the yellow dung fly Scathophaga stercoraria have demonstrated strong positive sexual and fecundity selection on male and female size. Nevertheless, the body size of flies from a Swiss study population has declined by ~10% 1993–2009. Given substantial heritability of body size, this negative evolutionary response of an evidently positively selected trait suggests important selective factors being missed. An episodic epidemic outbreak of the fungus Entomophthora scatophagae permitted assessment of natural selection exerted by this fatal parasite. Fungal infection varied over the season from ~50% in the cooler and more humid spring and autumn to almost 0% in summer. The probability of dying from fungal infection increased with adult fly body size. Females never laid any eggs after infection, so there was no fungus effect on female fecundity beyond its impact on mortality. Large males showed their typical mating advantage in the field, but this positive sexual selection was nullified by fungal infection. Mean fluctuating asymmetry of paired appendages (legs, wings) did not affect the viability, fecundity or mating success of yellow dung flies in the field. This study documents rare parasite-mediated disadvantages of large-sized flies in the field. Reduced ability to combat parasites such as Entomophthora may be an immunity cost of large body size in dung flies, although the hypothesized trade-off between fluctuating asymmetry, a presumed indicator of developmental instability and environmental stress, and immunocompetence was not found here

Environmental influences on the gametic investment of yellow dung fly males

The energetic investment per spermatozoon and in spermatogenesis is central to a male's reproductive strategy. Relatively little, however, is known about environmental influences on variation in male allocation decisions and associated trade-offs. Plasticity in sperm length and testis size in response to variable food and temperature conditions either before or after adult eclosion was investigated in Scathophaga stercoraria, a classic model organism for sperm competition. Both measures showed interesting and clear environmental effects and also a heritable component. Testis length, and thus presumably sperm production, showed a hypoallometric (b < 1), but non-linear increase with body size, indicating that the allometric relationship changed with size. Like body size, testis length decreased with increasing developmental temperatures, but also showed a complex cubic relationship with adult temperatures. In contrast, sperm length increased or showed a negative quadratic relationship with increasing temperatures. The increase of within-male variation in sperm length with increasing developmental temperature and decreasing adult food indicates that some of our treatments were stressful. Nevertheless, there was no evidence of a trade-off between testis size and sperm length. The missing effect of adult or larval food availability on testis and sperm length, despite strong effects of larval food on body size, suggests that investment into reproduction is less sensitive to food restriction than investment into growt

Energetic underpinnings of yellow dung fly mating success in the field

Foraging provides the basis for animal reproduction, but requires energy and time to be sustained, entailing a trade-off. Whereas females should maximize their time foraging for resources, males should minimize their foraging time by optimizing time budgets to maximize their access to mating partners. Mark-resight field studies are difficult and hence uncommon for small insects. Yellow dung flies (Scathophaga stercoraria L.) abound on pastures in cold-temperate regions across the northern hemisphere. Adult flies lick nectar from flowers for energy, but require small insect prey to produce eggs and sperm. Males wait for females around fresh cow dung, but at one point also need to replenish their energy and/or sperm reserves in the surrounding vegetation. Their foraging time budgets should depend on their body size, nutritional energy reserves, availability of sperm, competitor and female density. Marked male dung flies whose nutritional status was experimentally manipulated – water only (null control); water + sugar (energy replenishment); or water, sugar + Drosophila prey (energy and sperm replenishment) – were repeatedly observed on an experimental pasture for an entire day. Both nutrient types were expected to increase the mating success of especially large males. The total number of resighted males seen copulating was lowest for water-treated flies. Mating success was positively related to body size. The distance travelled between dung pats was greater for males fed sugar or prey and also increased with body size, while pat residence times decreased with size. No differences were found between the sugar- and prey-fed groups. Crucially however, there was no evidence in the field for a time budget or mating advantage of small males when nutrients were limited. Key Words body size, energy reserves, field observations, food manipulation, foraging, mating success, Scathophaga stercoraria, reproductio

Bergmann and Converse Bergmann Latitudinal Clines in Arthropods: Two Ends of a Continuum?

