Sexual selection on morphological and physiological traits and fluctuating asymmetry in the black scavenger fly Sepsis cynipsea

Previous univariate studies of the fly Sepsis cynipsea (Diptera: Sepsidae) have demonstrated spatiotemporally variable and consequently overall weak sexual selection favouring large male size, which is nevertheless stronger on average than fecundity selection favouring larger females. To identify specific target(s) of selection on body size and additional traits possibly affecting mating success, two multivariate field studies of sexual selection were conducted. In one study using seasonal replicates from three populations, we assessed 15 morphological traits. No clear targets of sexual selection on male size could be detected, perhaps because spatiotemporal variation in selection was again strong. In particular, there was no (current) selection on male abdomen length or fore coxa length, the only traits for which S. cynipsea males are not smaller than females. Interestingly, copulating males had a consistently shorter fore femur base, a secondary sexual trait, and a wider clasper (hypopygium) gap, an external genital trait. In a second study using daily and seasonal replicates from one population, we included physiological measures of energy reserves (lipids, glucose, glycogen), in addition to hind tibia length and fluctuating asymmetry (FA) of all pairs of legs. This study again confirmed the mating advantage of large males, and additionally suggests independent positive influences of lipids (the long-term energy stores), with effects of glucose and glycogen (the short-term energy stores) tending to be negative. FA of paired traits was not associated with male mating success. Our study suggests that inclusion of physiological measures and genital traits in phenomenological studies of selection, which is rare, would be fruitful in other species.     

Sexual conflict over copula timing: a mathematical model and a test in the yellow dung fly

Sexual conflict over mating occurrence, timing, or durationis common in animals. This explains conspicuous female materejection behavior in many species, often involving shaking,fighting, and occasional forced copulations. We present a simplemodel that generates predictions about whether and when copulationoccurs in such conflict situations and how much female rejectionbehavior should be observed. Predictions depend on 2 underlyingparameters affecting female resistance and male persistence.We supply 2 qualitative tests of the model using the yellowdung fly Scathophaga stercoraria (Diptera: Scathophagidae).We manipulated adult age, body size (large and small), and adultfood availability (low and high), independently in males andfemales, staging replicate pairings of all treatment combinations.In agreement with predictions of our model, shaking durationfirst increased to a maximum at intermediate age, when the averagefemale copulated, and then decreased again. Contrary to expectation,body size did not affect copulation timing, female resistance,or male persistence. As predicted, adult food limitation delayedsexual maturity and hence prolonged female resistance, resultingin later copulations after more shaking. However, although foodlimitation equally delayed the increase in male persistencewith age, copulation also occurred later after more shaking,opposite to the model prediction. We conclude that shaking isdriven primarily by female age and male responses to it. Althoughfemale shaking can initially successfully deter males in S.stercoraria, this behavior is subtle and has apparently shiftedfunction from an effective means of mate choice to a signalof nonreceptivity, though its importance in nature remains unclear.     

The heritability of sexually dimorphic traits in the yellow dung fly Scathophaga stercoraria (L.)

A precise method was used for estimating the proportion of heritable variation in two life history parameters of the yellow dung fly, whereby environmental components of variance were minimized. Significant heritable variation for body size was revealed for father to son and mother to daughter relationships. Variation in development time was not significantly heritable. There is a marked sexual dimorphism in body size in this species which is discussed in the light of the observed sex-genotype interaction in heritabilities and low genetic correlation for size between the sexes. It is suggested that opposing pressures of sexual and natural selection and/or genetic pleotropy may be responsible for the maintenance of heritable variation, and the evolution of sexual dimorphism in these two traits.     

