Gene regulatory evolution in cold-adapted fly populations neutralizes plasticity and may undermine genetic canalization

Abstract

The relationships between adaptive evolution, phenotypic plasticity, and canalization remain incompletely understood. Theoretical and empirical studies have made conflicting arguments on whether adaptive evolution may enhance or oppose the plastic response. Gene regulatory traits offer excellent potential to study the relationship between plasticity and adaptation, and they can now be studied at the transcriptomic level. Here we take advantage of three closely-related pairs of natural populations of Drosophila melanogaster from contrasting thermal environments that reflect three separate instances of cold tolerance evolution. We measure the transcriptome-wide plasticity in gene expression levels and alternative splicing (intron usage) between warm and cold laboratory environments. We find that suspected adaptive changes in both gene expression and alternative splicing tend to neutralize the ancestral plastic response. Further, we investigate the hypothesis that adaptive evolution can lead to decanalization of selected gene regulatory traits. We find strong evidence that suspected adaptive gene expression (but not splicing) changes in cold-adapted populations are more vulnerable to the genetic perturbation of inbreeding than putatively neutral changes. We find some evidence that these patterns may reflect a loss of genetic canalization accompanying adaptation, although other processes including hitchhiking recessive deleterious variants may contribute as well. Our findings augment our understanding of genetic and environmental effects on gene regulation in the context of adaptive evolution.

An Ancestral Balanced Inversion Polymorphism Confers Global Adaptation

“…(5) RNA-seq analyses of inverted and standard chromosomes in a sample from North America (Florida) reveal pronounced effects of inversion karyotype on gene expression that depend on developmental temperature: expression levels are higher for inverted chromosomes at low temperature, perhaps due to a loss of buffering or compensatory plasticity (cf. Huang et al 2022) and consistent with the notion that 3R Payne is susceptible to cool conditions (see above; cf. Kapun et al 2016a;Pool et al 2017;Kapun and Flatt 2019).…”

“…This suggests that variants associated with the inverted arrangement might be more sensitive to lower temperatures, maybe due to a loss of buffering or because of increased compensatory plasticity at 18°C (cf. Huang et al 2022), lending further support to the role of 3R Payne in climate adaptation (also see Pool et al 2016). These 'non-local' effects on DE suggest that the 3R Payne inversion exerts major transacting regulatory effects (cf.…”

Distinct signals of clinal and seasonal allele frequency change at eQTLs in Drosophila melanogaster

“…2015), and evidence suggests that whether plasticity is adaptive or maladaptive varies between populations (Huang et al. 2022) and among traits (Huang and Agrawal 2016; Mallard et al. 2020).…”

“…The first is that expression plasticity is adaptive. Whether this assumption is valid in general is an open question (Ghalambor et al 2015), and evidence suggests that whether plasticity is adaptive or maladaptive varies between populations (Huang et al 2022) and among traits (Huang and Agrawal 2016;Mallard et al 2020). The tests also assume that the environment changes in a specific way through space and time.…”

Disentangling the developmental origins of a novel phenotype: enhancement versus reversal of environmentally induced gene expression

“…The negative relationship observed in the liver between changes in gene expression induced by the environment and those induced by phenotypic accommodation recalls the pattern often seen during evolutionary adaptation. Recent work has shown that adaptation to a new environment often reverses or ‘neutralizes’ the gene expression responses a population first exhibits in that environment (in fish brain: [46], in lizard skeletal muscle: [47], in fish muscle: [50,51], in bacteria, yeast and fish brains: [52], in whole beetle carcass: [53], in fruit fly: [54]). That such a reversal seen during adaptation is also elicited by phenotypic accommodation supports the longstanding claim that phenotypic accommodation represents an initial stage of adaptive evolution [4,5,10,55].…”