Two seemingly opposite evolutionary patterns of clinal variation in body size and associated life history traits exist in nature. According to Bergmann's rule, body size increases with latitude, a temperature effect. According to the converse Bergmann rule, body size decreases with latitude, a season length effect. A third pattern causally related to the latter is countergradient variation, whereby populations of a given species compensate seasonal limitations at higher latitudes by evolving faster growth and larger body sizes compared to their low latitude conspecifics. We discuss these patterns and argue that they are not mutually exclusive because they are driven by different environmental causes and proximate mechanisms; they therefore can act in conjunction, resulting in any intermediate pattern. Alternatively, Bergmann and converse Bergmann clines can be interpreted as over- and undercompensating countergradient variation, respectively. We illustrate this with data for the wide-spread yellow dung fly, Scathophaga stercoraria (Diptera: Scathophagidae), which in Europe shows a Bergmann cline for size and a converse Bergmann cline (i.e., countergradient variation) for development time. A literature review of the available evidence on arthropod latitudinal clines further shows a patterned continuum of responses. Converse Bergmann clines due to end-of-season time limitations are more common in larger species with longer development times. Our study thus provides a synthesis to the controversy about the importance of Bergmann's rule and the converse Bergmann rule in natur

The quantitative genetics of two life history trade-offs in the yellow dung fly in abundant and limited food environments

The trade-offs between body size and development time and between egg size and egg number (clutch size) are central to life history theory, but evidence for them, particularly in terms of genetic correlations, is equivocal. For the yellow dung fly Scathophaga stercoraria (Diptera: Scathophagidae), we investigated variation in phenotypic and genetic variances and covariances, i.e. heritabilities and genetic correlations, of these life history traits (plus diapause) in benign and stressful larval field or adult laboratory food environments. We found both trade-offs to be weak, as evidenced by low phenotypic and genetic correlations, but stronger in the food limited environments. Broad sense heritabilities were generally significant for all traits considered, whereas the narrow sense heritabilities for egg and clutch size were nil. With regard to the question of how environmental stress affects heritabilities, we found a whole range of responses within one single species depending on the traits considered. All three possible patterns occurred, i.e. increased h2 due to increased VG or decreased $$V_{P^{\prime}}$$ decreased h2 due to increased $$V_{P^{\prime}}$$ and no change in h2 due to increased VG and VP. These can be explained by the particular ecological circumstances yellow dung flies face in their natural environment. Nevertheless, the majority of patterns was consistent with the idea that stressful conditions amplify phenotypic differences between genotypes. Such variable responses of traits even within one organism underscores the complexity of this issue and may well explain the multiple patterns found in various organism

Are yellow dung flies domesticated cow dung specialists?

The theory of niche differentiation implies some extent of specialization of species with regard to key resources, notably food. Coprophagous (dung-eating) insect larvae play a critical role in the decomposition of livestock dung in modern and traditional agricultural grasslands. The yellow dung fly (Scathophaga stercoraria L.; Diptera: Scathophagidae) is one of the largest, most common and abundant dung decomposers on pastures in cold-temperate regions across the entire northern hemisphere. As this fly is often associated with domesticated cattle or dairy cows, which are commonly kept for human nutrition worldwide (beef, milk, cheese, etc.), it is sometimes suspected to be a cow dung specialist. However, yellow dung flies are regularly active on and around other dung types, and must have reproduced on dung of wild vertebrates before the domestication of cattle. We therefore experimentally studied the performance of yellow dung fly larvae on dung of various large domestic vs. wild mammals (cow, horse, wild boar, red deer) in the laboratory in Switzerland. Larval performance in terms of juvenile survival, egg-to-adult development time, growth rate, and final adult body size, the major life history indicators of individual reproductive success, did not vary greatly among the various dung types tested. Thus, yellow dung flies can successfully reproduce on multiple types of mammal (vertebrate) dung, wild and domestic, and are therefore dung generalists rather than specialists. We conclude that yellow dung flies are common in European low- and highlands because they could plastically shift to dung of common herbivorous livestock after their domestication without losing the ability to reproduce on dung of common wild mammals

Heritability of three condition surrogates in the yellow dung fly

Condition capture has been proposed as a general mechanism maintaining additive genetic variation, Va, in sexually selected traits under directional selection. It relies on two main assumptions: condition-dependent trait expression and Va in condition. Although there is evidence for the former, direct evidence that condition is heritable is scarce, although this is a requirement of most models of handicap sexual selection. We used a parent-offspring, full-sib, two-container laboratory breeding design in the yellow dung fly Scathophaga stercoraria to demonstrate the broad- and narrow-sense heritability of three surrogates of condition commonly used in sexual selection studies: lipid and glycogen reserves (i.e., physiological condition), body size, and fluctuating asymmetry. All three measures are nutrition dependent and have been linked to sexual selection in free-living yellow dung flies. While lipid reserves and body size were heritable, asymmetry and glycogen reserves were not. Moreover, the evolvability of physiological condition was higher than that of the other two traits. Of the three surrogates, physiological condition is most akin to the original definition, but all have their limitations. We conclude that condition is a useful heuristic concept in evolutionary ecology, but its practical value may be limited by the fact that it cannot be measured directl