Heritability of three condition surrogates in the yellow dung fly

Condition capture has been proposed as a general mechanism maintainingadditive genetic variation, V_a, in sexually selected traitsunder directional selection. It relies on two main assumptions:condition-dependent trait expression and V_a in condition. Althoughthere is evidence for the former, direct evidence that conditionis heritable is scarce, although this is a requirement of mostmodels of handicap sexual selection. We used a parent–offspring,full-sib, two-container laboratory breeding design in the yellowdung fly Scathophaga stercoraria to demonstrate the broad- andnarrow-sense heritability of three surrogates of condition commonlyused in sexual selection studies: lipid and glycogen reserves(i.e., physiological condition), body size, and fluctuatingasymmetry. All three measures are nutrition dependent and havebeen linked to sexual selection in free-living yellow dung flies.While lipid reserves and body size were heritable, asymmetryand glycogen reserves were not. Moreover, the evolvability ofphysiological condition was higher than that of the other twotraits. Of the three surrogates, physiological condition ismost akin to the original definition, but all have their limitations.We conclude that condition is a useful heuristic concept inevolutionary ecology, but its practical value may be limitedby the fact that it cannot be measured directly.     

Temporal and microspatial variation in the intensities of natural and sexual selection in the yellow dung fly Scathophaga stercoraria

Studies of phenotypic selection in natural populations often concentrate only on short time periods and do not quantify selection intensities. We quantified temporal and microspatial variation in the intensities of natural and sexual selection for body size in the yellow dung fly over 2 years. Female fecundity selection intensity remained approximately constant over the season with an overall mean ± SE of 0.187 ± 0.014. Selection intensity for male reproductive success, defined as eggs obtained by mating males, did not differ from zero, indicating there was no assortative mating by size. Sexual selection intensity for male mating success favouring large males was variable but overall strong in the two years (0.499 ± 0.053 and 0.510 ± 0.051). As theoretically expected for male–male competition, sexual selection intensity increased with competitor density and reached an asymptote at about 250 males per pat; it also decreased with time in spring and increased again in autumn as a function of density. Small males had the best chance of obtaining a female at very low male densities. Greater selection intensity for large size in males than females is consistent with, and might be responsible for, the observed sexual size dimorphism in this species, as males are larger. The seasonal pattern of mean male body size (smallest at the beginning and end of the season) most likely reflects mere environmental (primarily temperature) influences on phenotypic size.     

Spatiotemporal variation in selection on body size in the dung fly Sepsis cynipsea

Standardized measures of the strength of selection on a character allow quantitative comparisons across populations in time and space. Spatiotemporal variation in selection influences patterns of adaptation and the evolution of characters and must therefore be documented. For the dung-breeding fly Sepsis cynipsea, we document patterns of variation in sexual, fecundity and larval and adult viability selection on body size at several spatiotemporal scales: between-populations, over the season, over the day and between dung pats. Adult viability selection based on residual physiological survivorship in the laboratory was nil or weakly negative. In contrast, larval viability selection in two laboratory environments was weakly positive for males at low competition and females at high competition. Fecundity selection was positive and strong at all times and in all populations. Sexual selection reflecting pairing success was overall strongly positive (about three times stronger than fecundity selection), while selection reflecting male reproductive success via the clutch size of his mate (i.e. assortative mating) was essentially nil. Only sexual selection varied significantly at coarse (between populations and seasonally) but not at fine (within a day or between pats on a pasture) spatial and temporal scales. Quadratic and correlational selection differentials were low and inconsistent in all episodes except for fecundity selection, where there was some evidence that clutch size reaches an asymptote at large body sizes, implying weaker selection for large size as females get bigger. Implications of these results for the evolution of body size and body size dimorphism are discussed.     

Size-dependent alternative male mating tactics in the yellow dung fly,Scathophaga stercoraria

Whenever males can monopolize females and/or resources used by females, the opportunity for sexual selection will be great. The greater the variation among males in reproductive success, the greater the intensity of selection on less competitive males to gain matings through alternative tactics. In the yellow dung fly, Scathophaga stercoraria, males aggressively compete for access to receptive, gravid females on fresh dung. Larger males are better able to acquire mates and to complete copulation successfully and guard the female throughout oviposition. Here we demonstrate that when an alternative resource is present where females aggregate (i.e. apple pomace, where both sexes come to feed), smaller males will redirect their searching for females from dung to the new substrate. In addition, we identify a class of particularly small males on the alternative substrate that appears never to be present searching for females on or around dung. Smaller males were found to have a mating ‘advantage’ on pomace, in striking contrast to the pattern observed on dung, providing further support for the existence of an alternative male reproductive tactic in this species.     

