Fuller Zachary L, Haynes Gwilym D, Richards Stephen, Schaeffer Stephen W
Department of Biology, 208 Erwin W. Mueller Laboratory, The Pennsylvania State University, University Park, PA, USA.
Human Genome Sequencing Center, Baylor College of Medicine, Houston, TX, USA.
Mol Ecol. 2017 Dec;26(23):6539-6562. doi: 10.1111/mec.14381. Epub 2017 Nov 15.
The evolution of complex traits in heterogeneous environments may shape the order of genes within chromosomes. Drosophila pseudoobscura has a rich gene arrangement polymorphism that allows one to test evolutionary genetic hypotheses about how chromosomal inversions are established in populations. D. pseudoobscura has >30 gene arrangements on a single chromosome that were generated through a series of overlapping inversion mutations with >10 inversions with appreciable frequencies and wide geographic distributions. This study analyses the genomic sequences of 54 strains of Drosophila pseudoobscura that carry one of six different chromosomal arrangements to test whether (i) genetic drift, (ii) hitchhiking with an adaptive allele, (iii) direct effects of inversions to create gene disruptions caused by breakpoints, or (iv) indirect effects of inversions in limiting the formation of recombinant gametes are responsible for the establishment of new gene arrangements. We found that the inversion events do not disrupt the structure of protein coding genes at the breakpoints. Population genetic analyses of 2,669 protein coding genes identified 277 outlier loci harbouring elevated frequencies of arrangement-specific derived alleles. Significant linkage disequilibrium occurs among distant loci interspersed between regions with low levels of association indicating that distant allelic combinations are held together despite shared polymorphism among arrangements. Outlier genes showing evidence of genetic differentiation between arrangements are enriched for sensory perception and detoxification genes. The data presented here support the indirect effect of inversion hypothesis where chromosomal inversions are favoured because they maintain linked associations among multilocus allelic combinations among different arrangements.
复杂性状在异质环境中的进化可能会塑造染色体上基因的排列顺序。拟暗果蝇具有丰富的基因排列多态性，这使得人们能够检验关于染色体倒位在种群中如何建立的进化遗传学假设。拟暗果蝇在一条染色体上有超过30种基因排列，这些排列是通过一系列重叠的倒位突变产生的，其中有超过10种倒位具有可观的频率和广泛的地理分布。本研究分析了54株携带六种不同染色体排列之一的拟暗果蝇的基因组序列，以检验以下因素是否导致了新基因排列的建立：（i）遗传漂变；（ii）与适应性等位基因的搭便车效应；（iii）倒位通过断点造成基因破坏的直接效应；或（iv）倒位在限制重组配子形成方面的间接效应。我们发现倒位事件在断点处不会破坏蛋白质编码基因的结构。对2669个蛋白质编码基因的群体遗传学分析确定了277个异常位点，这些位点含有特定排列衍生等位基因的频率升高。在低关联区域之间散布的远距离位点之间发生了显著的连锁不平衡，这表明尽管排列之间存在共享多态性，但远距离等位基因组合仍被维系在一起。显示出排列之间遗传分化证据的异常基因在感觉感知和解毒基因中富集。本文提供的数据支持倒位假说的间接效应，即染色体倒位受到青睐是因为它们维持了不同排列之间多位点等位基因组合的连锁关联。
