BackgroundPigmentation has a long history of investigation in evolutionary biology. In Drosophila melanogaster, latitudinal and altitudinal clines have been found but their underlying causes remain unclear. Moreover, most studies were conducted on cosmopolitan populations which have a relatively low level of genetic structure and diversity compared to sub-Saharan African populations. We investigated: 1) the correlation between pigmentation traits within and between the thorax and the fourth abdominal segment, and 2) their associations with different geographical and ecological variables, using 710 lines belonging to 30 sub-Saharan and cosmopolitan populations.ResultsPigmentation clines substantially differed between sub-Saharan and cosmopolitan populations. While positive correlations with latitude have previously been described in Europe, India and Australia, in agreement with Bogert's rule or the thermal melanism hypothesis, we found a significant negative correlation in Africa. This correlation persisted even after correction for altitude, which in its turn showed a positive correlation with pigmentation independently from latitude. More importantly, we found that thoracic pigmentation reaches its maximal values in this species in high-altitude populations of Ethiopia (1,600-3,100 m). Ethiopian flies have a diffuse wide thoracic trident making the mesonotum and the head almost black, a phenotype that is absent from all other sub-Saharan or cosmopolitan populations including high-altitude flies from Peru (~3,400 m). Ecological analyses indicated that the variable most predictive of pigmentation in Africa, especially for the thorax, was ultra-violet (UV) intensity, consistent with the so-called Gloger's rule invoking a role of melanin in UV protection.ConclusionOur data suggest that different environmental factors may shape clinal variation in tropical and temperate regions, and may lead to the evolution of different degrees of melanism in different high altitude populations in the tropics.

In higher organisms, the phenotypic impacts of potentially harmful or beneficial mutations are often modulated by complex developmental networks. Stabilizing selection may favor the evolution of developmental canalization—that is, robustness despite perturbation—to insulate development against environmental and genetic variability. In contrast, directional selection acts to alter the developmental process, possibly undermining the molecular mechanisms that buffer a trait’s development, but this scenario has not been shown in nature. Here, we examined the developmental consequences of size increase in highland Ethiopian Drosophila melanogaster. Ethiopian inbred strains exhibited much higher frequencies of wing abnormalities than lowland populations, consistent with an elevated susceptibility to the genetic perturbation of inbreeding. We then used mutagenesis to test whether Ethiopian wing development is, indeed, decanalized. Ethiopian strains were far more susceptible to this genetic disruption of development, yielding 26 times more novel wing abnormalities than lowland strains in F2 males. Wing size and developmental perturbability cosegregated in the offspring of between-population crosses, suggesting that genes conferring size differences had undermined developmental buffering mechanisms. Our findings represent the first observation, to our knowledge, of morphological evolution associated with decanalization in the same tissue, underscoring the sensitivity of development to adaptive change.

Understanding the physiological and genetic basis of growth and body size variation has wide‐ranging implications, from cancer and metabolic disease to the genetics of complex traits. We examined the evolution of body and wing size in high‐altitude Drosophila melanogaster from Ethiopia, flies with larger size than any previously known population. Specifically, we sought to identify life history characteristics and cellular mechanisms that may have facilitated size evolution. We found that the large‐bodied Ethiopian flies laid significantly fewer but larger eggs relative to lowland, smaller‐bodied Zambian flies. The highland flies were found to achieve larger size in a similar developmental period, potentially aided by a reproductive strategy favoring greater provisioning of fewer offspring. At the cellular level, cell proliferation was a strong contributor to wing size evolution, but both thorax and wing size increases involved important changes in cell size. Nuclear size measurements were consistent with elevated somatic ploidy as an important mechanism of body size evolution. We discuss the significance of these results for the genetic basis of evolutionary changes in body and wing size in Ethiopian D. melanogaster.