Genetic and environmental sources of covariance among internal reproductive traits in the yellow dung fly

Substantial inter- and intraspecific variation is found in reproductive traits, but the evolutionary implications of this variation remain unclear. One hypothesis is that natural selection favours female reproductive morphology that allows females to control mating and fertilization and that diverse male reproductive traits arise as counter adaptations to subvert this control. Such co-evolution predicts the establishment of genetic correlations between male and female reproductive traits that closely interact during mating. Therefore, we measured phenotypic and genetic correlations between male and female reproductive tract characteristics in the yellow dung fly, Scathophaga stercoraria (Diptera: Scathophagidae), using a nested half-sib breeding experiment. We found significant heritabilities for the size of most reproductive tract traits investigated in both females (spermathecae and their ducts, accessory glands and their ducts) and males (testis size but not sperm length). Within the sexes, phenotypic and genetic correlations were mostly nil or positive, suggesting functional integration of or condition-dependent investment in internal reproductive traits. Negative intrasexual genetic correlations, potentially suggestive of resource allocation trade-offs, were not evident. Intersexual genetic correlations were mostly positive, reflecting expected allometries between male and female morphologies. Most interestingly, testis size correlated positively with female accessory gland size and duct length, potentially indicative of a co-evolutionary arms race. We discuss these and alternative explanations for these patterns of genetic covariance.     

Sex and immunity in the yellow dung fly Scathophaga stercoraria

The immune system is of increasing interest to evolutionary biologists. Immunity may trade-off against other fitness components, with recent work suggesting reproduction in particular impinges on immune defence. There may also be sex differences in the immune system. Additionally, while life history traits typically have low heritability, little is known about additive genetic variance of immunity. An insect's major defence against multicellular pathogens is to encapsulate the invader. Phenoloxidase (PO) is a key enzyme in the cascade resulting in the melanized capsule, and is often used to estimate resistance to an immune insult. We examined the effects of copulation, egg laying, sex and age on PO in Scathophaga stercoraria. We also measured the heritability of PO activity. The sexes differed in haemolymph PO activity and PO was significantly affected by age, but not by copulation or egg laying. There was significant heritable variation for haemolymph PO.     

Correlated responses to artificial body size selection in growth, development, phenotypic plasticity and juvenile viability in yellow dung flies

Most life history traits are positively influenced by body size, whereas disadvantages of large body size are poorly documented. To investigate presumed intrinsic costs of large size in the yellow dung fly (Scathophaga stercoraria; Diptera: Scathophagidae), we established two replicates each of three body size laboratory selection lines (small, control and large; selection on males only), and subjected flies of the resulting extended body size range to various abiotic stresses. Response to selection was symmetrical in the small and large lines (realized h(2) = 0.16-0.18). After 24 generations of selection body size had changed by roughly 10%. Female size showed a correlated response to selection on male size, whereas sexual size dimorphism did not change. Development time also showed a correlated response as, similar to food limited flies, small line flies emerged earlier at smaller body size. At the lowest larval food limit possible, flies of all lines emerged at the same small body size after roughly the same development time; so overall phenotypic plasticity in body size and development time strongly increased following selection. Juvenile mortality increased markedly when food was extremely limited, large line flies showing highest mortality. Winter frost disproportionately killed large (line) flies because of their longer development times. Mortality at high temperatures was high but size-selective effects were inconsistent. In all environments the larger males suffered more. Initial growth rate was higher for males and at unlimited food. Small line individuals of both sexes grew slowest at unlimited larval food but fastest at limited larval food, suggesting a physiological cost of fast growth. Overall, extension of the natural body size range by artificial selection revealed some otherwise cryptic intrinsic juvenile viability costs of large size, mediated by longer development or faster growth, but only in stressful environments.     

