Evolution of Plasticity in Response to Ethanol between Sister Species with Different Ecological Histories (Drosophila melanogasterandD. simulans)

Abstract

The contribution of phenotypic plasticity to adaptation is contentious, with contradictory empirical support for its role in evolution. Here I investigate the possibility that phenotype plasticity has contributed to adaptation to a novel resource. If phenotype plasticity contributes to adaptation, it is thought to evolve in a process termed genetic accommodation. Under this model, the initial response to the environment is widely variable due to cryptic genetic variation, which is then refined by selection to a single adaptive response. I examine the role of phenotypic plasticity in adaptation here by comparing two species of Drosophila that differ in their adaptation to ethanol (Drosophila melanogaster and D. simulans). Both species are human commensals with a recent cosmopolitan expansion, but only D. melanogaster is adapted to ethanol exposure. I measure phenotype plasticity in response to ethanol with gene expression and an approach that combines information about expression and alternative splicing. I find evidence for adaptation to ethanol through genetic accommodation, suggesting that the evolution of phenotype plasticity contributed to the ability of D. melanogaster to exploit a novel resource. I also find evidence that alternative splicing may be more important for the adaptive response to ethanol than overall changes in exon expression.

Selection on structural allelic variation biases plasticity estimates

“…Additionally, Wang and Althoff () quantified ADH activity rather than overall gene expression changes, and the fitness effect of the latter is much less clear than the former. Furthermore, we do not think that a lack of significant genes for interaction variance in response to alcohol in Signor and Nuzhdin () is sufficient reason to suggest that there is no genetic variation in ADH plasticity.…”

“…We have explained a source of bias that can arise when sib‐groups are used as surrogates of replicated genotypes. Interestingly, a recent preprint by Signor and Nuzhdin () has also analyzed plastic responses to high ethanol concentration in D . melanogaster and D .…”

“…However, aside from methodological differences between the two studies, there are additional differences to consider. The use of adults (Signor and Nuzhdin ) versus larvae (Wang and Althoff ) is important for interpreting the results, because the regulation of ADH expression is known to be under separate genetic control in these two life stages (Posakony et al. ).…”

Phenotypic Plasticity & Evolution

“…Convergence of responses on an adaptive reaction norm will also shield unexpressed genetic variants among those genotypes from selection Schwab et al 2019). Signor (2020) documents the canalization of reaction norms in a comparison of ethanol tolerance in Drosophila simulans-possessing the ancestral non-tolerant phenotype-and D. melanogaster-with an evolved tolerance to ethanol. She finds substantial genetic variation in the reaction norms of gene expression to ethanol of D. simulans but no such variation in D. melanogaster, a lack of variation expected if an ethanol tolerant reaction norm had been strongly selected.…”

Transposable elements in individual genotypes of Drosophila simulans

“…The first read from each pair was used for mapping. The 169 California lines were collected from the Zuma Organic Orchard in Los Angeles, CA, on two consecutive weekends of February 2012 (Table 1; Signor, New, & Nuzhdin, 2017; Signor & Nuzhdin, 2018, 2019). Reads were single‐end 100 bp, and this project has been deposited at the SRA under accession SRP075682.…”