The Evolution of Larger Size in High Altitude Drosophila melanogaster has a Polymorphic Genetic Architecture

Important uncertainties persist regarding the genetic architecture of adaptive trait evolution in natural populations, including the number of genetic variants involved, whether they are drawn from standing genetic variation, and whether directional selection drives them to complete fixation. Here, we take advantage of a unique natural population of Drosophila melanogaster from the Ethiopian highlands, which has evolved larger body size than any other known population of this species. We apply a bulk segregant quantitative trait locus (QTL) mapping approach to four unique crosses between highland Ethiopian and lowland Zambian populations for both thorax length and wing length. Results indicated a persistently variable genetic basis for these evolved traits (with largely distinct sets of QTLs for each cross), and at least a moderately polygenic architecture with relatively strong effects present. We complemented these mapping experiments with population genetic analyses of QTL regions and gene ontology enrichment analysis, generating strong hypotheses for specific genes and functional processes that may have contributed to these adaptive trait changes.Finally, we find that our QTL mapping results for size traits mirror those from similar experiments on other traits. Collectively, these studies suggest a recurring pattern of polygenic adaptation in this species, in which causative variants do not approach fixation and moderately strong effect loci are present.

当前，自然种群适应性性状演化的遗传架构仍存在诸多关键待解问题，包括所涉及的遗传变异数量、这些变异是否源自现存遗传变异，以及定向选择是否会驱使它们完全固定。本研究依托一个独特的埃塞俄比亚高地野生黑腹果蝇（Drosophila melanogaster）种群，该种群的体型较该物种所有已知野生种群更为庞大。我们针对埃塞俄比亚高地种群与赞比亚低地种群间的4组独特杂交组合，对胸长和翅长两个性状采用集群分离数量性状位点（quantitative trait locus, QTL）定位法开展分析。结果显示，这些演化而来的性状的遗传基础存在显著差异（每个杂交组合的QTL集合大多互不相同），且至少具备中度多基因遗传架构，同时存在效应较强的位点。我们通过对QTL区域的群体遗传学分析与基因本体（gene ontology, GO）富集分析对该定位实验进行补充，进而为可能参与这些适应性性状改变的特定基因与功能过程提出了强有力的假说。最后，我们发现本次针对体型性状的QTL定位结果，与其他针对不同性状的同类实验结果高度吻合。综合来看，本研究表明该物种存在多基因适应性演化的重复模式：即致因变异不会趋近于固定，且存在效应中等偏强的位点。