Evolutionary adaptation to juvenile malnutrition impacts adult metabolism and impairs adult fitness inDrosophila

Abstract

Juveniles are often first to suffer from nutrient shortage, and juvenile undernutrition is likely an important force of natural selection shaping animal physiology, with consequences potentially extending into adulthood. We combined RNAseq, targeted metabolomics and genomics to study the consequences of experimental evolution under juvenile undernutrition for metabolism of reproductively active adult females of Drosophila melanogaster. Compared to six Control populations maintained on standard diet, six Selected populations evolved for over 230 generations on a nutrient-poor larval diet showed major changes in adult gene expression and metabolite abundance. In particular, Selected flies were relatively deficient in essential amino acids and purine nucleotides, but showed overabundance of several non-essential amino-acids involved in purine synthesis and overexpression of multiple enzymes catalyzing this pathway. Selected flies also accumulated medium-chain acylcarnitines suggestive of congestion in beta-oxidation, possibly linked to deficiency of electron transporters. Some aspects of the metabolic profile of Selected flies resembled that of flies subject to starvation. Furthermore, differences between Selected and Control populations in adult gene expression were in general positively correlated with differences in larval expression, consistent with pleiotropy in gene regulation between the life stages. Finally, Selected flies were less fit in terms of fecundity than Controls even when both were raised under the conditions under which the Selected populations evolved. These results suggest that evolutionary adaptation to juvenile undernutrition has large pleiotropic consequences for adult metabolism, and that they are costly rather than adaptive for adult fitness.

Cis-regulatory polymorphism at fiz ecdysone oxidase contributes to polygenic evolutionary response to malnutrition in Drosophila

“…Only SNPs assessed as significantly differentiated between Selected and Control populations are plotted; for a full list of polymorphisms in this region see S1 Table . B. Expression of fiz in third instar larvae raised on the poor diet, based on previously published RNAseq data [11,19]. The values are averages from the two conditions used in that study (germ free and Acetobacter-inoculated); the expression in the two conditions was highly correlated across populations (r = 0.99).…”

“…To identify most promising candidates for genes causally mediating the evolutionary adaptation to nutritional conditions, we examined genes that were both differentially expressed between Selected and Control populations in a previously published RNAseq data [ 11 , 19 ] and had at least one candidate SNP within their sequence boundaries or 5kb upstream and downstream [ 18 ]. Of 102 such genes, the one with by far the largest difference in expression was fiz ( fezzik , CG9509, FBgn0030594).…”

“…B. Expression of fiz in third instar larvae raised on the poor diet, based on previously published RNAseq data [ 11 , 19 ]. The values are averages from the two conditions used in that study (germ free and Acetobacter -inoculated); the expression in the two conditions was highly correlated across populations ( r = 0.99).…”