物种形成过程中的分化基因组岛及其形成机制

doi:10.17520/biods.2021383

摘要/Abstract

摘要：

理解物种形成机制是生态和进化领域的重要任务。得益于测序技术的快速发展, 越来越多研究发现分化种群(亚种、物种)间的基因组常呈现异质性分化景观, 存在分化基因组岛, 这被认为是基因流存在下的歧化选择引起的, 支持基因流存在下的成种假说。然而, 基因渐渗、祖先多态性的差异分选、连锁选择等其他进化过程也可导致分化基因组岛的形成。现有实证研究在解析分化基因组岛的形成机制时, 往往忽略了上述其他进化过程的作用。为此, 本文在辨析分化基因组岛相关概念的基础上, 总结了利用种群基因组数据鉴定分化基因组岛的方法, 对比了不同进化过程形成分化基因组岛的特征, 指出在区分不同机制时联用基因渐渗程度、绝对分化指数(d_XY)、相对节点深度(RND)、重组率等多个指标的必要性, 归纳了物种形成过程中分化基因组岛形成机制解析的研究思路, 并对未来在生殖隔离机制上的深入探索以及实证研究的整合分析等方面进行了展望。

关键词: 成种, 基因流, F_ST, 基因组分化景观, 种群基因组

Abstract

Background & Aims Understanding the mechanisms underlying the formation of species is a major task of ecological and evolutionary studies. Aided by the rapid development of sequencing technologies during the last two decades, a growing body of research has revealed a heterogeneous genomic landscape of divergence with the existence of genomic islands of divergence between closely related taxa. This pattern was interpreted as evidence for the speciation-with-gene-flow model, and genomic islands in divergence landscape were hypothesized to be caused by divergent selection in the face of gene flow. However, genomic islands can also arise from other evolutionary processes, such as introgression, divergent sorting of ancient polymorphisms, and linked selection. Previous empirical studies often focused on part of evolutionary processes when discerning the mechanism governing the formation of genomic islands. Therefore, this paper aims to clarify genomic island of divergence and related concepts, summarize the pros and cons of different methods of identifying genomic islands, compare the predicted properties of genomic islands of divergence under different evolutionary processes, and propose a research route for discerning the mechanism contributing to genomic islands during speciation. This paper may provide a guide for future studies on genomic islands and their underlying mechanisms.

Progress In recent years, various empirical and model-based approaches have been proposed to identify genomic islands. After comparing the pros and cons of these approaches, we think the significance test on observed F_ST using the null distribution of F_ST under different recombination rate according to the inferred best-fitting demographic model is the most reasonable. Based on similarities and differences of the predicted properties of genomic islands of divergence under different evolutionary processes, we point out the necessity of exploiting multiple indicators, such as introgression level, absolute divergence (d_XY), relative node depth (RND), and recombination rate, when discerning the mechanism contributing to genomic islands during speciation.

Prospects We suggest more attention should be paid to the ecological and genetic basis of reproductive isolation after discerning the mechanism underlying the formation of genomic islands. Meanwhile, future researches should be standardized to facilitate integrative analysis in a comparative framework, thus improving our understandings of the frequency of speciation with gene flow in the natural world.

Key words: speciation, gene flow, F_ST, genomic landscape of divergence, population genome

孙琼, 王嵘, 陈小勇 (2022) 物种形成过程中的分化基因组岛及其形成机制. 生物多样性, 30, 21383. DOI: 10.17520/biods.2021383.

Qiong Sun, Rong Wang, Xiaoyong Chen (2022) Genomic island of divergence during speciation and its underlying mechanisms. Biodiversity Science, 30, 21383. DOI: 10.17520/biods.2021383.

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链接本文: https://www.biodiversity-science.net/CN/10.17520/biods.2021383

https://www.biodiversity-science.net/CN/Y2022/V30/I3/21383

图/表 5

图1 基因流存在下的成种与分化基因组岛。(A)基因流存在下的成种过程初期在基因水平的图示。刚开始分化的两个种群染色体上仅少量位点(此处仅展示1个)受歧化选择, 其等位基因在种群间的交换受限。双向箭头粗细表示有效基因流强弱。(B)中性位点与受歧化选择位点的遗传连锁及中性位点的有效基因流在染色体上的变化。(C)异质性基因组分化景观与分化基因组岛。“海平面”将“分化基因组岛”和“海床”分开来。改自Wu (2001)、Nosil和Feder (2012)和Aeschbacher等(2017)。