Mate Choice and Toxicity in Two Species of Leaf Beetles with Different Types of Chemical Defense

Evidence for the use of defensive compounds for sexual purposes is scarce, even though sexual selection might have some importance for the evolution of defensive traits. This study investigates the effect of defense-related traits and body size on mating success in two sister species of leaf beetle differing in their type of chemical defense. Oreina gloriosa produces autogenous cardenolides, whereas O. cacaliae sequesters pyrrolizidine alkaloids from its food plant. Larger O. gloriosa males with more toxin or higher toxin concentration had a mating advantage, likely due to direct or indirect female choice. In the laboratory, particular pairings recurred repeatedly in this species, indicating mate fidelity. O. gloriosa females were also subject to sexual selection, possibly by male choice, because larger females and those with higher toxin concentration mated more readily and more often. In O. cacaliae, in contrast, sexual selection for toxicity and body size was not detected, or at best was much weaker. Because toxicity is heritable in O. gloriosa but environment-dependent in O. cacaliae, individuals of the former species could be choosing well-defended partners with "good genes.” Our study suggests that sexual selection may contribute to the maintenance of heritable defensive trait

Taxonomic resolution and treatment effects – alone and combined – can mask significant biodiversity reductions

Taxonomic resolution or uncertainty poses an important problem in biodiversity research. Assessment of biodiversity at the species level is most informative and preferred, but requires effort and expertise. Alternatively, researchers often bin species into higher taxa because they are unable to recognize them, or to save money and time. Here we analyse, by simulation and analytical modelling, the combined effects of dose-dependent mortality and taxonomic binning on biodiversity indices for a fictitious community of organisms. We asked (1) how binning species in a sample into higher taxa significantly affects biodiversity measures, and (2) whether dose-dependent mortality effects, alone or in combination with taxonomic uncertainty, are duly captured by classic biodiversity indices. Our study shows that haphazard binning into various taxonomic levels is legitimate and preferable to orderly binning (all taxa binned at the same level), because it provides the best resolution. We further show that binning will regularly obscure statistical detection of biodiversity differences, if only due to scaling of mean and variance. Also, treatment effects in combination with taxonomic uncertainty can introduce estimation biases of at times complex nonlinear and non-intuitive nature under any taxonomic resolution scenario, potentially including relative increases in the biodiversity index when intuitively decreases would be expected. We recommend being specific about the expected qualitative and quantitative effects of any treatment or natural comparison before formulating a hypothesis regarding biodiversity reductions. Our theoretical study should aid in this endeavour

The effect of female arrivals on mate monopolization in the yellow dung fly

The degree of resource monopolization relates to the distribution of resources in space and time. In general, monopolization is predicted to be high when resources (food or mates) are clumped in space, dispersed in time, and predictable in space or time. Using the yellow dung fly, Scathophaga stercoraria (Diptera: Scathophagidae), we qualitatively tested a general model that predicts the distribution of mating success among competing males based on the temporal pattern of female arrivals relative to mating time and a ranking of males in priority of access to the resource (here by body size). In a laboratory experiment approximating the natural mating situation, a constant number of males of various sizes were allowed to compete for females. As predicted, mate monopolization decreased as the temporal clumping of female arrivals increased, mediated by either a decrease in the mean or an increase in the variance of female inter-arrival times, which were manipulated independently. Males appeared to adjust their behavior to variation in female arrivals in a manner consistent with the marginal value theory of Parker and associates: forcible take-overs of females were rarer, and copula durations shorter, when females arrived regularly at short intervals. Therefore, a complex interaction of variation in intrinsic characteristics affecting male resource holding potential, mating time and stochastic, extrinsic variables increasing temporal clumping of mates generally reduces the variance in mating success among competing males and thus ultimately the opportunity and intensity of sexual selection on traits influencing male success. This theory extends operational sex ratio theory at the mechanistic, behavioral leve