Population genetic evidence for cold adaptation in European Drosophila melanogaster populations

et al. 2016

Genetics

Unraveling the genetic architecture of adaptive phenotypic divergence is a fundamental quest in evolutionary biology. In Drosophila melanogaster, high-altitude melanism has evolved in separate mountain ranges in sub-Saharan Africa, potentially as an adaptation to UV intensity. We investigated the genetic basis of this melanism in three populations using a new bulk segregant analysis mapping method. We identified 19 distinct QTL regions from nine mapping crosses, with several QTL peaks overlapping between two or all populations, and yet different crosses involving the same melanic population commonly yielded distinct QTL. The strongest QTL often overlapped well-known pigmentation genes, but we typically did not find wide signals of genetic differentiation (FST) between lightly and darkly pigmented populations at these genes. Instead, we found small numbers of highly differentiated SNPs at the probable causative genes. A simulation analysis showed that these patterns of polymorphism were consistent with selection on standing genetic variation. Overall, our results suggest that, even for potentially simpler traits like pigmentation, the complexity of adaptive trait evolution poses important challenges for QTL mapping and population genetic analysis.

Section: Discussionmentioning

confidence: 61%

A Variable Genetic Architecture of Melanic Evolution inDrosophila melanogaster

Bastide¹,

Lange²,

et al. 2016

Genetics

“…Along these clines, populations exhibit different degrees of cold tolerance in the expected direction, suggesting spatially varying selection related to temperature (Hoffmann and Weeks 2007; Schmidt and Paaby 2008). The recent development of genomics has allowed identification of clinal genomic variants, which are candidates for thermal adaptation (e.g., Kolaczkowski et al 2011; Fabian et al 2012; Bozicevic et al 2016; Mateo et al 2018). There is also evidence of parallel evolution at the genomic and transcriptomic level (Reinhardt et al 2014; Bergland et al 2015; Machado et al 2015; Zhao et al 2015; Juneja et al 2016; Zhao and Begun 2017).…”

Section: Introductionmentioning

confidence: 99%

Parallel and Population-specific Gene Regulatory Evolution in Cold-Adapted Fly Populations

Huang

Hoppel

et al. 2019

Preprint

17Changes in gene regulation at multiple levels may comprise an important share of the molecular 18 changes underlying adaptive evolution in nature. However, few studies have assayed within-and 19 between-population variation in gene regulatory traits at a transcriptomic scale, and therefore 20 inferences about the characteristics of adaptive regulatory changes have been elusive. Here, we assess 21 quantitative trait differentiation in gene expression levels and alternative splicing (intron usage) 22 between three closely-related pairs of natural populations of Drosophila melanogaster from contrasting 23 thermal environments that reflect three separate instances of cold tolerance evolution. The cold-24 adapted populations were known to show population genetic evidence for parallel evolution at the 25 SNP level, and here we find significant although somewhat limited evidence for parallel expression 26 evolution between them, and less evidence for parallel splicing evolution. We find that genes with 27 mitochondrial functions are particularly enriched among candidates for adaptive expression 28 evolution. We also develop a method to estimate cis-versus trans-encoded contributions to 29 expression or splicing differences that does not rely on the presence of fixed differences between 30 parental strains. Applying this method, we infer important roles of both cis-and trans-regulation 31 among our putatively adaptive expression and splicing differences. The apparent contributions of cis-32 versus trans-regulation to adaptive evolution vary substantially among population pairs, with an 33 Ethiopian pair showing pervasive trans-effects, suggesting that basic characteristics of regulatory 34 evolution may depend on biological context. These findings expand our knowledge of adaptive gene 35 regulatory evolution and our ability to make inferences about this important and widespread process.36 37 50 The level of parallelism for gene expression abundance changes varies across study systems. In some 51 taxa and natural conditions, significantly more genes show parallel changes (repeatedly up-or down-52 regulated in one ecotype relative to the other among independent population pairs) than anti-53 directional changes (Zhao et al. 2015; Hart et al. 2018; Kitano et al. 2018; McGirr and Martin.54 2018). However, some other cases did not show significant parallel patterns, or they even show anti-55 parallel patterns (Derome et al. 2006; Lai et al. 2008; Hanson et al. 2017). The varying degree of 56 parallelism may partly be explained by the level of divergence among ancestors: more closely related 57 ancestors are expected to show a higher degree of parallel genetic evolution underlie similar 58 phenotypic evolution (Conte et al. 2012; Rosenblum et al. 2014). 59 60 Furthermore, gene expression evolution can be caused by the same or different molecular 61 underpinnings. Because of the difficulties of mapping expression QTL, a first step is to classify the 62 expression evolution into two regulatory classes. Cis-regulatory change...

“…The expansion of D. melanogaster from Africa into Eurasia, which occurred roughly 10,000 years ago (Thornton and Andolfatto 2006; Duchen et al 2013), may have involved novel genetic adaptation to cold environments. This apparent instance of cold tolerance evolution has been studied via comparisons between European and sub-Saharan African populations (Cohet et al 1980; Svetec et al 2011; Božičević et al 2016). However, the species’ sub-Saharan exodus entailed a strong population bottleneck that complicates the population genetic detection of adaptive differences between sub-Saharan and European populations, by stochastically increasing the level of neutral genome-wide differentiation between these populations.…”

Section: Introductionmentioning

confidence: 99%

Parallel Evolution of Cold Tolerance Within Drosophila melanogaster

Pool

Braun²,

2016

Mol Biol Evol

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.