Overall patterns of selection
Patterns of spatiotemporal variation in viability, fecundity and sexual selection on body size (head width) in three Swiss populations of the dung fly S. cynipsea differed markedly. To summarize briefly, adult viability selection, based on residual physiological survivorship in the laboratory, was nil or weakly negative. In contrast, larval viability selection was weakly positive for males at low and females at high competition. Fecundity selection was positive and strong at all times and in all populations. Sexual selection reflecting pairing success (SexS1) was overall positive, on average three to four times stronger than fecundity selection, but varied significantly at coarse (between populations and seasonally) but not at fine (within a day or between pats on one pasture) spatiotemporal scales. Selection reflecting male reproductive success via the body or clutch size of his mate (i.e. assortative mating; SexS2) was weak in comparison and only apparent in one population (Fehraltorf). Quadratic and correlational selection differentials were low and inconsistent for all episodes except for fecundity selection, which appeared to level off at large body sizes. We first discuss these findings in more detail and then their implications for body size evolution.
Even though we are aware of its many limitations, residual physiological longevity in the laboratory after capture may reflect at least some aspect of survivorship, provided that time of season (i.e. week) and size do not covary systematically. The 1995 study actually showed a clear seasonal pattern of body size variation: individuals were larger at the beginning and the end of the season. This can be largely explained by the differences in temperature and competition the six or more cohorts per season faced during development (Atkinson, 1994; Blanckenhorn, 1997; Morf, 1997). However, the summer decline in body size in 1995 really did not start before July, and a decline was also not evident early in the 1994 season (May and June). This is because all adults present during the first few weeks of the season are over-wintered individuals born in autumn of the previous year (Blanckenhorn, 1998a); the decline in size in early summer most likely coincides with the massive emergence of their first offspring which developed at higher temperatures. It is thus unlikely that our estimates of adult viability selection are strongly confounded by seasonal changes in size, though some offspring probably were present already in late June, thus possibly explaining the increasingly negative selection differentials toward the end of the 1994 sampling period (Table 1). However, we cannot dismiss the possibility that within a cohort the unpaired males were simply the young and inexperienced individuals and therefore lived longer in the laboratory after capture. Furthermore, our laboratory surrogate of adult viability selection does not include mortality due to predation or parasites and thus does not well represent the natural situation but, unfortunately, mark-recapture studies in the field are prohibitive in this small species. With all these caveats in mind, our data indicate that viability selection on body size as defined here was, if anything, only very weakly negative. Large males and females may thus be at a slight disadvantage, which can be interpreted as a consequence of greater environmental stress resulting from more pairing activity of large males and from higher reproductive investment of the larger females.
Larval viability selection was estimated with laboratory-reared F3 individuals to eliminate potential maternal effects, at two environments characterized by high and low intraspecific competition for food. Obviously, these two treatments do not encompass the variability in dung quantity and quality existing in nature. Nonetheless, based on our extensive rearing experience with this species, much lower per capita dung availability than that of the high competition treatment will rapidly reduce larval survivorship to zero. Our low (no) competition treatment estimated the base-line larval survivorship, and our high competition treatment led to a significant increase in larval mortality, as expected. In addition, body size was reduced by intraspecific larval competition but development time was not. Development times of males and females are the same despite the difference in body size, which may explain why there were no systematic differences in mortality between the sexes as a function of treatment (Blanckenhorn, 1997; this study). Somewhat surprisingly, larval viability selection on body size tended to be positive, at least for males at low and females at high competition. We expected the opposite, as greater body size is often associated with longer development time within individuals, which should entail a disadvantage in a rapidly depleting habitat such as dung (Roff, 1980; e.g. Partridge & Fowler, 1993; Blanckenhorn, 1998b). However, the presumed positive correlation between development time and body size apparently does not hold in S. cynipsea and, in retrospect, negates this argument (Blanckenhorn, 1997; this study). Instead, small, heritable differences in larval growth rate between individuals that become magnified during development may confer a competitive advantage to large genotypes and explain our results. This assumes that the base-line mortality that occurred at no competition did not selectively target large genotypes. Should this be so, increased mortality of large genotypes would be intrinsic (e.g. due to pleiotropic genetic effects) and difficult to assess experimentally. The crucial result is that, as was the case for our estimates of adult viability selection, larval viability selection as estimated here appeared weak in comparison to fecundity and sexual selection. We consider it unlikely that our results are strongly affected by two generations of laboratory rearing, which may alter or relax natural selection pressures, as individuals were reared and held in mass containers under seminatural conditions.
