Parallel Evolution of Cold Tolerance Within Drosophila melanogaster

Abstract

Drosophila melanogaster originated in tropical Africa before expanding into strikingly different temperate climates in Eurasia and beyond. Here, we find elevated cold tolerance in three distinct geographic regions: beyond the well-studied non-African case, we show that populations from the highlands of Ethiopia and South Africa have significantly increased cold tolerance as well. We observe greater cold tolerance in outbred versus inbred flies, but only in populations with higher inversion frequencies. Each cold-adapted population shows lower inversion frequencies than a closely-related warm-adapted population, suggesting that inversion frequencies may decrease with altitude in addition to latitude. Using the FST-based “Population Branch Excess” statistic (PBE), we found only limited evidence for parallel genetic differentiation at the scale of ∼4 kb windows, specifically between Ethiopian and South African cold-adapted populations. And yet, when we looked for single nucleotide polymorphisms (SNPs) with codirectional frequency change in two or three cold-adapted populations, strong genomic enrichments were observed from all comparisons. These findings could reflect an important role for selection on standing genetic variation leading to “soft sweeps”. One SNP showed sufficient codirectional frequency change in all cold-adapted populations to achieve experiment-wide significance: an intronic variant in the synaptic gene Prosap. Another codirectional outlier SNP, at senseless-2, had a strong association with our cold trait measurements, but in the opposite direction as predicted. More generally, proteins involved in neurotransmission were enriched as potential targets of parallel adaptation. The ability to study cold tolerance evolution in a parallel framework will enhance this classic study system for climate adaptation.

The adaptive significance of chromosomal inversion polymorphisms inDrosophila melanogaster

“…van Delden and Kamping (1991) also found effects of In(2L)t on fitness traits, showing that inverted homokaryotypes had longer development time and lower body weight than the heterokaryotypes and noninverted standard homokaryotypes. Weeks et al (2002) found that the frequency of In(3L)P is negatively associated with cold resistance-an observation consistent with the findings of Anderson et al (2003) and Durmaz et al (2018) for In(3R)Payne and those of Pool et al (2017) showing that African highland populations are more cold-tolerant but have lower frequencies of common inversion polymorphisms. Given the tropical African origin of common cosmopolitan inversions, and their typically higher frequency in warmer climates, the negative relationship between their frequency and cold tolerance is intriguing and strongly points to a direct causal involvement of these chromosomal rearrangements in climate adaptation.…”

“…For example, in African populations of D. melanogaster the four common polymorphisms tend to be more frequent in tropical lowland sites as compared to high-altitude locations, perhaps suggesting that the continent-wide latitudinal clines are locally mirrored by altitudinal clines (Pool et al, 2017; also see discussion in Klepsatel, Gáliková, Huber, & Flatt, 2014;and Fabian et al, 2015). In addition, there is evidence that several inversions, especially In(2L)t and In(3L) P, exhibit longitudinal clinality, although such clines tend to be less pronounced and often covary with latitudinal patterns (see Figure 2, Supporting Information Table S2; Aulard et al, 2002;Kapun et al, 2018;Kapopoulou et al, 2018;Knibb, 1982).…”

“…The In(2L)t, In(2R) NS,In(3LP) and In(3R)P polymorphisms have received particular attention because they exhibit a cosmopolitan distribution-the fact that they are common and geographically widespread might be a first-albeit inconclusive-hint that they might be maintained by selection. Beginning in the 1970s, many studies performed comprehensive surveys of the frequencies of these inversions in North America (Fabian et al, 2012;Kapun, Fabian et al, 2016;Knibb, 1982;Machado et al, 2018;Mettler et al, 1977;Sezgin et al, 2004;Stalker, 1976Stalker, , 1980Voelker et al, 1978), Australia (Anderson, Knibb, & Oakeshott, 1987;Knibb, 1982Knibb, , 1986Knibb, Oakeshott, & Gibson, 1981), Southern and Eastern Asia (Das & Singh, 1990Glinka, Stephan, & Das, 2005;Inoue & Igarashi, 1994;Inoue & Watanabe, 1979;Singh & Das, 1992) and-to a lesser extent-in Africa and Europe (Aguadé & Serra, 1980;Aulard, David, & Lemeunier, 2002;Aulard & Lemeunier, 1985;Kapun et al, 2018;Pool, Braun, & Lack, 2017;Taberner & González, 1991;Zacharopoulou & Pelecanos, 1980). Overall, these studies reveal that these inversions are typically more common in low-latitude populations from subtropical/tropical climates than in high-latitude populations from temperate regions where they are at low frequency or absent (see the meta-analysis below; Figure 2, Supporting Information Tables S1 and S2; also cf.…”

Stress response, behavior, and development are shaped by transposable element-induced mutations in Drosophila

“…Thus, it is likely that by exploring more natural populations we could identify additional adaptive insertions. We are also missing TEs that could be playing a role in seasonal and altitudinal adaptation, as both dimensions have been shown to be relevant for D. melanogaster [74-76]. Finally, our study is also limited to those insertions present in the reference genome.…”

A simple and dynamic thermal gradient device for measuring thermal performance in small ectotherms

“…As insects are easily manipulated and maintained in the lab, model insect species are widely used for studies of the genetics, molecular biology, environmental physiology, behaviour, and evolution of thermal performance traits [3][4][5][6][7]. Laboratory studies of Drosophila thermal tolerance, for example, have recently allowed for investigation of the molecular or physiological processes that limit their biogeography, and how limits to thermal performance may evolve following changes in abiotic conditions [4,[8][9][10].…”