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Gene Flow Increases Phylogenetic Structure and Inflates Cryptic Species Estimations: A Case Study on Widespread Philippine Puddle Frogs (Occidozyga laevis)
Systematic Biology ( IF 6.1 ) Pub Date : 2021-05-06 , DOI: 10.1093/sysbio/syab034
Kin Onn Chan, Carl R Hutter, Perry L Wood, Yong-Chao Su, Rafe M Brown

In cryptic amphibian complexes, there is a growing trend to equate high levels of genetic structure with hidden cryptic species diversity. Typically, phylogenetic structure and distance-based approaches are used to demonstrate the distinctness of clades and justify the recognition of new cryptic species. However, this approach does not account for gene flow, spatial, and environmental processes that can obfuscate phylogenetic inference and bias species delimitation. As a case study, we sequenced genome-wide exons and introns to evince the processes that underlie the diversification of Philippine Puddle Frogs—a group that is widespread, phenotypically conserved, and exhibits high levels of geographically based genetic structure. We showed that widely adopted tree- and distance-based approaches inferred up to 20 species, compared to genomic analyses that inferred an optimal number of five distinct genetic groups. Using a suite of clustering, admixture, and phylogenetic network analyses, we demonstrate extensive admixture among the five groups and elucidate two specific ways in which gene flow can cause overestimations of species diversity: 1) admixed populations can be inferred as distinct lineages characterized by long branches in phylograms; and 2) admixed lineages can appear to be genetically divergent, even from their parental populations when simple measures of genetic distance are used. We demonstrate that the relationship between mitochondrial and genome-wide nuclear $p$-distances is decoupled in admixed clades, leading to erroneous estimates of genetic distances and, consequently, species diversity. Additionally, genetic distance was also biased by spatial and environmental processes. Overall, we showed that high levels of genetic diversity in Philippine Puddle Frogs predominantly comprise metapopulation lineages that arose through complex patterns of admixture, isolation-by-distance, and isolation-by-environment as opposed to species divergence. Our findings suggest that speciation may not be the major process underlying the high levels of hidden diversity observed in many taxonomic groups and that widely adopted tree- and distance-based methods overestimate species diversity in the presence of gene flow. [Cryptic species; gene flow; introgression; isolation-by-distance; isolation-by-environment; phylogenetic network; species delimitation.]

中文翻译:

基因流增加系统发育结构并夸大隐蔽物种估计:以广泛分布的菲律宾水蛙 (Occidozyga laevis) 为例

在神秘的两栖动物群中,将高水平的遗传结构与隐藏的神秘物种多样性等同起来的趋势越来越明显。通常,系统发育结构和基于距离的方法用于证明进化枝的独特性并证明识别新的神秘物种的合理性。然而,这种方法没有考虑到基因流、空间和环境过程,这些过程可能会混淆系统发育推断和偏向物种界定。作为一个案例研究,我们对全基因组的外显子和内含子进行了测序,以证明菲律宾水坑蛙多样化的过程——一个分布广泛、表型保守且表现出高水平地理遗传结构的群体。我们表明,广泛采用的基于树和距离的方法可以推断出多达 20 个物种,与推断出五个不同遗传组的最佳数量的基因组分析相比。使用一套聚类、混合和系统发育网络分析,我们证明了这五个群体之间的广泛混合,并阐明了基因流动可能导致物种多样性高估的两种具体方式:1)混合种群可以推断为具有长期特征的不同谱系。系统图中的分支;2) 混合血统在遗传上可能看起来是不同的,即使在使用简单的遗传距离测量时,甚至与它们的亲代种群也是如此。我们证明线粒体和全基因组核$p$-距离之间的关系在混合进化枝中解耦,导致对遗传距离的错误估计,从而导致物种多样性。此外,遗传距离也受到空间和环境过程的影响。总体而言,我们发现菲律宾水坑蛙的高水平遗传多样性主要包括通过复杂的混合模式、距离隔离和环境隔离而不是物种分化而产生的元种群谱系。我们的研究结果表明,物种形成可能不是在许多分类群中观察到的高水平隐藏多样性的主要过程,并且广泛采用的基于树和距离的方法在基因流存在的情况下高估了物种多样性。[神秘物种;基因流;基因渗入;距离隔离;环境隔离;系统发育网络;物种划分。] 我们发现,菲律宾水坑蛙的高水平遗传多样性主要包括通过复杂的混合模式、距离隔离和环境隔离而不是物种分化而产生的元种群谱系。我们的研究结果表明,物种形成可能不是在许多分类群中观察到的高水平隐藏多样性的主要过程,并且广泛采用的基于树和距离的方法在基因流存在的情况下高估了物种多样性。[神秘物种;基因流;基因渗入;距离隔离;环境隔离;系统发育网络;物种划分。] 我们发现,菲律宾水坑蛙的高水平遗传多样性主要包括通过复杂的混合模式、距离隔离和环境隔离而不是物种分化而产生的元种群谱系。我们的研究结果表明,物种形成可能不是在许多分类群中观察到的高水平隐藏多样性的主要过程,并且广泛采用的基于树和距离的方法在基因流存在的情况下高估了物种多样性。[神秘物种;基因流;基因渗入;距离隔离;环境隔离;系统发育网络;物种划分。] 我们的研究结果表明,物种形成可能不是在许多分类群中观察到的高水平隐藏多样性的主要过程,并且广泛采用的基于树和距离的方法在基因流存在的情况下高估了物种多样性。[神秘物种;基因流;基因渗入;距离隔离;环境隔离;系统发育网络;物种划分。] 我们的研究结果表明,物种形成可能不是在许多分类群中观察到的高水平隐藏多样性的主要过程,并且广泛采用的基于树和距离的方法在基因流存在的情况下高估了物种多样性。[神秘物种;基因流;基因渗入;距离隔离;环境隔离;系统发育网络;物种划分。]
更新日期:2021-05-06
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