Abstract

Signatures of spatially varying selection have been investigated both at the genomic and transcriptomic level in several organisms. In Drosophila melanogaster, the majority of these studies have analyzed North American and Australian populations, leading to the identification of several loci and traits under selection. However, several studies based mainly in North American populations showed evidence of admixture that likely contributed to the observed population differentiation patterns. Thus, disentangling demography from selection might be challenging when analyzing these populations. European populations could help identify loci under spatially varying selection provided that no recent admixture from African populations would have occurred. In this work, we individually sequence the genome of 42 European strains collected in populations from contrasting environments: Stockholm (Sweden) and Castellana Grotte (Southern Italy). We found low levels of population structure and no evidence of recent African admixture in these two populations. We thus look for patterns of spatially varying selection affecting individual genes and gene sets. Besides single nucleotide polymorphisms, we also investigated the role of transposable elements in local adaptation. We concluded that European populations are a good dataset to identify candidate loci under spatially varying selection. The analysis of the two populations sequenced in this work in the context of all the available D. melanogaster data allowed us to pinpoint genes and biological processes likely to be relevant for local adaptation. Identifying and analyzing populations with low levels of population structure and admixture should help to disentangle selective from non-selective forces underlying patterns of population differentiation in other species as well.

Highlights

  • Understanding how organisms adapt to their environment and which genes and which biological processes are more relevant for adaptation are still open questions in evolutionary biology

  • To investigate the genetic diversity, population structure, and admixture patterns in European populations in the context of a more global dataset of natural populations, we used a joint genotyping strategy to call Single Nucleotide Polymorphisms (SNPs) in strains from these two European populations, one North American population (24 strains collected in Raleigh, North Carolina, USA)[44], and one African population collected in the ancestral range of the species (17 strains sequenced from haploid embryos, Gikongoro, Rwanda, Africa)[43] (Table S2, Supporting Information)

  • We estimated genome-wide diversity levels (π) for the two European populations sequenced in this study, and for the North American and African strains[43,44] (Fig. 2 and Table S3a, Supporting information)

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Summary

Introduction

Understanding how organisms adapt to their environment and which genes and which biological processes are more relevant for adaptation are still open questions in evolutionary biology. Insights on the genomic targets of spatially varying selection, the molecular mechanisms underpinning local adaptation, and the extent of parallel adaptation, in model and non-model species, is starting to accumulate[1,2,3] Several challenges such as the role of demography in the observed population differentiation patterns, and the identification of the true targets of spatially varying selection still remain[7]. D. melanogaster has several characteristics that makes it an exceptional organism to pinpoint adaptive variants, and to advance our knowledge on the genes and biological processes that are more relevant for adaptation This species has recently (10.000–16.000 years ago) colonized worldwide environments from its ancestral range in subtropical Africa[8]. Populations from the European continent might be a good dataset to identify loci under spatially varying selection as no evidence of admixture has been reported for the populations studied to date[22]

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