Detecting genetic variation in developmental instability by artificial selection on fluctuating asymmetry

Abstract Fluctuating asymmetry (FA) is frequently used as a measure of developmental instability (DI). Assuming a genetic basis to DI, many have argued that FA may be a good indicator of genetic quality to potential mates and to human managers of populations. Unfortunately FA is a poor indicator of DI, making it very difficult to verify this assertion. A recent review of the literature suggests that previous studies of the inheritance of FA and DI using half‐sib covariances and parent–offspring regression have been unable to put meaningful limits on the heritability of FA and DI because of the extremely low power of the experiments performed. In this study, we consider the power of artificial selection on FA as an alternative approach to studying the inheritance of FA and DI. Using simulations, we investigate the efficacy of selection for both increased and decreased FA for detecting genetic variation. We find that selection for increased FA has much more power to detect the presence of genetic variation than does selection for decreased FA. These results hold when realistic sample sizes are employed. Artificial selection for increased FA is currently the most powerful approach for the detection of genetic variation in DI.     

The causes of seasonal changes in numbers of the yellow dung fly, Scathophaga stercoraria (Diptera: Scathophagidae)

ABSTRACT. 1. Counts of adult Scathophaga stercoraria (L.) on cow pats were made in Houghall, County Durham, in 1964 and 1965.
2. A spring peak of numbers was due to adults (overwintered mainly as pupae or larvae) maturing and going to dung to breed. Numbers then dropped, rising to one or more peaks in late June—early July. In 1964 there was then a summer drop in numbers until late September. In 1965 high numbers persisted in summer associated with cooler, wetter weather. Autumn peaks in both years persisted until severe frosts or snow.
3. Mature adults, developed from eggs laid during the spring peak, form the first generation when breeding in mid-late June. No clear generations can be identified after this, due to eggs being laid daily (females have successive gonotrophic cycles). Changes in adult numbers breeding reflects survival of eggs and newly-hatched larvae 5–6 weeks earlier, and lower survival rates of adults in mid-summer compared with spring and autumn.
4. Adult Scathophaga numbers in vegetation rose as numbers on dung dropped. Females dissected to count ovariole tunica dilatations showed that most flies in vegetation were immature, with some parous flies hunting insects to develop the next batch of eggs.
5. Females on dung were dissected and found to range from immature to seven-parous. Those gravid for the first time were grossly under-represented, possibly due to wider dispersal.
6. It is suggested that seasonal changes in this r-strategist cannot be explained simply in terms of generations nor by the occurrence of adult diapause.     

The effect of sperm storage and timing of mating on offspring sex ratios in the yellow dung fly Scatophaga stercoraria

1. Offspring sex ratios in the yellow dung fly Scatophaga stercoraria were examined in the laboratory. 2. Previous work indicated that females using previously stored sperm to fertilise their eggs produced male‐biased sex ratios. This result may have been due to female influences or the effects of sperm storage per se. 3. This pattern was not reproduced in the study presented here. Females that were allowed to mate just prior to oviposition produced similarly male‐biased sex ratios to those females that used previously stored sperm to fertilise their clutch. 4. Captive‐reared females may have perceived a lack of males in the population and thus produced a male‐biased offspring sex ratio. Alternatively, gamete ageing or extra‐chromosomal sex ratio distorters may have produced the male bias.     

