Drainage-structuring of ancestral variation and a common functional pathway shape limited genomic convergence in natural high- and low-predation guppies.

Drainage-structuring of ancestral variation and a common functional pathway shape limited genomic convergence in natural high- and low-predation guppies.
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DOI:
10.1371/journal.pgen.1009566
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发表时间:
2021-05
期刊:
影响因子:
4.5
通讯作者:
Fraser BA
Fraser BA
中科院分区:
生物学2区
文献类型:
--
作者:
Whiting JR;Paris JR;van der Zee MJ;Parsons PJ;Weigel D;Fraser BA

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对野生种群趋同的研究通过提供自然选择的有力证据,有助于理解适应。在遗传水平上,我们开始认识到,在适应中重复使用相同的基因是通过不同的机制发生的,并且可能受到自然种群潜在性状结构和人口统计学特征的限制。在这里,我们在特立尼达孔雀鱼(Poecilia reticulata)的自然适应高(HP)和低捕食(LP)种群中探索这些过程。作为表型变化的模型,该系统为脊椎动物的快速和可重复进化提供了一些最早的证据;其遗传基础尚未在全基因组水平上进行研究。我们收集了来自10个种群(176个个体)的全基因组测序数据,这些种群代表了特立尼达北部三个主要流域的5对独立的HP-LP河流。我们评估了种群结构,揭示了几个LP瓶颈和可变的河流间渗入,这可能导致种群之间共享适应性变异的限制。因此,我们发现在所有流域中对共同基因或位点的选择有限。然而,通过途径类型分析,我们发现了钙粘蛋白信号传导中不同基因的重复选择的证据。最后,在来自同一流域的三条河流中,我们在20号染色体上发现了一个重复选择的大单倍型。综上所述,尽管河流之间的适应性变异共享有限,但我们发现了与HP-LP环境相关的趋同进化的证据,这些趋同进化存在于跨越不同流域的途径中,以及以前未报道的流域内的候选单倍型中。趋同进化是指在独立谱系中,相似表型在共同选择下进化的过程,为适应自然选择提供了强有力的证据。这一过程可能涉及基因组相同区域的变化,称为基因组趋同。我们在高捕食和低捕食的特立尼达孔雀鱼的复制进化中探索了这一点,这是表型进化研究的一个重要模型系统,但对潜在的遗传学知之甚少。我们的发现强调了遗传变异如何分布的局限性,限制了相同的突变或基因参与高捕食性和低捕食性孔雀鱼的趋同进化,但可能涉及功能相似的不同基因。我们还强调并研究了一个与来自同一流域的三条河流相关的大型候选区域。我们的研究结果在一定程度上证明了基因组趋同的局限性,但表明在这个重要的模型系统中,趋同表型进化的遗传基础具有一定的可重复性。因此,孔雀鱼系统中的基因组趋同比其他突出的研究系统更为有限,这表明自然界中这一过程的普遍性是高度依赖于环境的。
Studies of convergence in wild populations have been instrumental in understanding adaptation by providing strong evidence for natural selection. At the genetic level, we are beginning to appreciate that the re-use of the same genes in adaptation occurs through different mechanisms and can be constrained by underlying trait architectures and demographic characteristics of natural populations. Here, we explore these processes in naturally adapted high- (HP) and low-predation (LP) populations of the Trinidadian guppy, Poecilia reticulata. As a model for phenotypic change this system provided some of the earliest evidence of rapid and repeatable evolution in vertebrates; the genetic basis of which has yet to be studied at the whole-genome level. We collected whole-genome sequencing data from ten populations (176 individuals) representing five independent HP-LP river pairs across the three main drainages in Northern Trinidad. We evaluate population structure, uncovering several LP bottlenecks and variable between-river introgression that can lead to constraints on the sharing of adaptive variation between populations. Consequently, we found limited selection on common genes or loci across all drainages. Using a pathway type analysis, however, we find evidence of repeated selection on different genes involved in cadherin signaling. Finally, we found a large repeatedly selected haplotype on chromosome 20 in three rivers from the same drainage. Taken together, despite limited sharing of adaptive variation among rivers, we found evidence of convergent evolution associated with HP-LP environments in pathways across divergent drainages and at a previously unreported candidate haplotype within a drainage. Convergent evolution is the process whereby similar phenotypes evolve in response to common selection in independent lineages, providing strong evidence of adaptation in response to natural selection. This process can involve changes at the same regions of the genome, known as genomic convergence. We explore this in the replicated evolution of high- and low-predation Trinidadian guppies, an important model system for studies of phenotypic evolution, but where little is known about the underlying genetics. Our findings highlight that limitations on how genetic variation is distributed have restricted the same mutations or genes being involved in the convergent evolution of high- and low-predation guppies, but different genes of similar function are likely involved. We also highlight and examine a large candidate region associated with three rivers from the same drainage. Our results demonstrate constraints on genomic convergence at certain levels, but suggest there is some repeatability in the genetic basis of convergent phenotypic evolution in this important model system. Genomic convergence in the guppy system is therefore more limited than in other prominent study systems, suggesting the pervasiveness of this process in nature is highly context-dependent.
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