The genomic architecture of adaptation to larval malnutrition points to a trade-off with adult starvation resistance inDrosophila

Abstract

Periods of nutrient shortage impose strong selection on animal populations. Experimental studies of genetic adaptation to nutrient shortage largely focus on resistance to acute starvation at adult stage; it is not clear how conclusions drawn from these studies extrapolate to other forms of nutritional stress. We studied the genomic signature of adaptation to chronic juvenile malnutrition in six populations of Drosophila melanogaster evolved for 150 generations on an extremely nutrient-poor larval diet. Comparison with control populations evolved on standard food revealed repeatable genomic differentiation between the two set of population, involving >3,000 candidate SNPs forming >100 independently evolving clusters. The candidate genomic regions were enriched in genes implicated in hormone, carbohydrate, and lipid metabolism, including some with known effects on fitness-related life-history traits. Rather than being close to fixation, a substantial fraction of candidate SNPs segregated at intermediate allele frequencies in all malnutrition-adapted populations. This, together with patterns of among-population variation in allele frequencies and estimates of Tajima's D, suggests that the poor diet results in balancing selection on some genomic regions. Our candidate genes for tolerance to larval malnutrition showed a high overlap with genes previously implicated in acute starvation resistance. However, adaptation to larval malnutrition in our study was associated with reduced tolerance to acute adult starvation. Thus, rather than reflecting synergy, the shared genomic architecture appears to mediate an evolutionary trade-off between tolerances to these two forms of nutritional stress.

Adaptation in outbred sexual yeast is repeatable, polygenic, and favors rare haplotypes

“…We observed very high levels of repeatability across evolutionary replicates within drugs, with responses over drugs being different from one another. The two previous studies in budding yeast starting from an outbred base appeared highly repeatable ( Burke et al, 2014;Kosheleva & Desai, 2018) as have several studies from flies (Burke et al, 2010;Hoedjes et al, 2019;Iranmehr et al, 2021;Jalvingh et al, 2014;Jha et al, 2015;Kang et al, 2016;Kawecki et al, 2021;Kelly & Hughes, 2019;Martins et al, 2014;Michalak et al, 2017;Phillips et al, 2016Phillips et al, , 2018Remolina et al, 2012;Tobler et al, 2014;Turner & Miller, 2012;Zhou et al, 2011). Contradictory results have occasionally been reported in flies, in which the level of repeatability is much lower across replicate populations (Barghi et al, 2019;Griffin et al, 2017;Hardy et al, 2018).…”

“…Here, we employ 18 founders, still far fewer than fly experiments, but much more variation than previous budding yeast E&R experiments. The bulk of previous E&R work in Drosophila has been carried out for fewer than 100 generations (Barghi et al, 2017;Barghi et al, 2019;Franssen et al, 2015;Griffin et al, 2017;Hardy et al, 2018;Huang et al, 2014;Jalvingh et al, 2014;Jha et al, 2015;Kelly & Hughes, 2019;Martins et al, 2014;Michalak et al, 2017;Orozco-terWengel et al, 2012;Remolina et al, 2012;Shahrestani et al, 2021;Sørensen et al, 2020;Tobler et al, 2014;Turner & Miller, 2012), with a handful of studies carried out for between 100 to 200 generations (Hoedjes et al, 2019;Iranmehr et al, 2021;Kawecki et al, 2021;Turner et al, 2011;Zhou et al, 2011) and only a few studies maintained for between 400 to greater than 900 generations (Burke et al, 2010;Phillips et al, 2016Phillips et al, , 2018. Minimum census population sizes in these studies have ranged from hundreds to greater than two thousand individuals (Shahrestani et al, 2021).…”

“…In contrast our study maintained population sizes one to two orders of magnitude greater. The majority of studies in flies have evolved 2-5 replicate populations under 2-3 selection regimens, with the exception of a recent study in D simulans which used 10 replicates (Barghi et al, 2019) as well as a recent study in D melanogaster which used 6 replicates (Kawecki et al, 2021). The physical size of haplotype blocks changing in concert in fly E&R experiments varies among experiments and is difficult to estimate, but studies have suggested that such blocks can extend over several megabases (Barghi et al, 2019;Franssen et al, 2015), a significant fraction of the 120Mb Drosophila genome.…”

“…A large number of studies in flies have claimed that adaptation in outbred sexuals is highly polygenic, with many loci throughout the genome responding to selection (Barghi et al, 2017;Barghi et al, 2019;Burke et al, 2010;Chandler, 2014;Clark et al, 2007;Coop et al, 2009;Griffin et al, 2017;Hardy et al, 2018;Hoedjes et al, 2019;Huang et al, 2014;Jha et al, 2015;Kang et al, 2016;Kawecki et al, 2021;Orozco-terWengel et al, 2012;Phillips et al, 2016;Remolina et al, 2012;Shahrestani et al, 2021;Sørensen et al, 2020;Tobler et al, 2014;Turner et al, 2011;Turner & Miller, 2012;Tusso et al, 2021), but to some extent the inference of polygenicity is based on a visual inspection of Manhattan plots. Very few studies attempt to estimate the minimum number of factors consistent with observed results.…”

“…E&R experiments are typically initiated from an outbred base population and then changes in the frequency of SNPs observed following adaptation (Barghi et al, 2017;Barghi et al, 2019;Burke et al, 2010;Franssen et al, 2015;Griffin et al, 2017;Hardy et al, 2018;Huang et al, 2014;Jalvingh et al, 2014;Jha et al, 2015;Kelly & Hughes, 2019;Martins et al, 2014;Michalak et al, 2017;Orozco-terWengel et al, 2012;Phillips et al, 2016Phillips et al, , 2018Remolina et al, 2012;Shahrestani et al, 2021;Sørensen et al, 2020;Tobler et al, 2014;Turner & Miller, 2012;Hoedjes et al, 2019;Iranmehr et al, 2021;Kawecki et al, 2021;Turner et al, 2011;Zhou et al, 2011). Such studies have several strengths, but it is difficult to distinguish SNPs that are drivers versus responders.…”