Alternative mating tactics in the yellow dung fly: resolving mechanisms of small-male advantage off pasture

Recent work suggests that the yellow dung fly mating system may include alternative patroller–competitor mating tactics in which large males compete for gravid females on dung, whereas small, non-competitive males search for females at foraging sites. Small males obtain most matings off pasture, yet the behavioural mechanism(s) giving rise to this pattern are unknown. We investigated the male and female behaviours that determine mating success in this environment by conducting field mating experiments and found small males to benefit from several attributes specific to the off-pasture mating environment. First, small males from foraging sites exhibited higher mating propensity, indicating that large males away from dung may be depleted of energy and/or sperm. Second, small males were more discriminating, being significantly less likely to attempt with non-gravid females, which are absent on dung but common off pasture. Third, non-gravid females were generally more likely to actively struggle and reject mating attempts; however, such behaviours occurred disproportionately more often with large males. Female Scathophaga stercoraria thus appear to preferentially mate with small males when off pasture. These findings challenge assumptions about male–female interactions in systems with alternative mating tactics and reveal hidden processes that may influence selection patterns in the field.     

Developmental stability in yellow dung flies (Scathophaga stercoraria): fluctuating asymmetry,heterozygosity and environmental stress

The genetic basis for developmental stability, the ability of an organism to withstand genetic and environmental disturbance of development, is poorly understood. Fluctuating asymmetry (FA: small random deviations from symmetry in paired, bilateral traits) is the most widely used measure of developmental stability, and evidence suggests FA is weakly and negatively associated with genome‐wide heterozygosity. We investigated the genetic basis of developmental stability in the yellow dung fly. Fly lines were inbred for 16 generations at which time they were homozygous at the phosphoglucomutase (PGM) loci and PGM appears to influence FA in at least one other taxon. After 16 generations of inbreeding, lines homozygous for different PGM alleles were crossed and levels of FA for four metric traits were compared in the inbred and crossed flies. We also compared FA levels in these flies with previously gathered data on wild‐type (second generation outcrossed) flies, and additionally looked at the effects of two environmental stresses (larval food limitation and increased temperature) on FA. There were no significant differences in any measure of FA, nor in mean FA, in any trait when inbred and crossed flies were compared. Comparison of FA in these and wild flies also revealed no significant differences. Food limitation had no influence on FA, whereas heat stress increased FA of naturally, but not sexually, selected traits. Our results do not show a negative relationship between heterozygosity and FA, but support the notion that FA levels are stress, trait and taxon specific.     

Individual differences in developmental precision and fluctuating asymmetry: a model and its implications

In many studies, fluctuating asymmetry (FA) has been used as a measure of individual differences in developmental imprecision. A model of how variation in developmental imprecision is associated with variation in asymmetry is described and applied to important issues about FA. If individual differences in developmental imprecision exist, asymmetry due to developmental error should be leptokurtically distributed. Moreover, the greater the magnitude of individual differences, the greater the leptokurtosis. Asymmetry purportedly due to developmental error in a variety of species is indeed leptokurtically distributed. The level of leptokurtosis suggests that the CV in individual differences in underlying developmental imprecision is generally 20–25, consistent with it being a fitness trait. In addition, data suggest that: (1) the individual differences that underlie the developmental imprecision of different traits are largely shared across traits and not trait-specific; (2) the heritability of these individual differences may average between 35 and 55%, despite small heritabilities of individual trait FAs; and (3) correlations between FA and fitness traits or components suggest high correlations between underlying variation in developmental precision and fitness in many species. Theoretical implications are discussed.     

Response of fluctuating and directional asymmetry to selection on wing shape in Drosophila melanogaster

We tested whether directional selection on an index-based wing character in Drosophila melanogaster affected developmental stability and patterns of directional asymmetry. We selected for both an increase (up selection) and a decrease (down selection) of the index value on the left wing and compared patterns of fluctuating and directional asymmetry in the selection index and other wing traits across selection lines. Changes in fluctuating asymmetry across selection lines were predominantly small, but we observed a tendency for fluctuating asymmetry to decrease in the up-selected lines in both replicates. Because changes in fluctuating asymmetry depended on the direction of selection, and were not related to changes in trait size, these results fail to support existing hypotheses linking directional selection and developmental stability. Selection also produced a pattern of directional asymmetry that was similar in all selected lines whatever the direction of selection. This result may be interpreted as a release of genetic variance in directional asymmetry under selection.