Fecundity selection was positive and strong at all times and in all populations, as could be expected for ectotherms (e.g. Wootton, 1979). Of course, clutch size is an imperfect estimator of lifetime reproductive success (Lande & Arnold, 1983; Arnold & Wade, 1984a,b; Endler, 1986). However, given that longevity in this species in the laboratory is highly variable and shows little pattern with regard to body size (Blanckenhorn, 1997; this study), using clutch size as an index of female fitness appears reasonable in this context. A negative nonlinear in combination with a positive linear regression coefficient suggests that clutch size reaches an asymptote at large body sizes, implying weaker selection for large size as females get bigger. Clutch size may be limited by mechanical or loading constraints that could reduce the flight performance and hence survivorship of large females, ultimately limiting female size (Fairbairn, 1990; Berrigan, 1991; Roff, 1992). However, this effect cannot be very strong, as we might expect it to be detectable even in the laboratory (compare above and below).
Based on head width as an index of body size, sexual selection for large males in S. cynipsea was seasonally variable but overall consistent. Throughout the year and in all populations it was positive or nil, but never negative, and our mean estimates for the two years in Fehraltorf were very similar. As already mentioned in the Methods, we did not differentiate between copulating and noncopulating pairs, thus ignoring one of the three selection episodes in the sexual context described in this species. Our sexual selection differentials are thus probably underestimates, as the large male advantage has been shown to occur in all three selection episodes (Ward, 1983; Ward et al., 1992) and the differentials of the three episodes are simply additive because the selection episodes are multiplicative (Arnold & Wade, 1984b). However, we do not know the magnitude of this supposed underestimation.
Implications of spatiotemporal variability in selection
Selection regimes, particularly those of sexual selection, are expected to differ in space and time, and this has important implications for evolutionary change (Lande & Arnold, 1983; Endler, 1986). For example, selection can change sign over the season and thus, on average, have a stabilizing effect (fluctuating-stabilizing selection; Istock, 1981). Various mechanisms can cause seasonal variation in sexual selection: it may be caused by seasonal changes in the availability of mating sites or host plants affecting local competitor density (McLain, 1992; McLain et al., 1993), by fluctuations in population density per se (Nishida, 1994) or by density-dependent female reluctance to mate (‘convenience polyandry’; Parker, 1972a; Thornhill & Alcock, 1983; Arnqvist, 1989; 1992a,b; Rowe, 1992; Rowe et al., 1994). The last of these mechanisms may operate in S. cynipsea (Blanckenhorn et al., unpublished). Of course, temporal changes in selection or in the conditions affecting selection within populations may be merely stochastic.
Our bivariate analysis suggests that head width is positively correlated with the real target of selection while for tibia length selection tends to be in the opposite direction, even though both (as well as other morphometric) measures are generally highly positively correlated in S. cynipsea (Reusch & Blanckenhorn, 1998). Why this is so is unclear at this point, but it implies that not all morphometric measurements can be taken as equally good indices for body size, as selection seems to target them differentially, thus affecting shape as well as size (Fairbairn, 1992). It also implies that the foregoing interpretation of our results has to be understood as evidence for selection on head width (or a correlate thereof) and not necessarily on body size per se. If females can measure male weight during pairing, a possible simple assessment mechanism, a measure directly reflecting overall body volume like head width may reflect this kind of selection better than tibia length, which additionally may be subject to different selection pressures (Fairbairn, 1990; Klingenberg & Zimmermann, 1992). Moreover, if females have an absolute weight threshold, the simplest selection mechanism possible, they should have difficulties choosing among a large number of invariably small males in summer, resulting in the lower sexual selection intensities observed during that time in our 1995 study. However, a multivariate selection study incorporating more morphometric traits (which is under way) is necessary to dissect the various selection pressures that affect size and shape in S. canipsea.
Temporal variation within populations notwithstanding, consistently more intense sexual selection favouring larger males should produce larger mean body sizes over evolutionary time, as fluctuating-stabilizing selection limiting the evolution of larger body sizes does not seem to occur in our populations (Istock, 1981). Sexual selection favouring larger males should also predictably affect the degree of sexual size dimorphism such that in species like S. cynipsea, where males are smaller, the size difference between males and females should decrease and, perhaps, ultimately reverse (Fairbairn & Preziosi, 1994). Our small population comparison indicates that sexual selection indeed tended to be strongest in the population with the greatest mean body size (Fehraltorf) and weakest in the population with the smallest mean body size (Luzern). We are currently extending our data set to rigorously test Fairbairn & Preziosi's (1994) hypothesis. The results of this study are of practical relevance in this context because they imply that sampling any pat at any time on a given day will not affect our population estimate of sexual selection, but when we sample in the season will. The latter may crucially hamper detecting variation in selection between populations if such variation is small compared to the seasonal variation detected here: in the extreme, sampling a population once in summer may yield a selection differential of zero even though, overall, sexual selection occurs in this population.