This integrative dissertation explores the ultimate (evolutionary) as well as proximate (i.e. mechanistic developmental) drivers of life-history traits in insects. The focus lies on the evolution of body size, sexual size dimorphism (SSD) and sex-specific body size plasticity, which are studied on different levels of biological organization. The following six chapters integrate experimental and quantitative genetic studies with comparative approaches and aim at broadening our current knowledge on how the astonishing phenotypic variation observed across the tree of life came about and how it is maintained.
Chapter 1 explores global patterns of body size, sexual size dimorphism, relative wing size and geographic range size among 151 species of fruit flies (Diptera: Drosophilidae). In vertebrates, these traits accord fairly predictably with prominent ecogeographic “rules” (Bergmann’s, Rensch’s, Allen’s, Rapoport’s rules). However, the predictive power of these rules in invertebrates — and insects in particular — is very poor, at least in part due to lack of a mechanistic understanding of the drivers of such variation. As these traits are to some extent evolutionarily or ecologically interdependent, possible confounding effects between macroecological patterns are expected and might explain some of the apparent idiosyncrasy. Such interrelations are rarely considered. Here, I test the predictions of Bergmann, Rensch, Allen and Rapoport for a large number of drosophilids across the globe to investigate potential confounding effects between patterns. Although there is limited evidence for any confounding effects, I nevertheless demonstrate the usefulness of studying several macroecological patterns simultaneously, as it allows for a deeper, mechanistic understanding of ecogeographic variation.
In chapter 2, I assess quantitative genetic latitudinal differentiation in life history traits in the widespread sepsid fly Sepsis fulgens (Diptera: Sepsidae) across 13 populations spanning 20 degrees latitude from southern Italy to Estonia. Despite very short generation times, I found a converse Bergmann cline (smaller size at higher latitudes). As development time did not change with latitude (flat cline), integral growth rate thus likely declines towards the pole. At the same time, early fecundity, but not egg size, increased with latitude. Rather than being mediated by seasonal time constraints, the body size reduction in the northernmost flies from Estonia could suggest that these are marginal, edge populations, as when omitting them the body size cline became flat as well. Most of the other sepsid species investigated to date also show flat body size clines, a pattern that strikingly differs from Drosophila. I conclude that S. fulgens life history traits appear to be shaped by similar environmental pressures and selective mechanisms across Europe, be they adaptive or not. This reiterates the suggestion that body size clines can result as a secondary consequence of selection pressures shaping an entire life history syndrome, rendering them inconsistent and unpredictable in general.
Chapter 3 focusses on the evolution of sexual size dimorphism (SSD) and sex-specific body size plasticity. In insects, females are usually the larger and more plastic sex. However, because females are larger than males in most species, it is difficult to assess whether their greater plasticity is driven by selection on size or represents an effect of the female reproductive role per se. I here estimate sex-specific body size plasticity of populations and species that vary in the direction and extent of SSD, and show that males are typically more plastic than females if they are the larger sex. Hence, my findings indicate that primarily selection on size, rather than the reproductive role per se, drives the evolution of sex-specific body size plasticity. However, sepsid flies, and possibly Diptera in general, show a clear sexual asymmetry with greater male than female plasticity related to SSD, likely driven by strong sexual selection on males. Although further research controlling for phylogenetic and ecological confounding effects is needed, the patterns are congruent with theory suggesting that condition dependence plays a pivotal role in the evolution of sexual size dimorphism.
In chapter 4, I investigate the potential link between the extent of sexual dimorphism and sex-specific condition dependence among traits and species. Sexual selection can displace traits acting as ornaments or armaments from their viability optimum in one sex, ultimately giving rise to sexual dimorphism. The degree of dimorphism should hence not only mirror the strength of sexual selection, but also the net viability costs and benefits of trait maintenance at equilibrium. The ability of organisms to bear exaggerated traits will depend on their condition. More sexually dimorphic traits should therefore also exhibit greater sex differences in condition dependence. While this has been shown to apply among traits within species, condition dependence and sexual dimorphism are also expected to correlate across the phylogeny. I investigated and quantified this prediction within and across 11 (sub)species of black scavenger flies that vary in their mating system. When estimating sex-specific condition dependence for seven sexual and non-sexual traits that vary in their sexual dimorphism, we not only found a positive relationship between the sex difference in allometric slopes (as our measure of condition dependence) and relative trait exaggeration among traits within species, but also across species for those traits expected to be under sexual selection in males. I additionally show species with more pronounced male aggression to have relatively larger and more condition-dependent male fore and mid legs. My comparative study suggests a common genetic/developmental basis of sexual dimorphism and sex-specific plasticity that apparently evolves across the phylogeny, and that the evolution of trait size consistently alters scaling relationships and thus contributes to the allometric variation of sexual armaments or ornaments in animals.
In chapter 5, I investigate the physiological basis of adaptive size variation in the yellow dung fly Scathophaga stercoraria, which shows pronounced male-biased sexual size dimorphism and strong body size plasticity. I estimate variation of a major physiological threshold, the critical weight, which is the mass at which a larva initiates pupariation. Critical weight is associated with sexual size dimorphism and sex-specific plasticity, and is thus a likely target of selection on adult size. Detailed larval growth trajectories derived from individuals raised at two food and temperature treatments further reveal that sex-specific size plasticity is mediated by faster initial growth of males that later becomes reduced by greater male weight loss during the wandering stage. Hence, I illustrate the importance of detailed assessments of ontogenetic growth trajectories for the understanding of adaptive size variation and discuss the mechanistic basis of size determination in shaping sex-specific phenotypic plasticity.
Chapter 6 is devoted to the effect temperature on the evolution of insect wings. Given its profound effect on biological systems, temperature is often held responsible for eliciting phenotypic plasticity as well as quantitative genetic differentiation. If genetic and plastic responses to temperature are adaptive, they should be related in magnitude and form, a pattern that should evolve repeatedly in different lineages. I quantified this putative relationship between quantitative genetic latitudinal variation in wing loading and wing shape and their thermal plasticity in two closely related sepsid flies with contrasting sexual size dimorphism. Common garden rearing revealed decreasing wing loading with latitude independently in both species, likely driven by selection for increased dispersal capacity in the cold. Thermal plasticity for wing loading was however non-linear, suggesting that the relationship between plasticity and genetic differentiation is more complex. Although both species showed similar patterns of wing shape allometry, sexual dimorphism and thermal plasticity, latitudinal differentiation only mirrored thermal plasticity in one but not the other species. Arguing that such discrepancies may be driven by variation in gene flow and demography, these results reiterate the notion that genetic wing shape differentiation may be complex and idiosyncratic even among ecologically similar closely related species.
In summary, by integrating studies on different insect systems at multiple levels of biological organization (from single genotypes to population differentiation within species to global interspecific variation), this dissertation provided insights into the evolution of life histories and hence contributes to the understanding of diversity and disparity in the broadest sense.