Fig. 1 Speciation with gene flow and genomic island of divergence. (A) Conceptual diagram showing the early stage of the process of speciation with gene flow from the genic view. When Pop.1 and Pop.2 start to diverge, only a few loci on the chromosome (here only one is shown) are under divergent selection, and the exchange of the alleles at these loci between populations is restricted. The thickness of the double-headed arrows represents the strength of effective gene flow. (B) Variation of the genetic linkage between neutral loci and divergently selected locus and the effective gene flow at neutral sites along the chromosome. (C) Heterogeneous landscape of genomic divergence and genomic island of divergence. Sea level separates the genomic island of divergence and the sea floor. Adapted from Wu (2001), Nosil & Feder (2012), and Aeschbacher et al (2017).

表1 不同分化基因组岛鉴定方法的比较

Table 1 Comparison of different methods for identifying genomic island of divergence

方法 Methods	优点 Pros	缺点 Cons	示例文献 Example references
基于经验的方法 Empirical approach
固定/近固定差异的局部聚集程度 Extent of regional clustering of fixed/nearly fixed differences	非常简单便捷 Very simple and convenient	未充分考虑种群统计的影响; 仅使用固定/近固定差异的分子标记进行分析, 忽略了基因组中大量的其他变异信息 The effect of population demography is not fully considered; Only fixed or nearly fixed differences are used in the analysis, with numerous differences in the genome ignored	Turner et al, 2005; Harr, 2006
F_ST百分位数 Percentile of F_ST	非常简单便捷 Very simple and convenient	未充分考虑种群统计的影响 The effect of population demography is not fully considered	Renaut et al, 2013; Poelstra et al, 2014; Ma et al, 2018; Battey, 2020
Z标准化后的F_ST (ZF_ST)大小 Value of Z-transformed F_ST (ZF_ST)	非常简单便捷 Very simple and convenient	未充分考虑种群统计的影响 The effect of population demography is not fully considered	Han et al, 2017; Wang et al, 2019; Choi et al, 2020; Behrens et al, 2021
根据实际数据重抽样构造F_ST零分布检验观测F_ST的显著性 Significance test on observed F_ST using the null distribution of F_ST built by resampling real data	简单便捷 Simple and convenient	未充分考虑种群统计的影响 The effect of population demography is not fully considered	Michel et al, 2005; Nadeau et al, 2012; Berg et al, 2015; Feulner et al, 2015; Larson et al, 2017; Mořkovský et al, 2018; Ackiss et al, 2020
基于模型的方法 Model-based approach
隐马尔科夫模型 Hidden Markov model (HMM)	简单便捷; 无需设置滑窗大小, 考虑了相邻分子标记之间的非独立性 Simple and convenient; No need to set the sliding window size, and the non-independence among neighboring markers is modeled	未充分考虑种群统计的影响; 每种隐含状态对应观测值的分布、高/低分化水平两种隐含状态互相的转移概率是否为0等方面的假设对鉴定结果有一定影响 The effect of population demography is not fully considered; The identification result is affected by the assumptions such as the distribution of observations corresponding to each hidden state and whether the transition probability between the two hidden states of high/low divergence is 0	Turner et al, 2005; Hofer et al, 2012; Soria-Carrasco et al, 2014; Marques et al, 2016; Morales et al, 2018
BayeScan	简单便捷 Simple and convenient	当研究对象中有经历过严重瓶颈效应的种群时, 鉴定结果存在较高的假阳性率 High false positive rate when studied population underwent a strong bottleneck	Michel et al, 2010; Andrew & Rieseberg, 2013; Larson et al, 2019; McCulloch et al, 2021
根据假定的种群动态场景构建不同杂合度下F_ST的零分布检验观测F_ST的显著性 Significance test on observed F_ST using the null distribution of F_ST under different heterozygosity according to the assumed population demographic scenario	简单便捷; 相关软件内置了不同种群动态场景 Simple and convenient; Different population demographic models are built in related softwares	假定的种群动态场景可能与现实场景相差甚远, 导致假阳性率较高 The assumed population demographic model may be very different from the real scenario, resulting in a high false positive rate	Michel et al, 2010; Tsumura et al, 2012; Bradbury et al, 2013; Hudson et al, 2013
根据推断的最优种群统计模型构建F_ST的零分布检验观测F_ST的显著性 Significance test on observed F_ST using the null distribution of F_ST according to the inferred best-fitting demographic model	构造F_ST零分布时使用的种群统计模型更符合现实场景 The demographic model used to build the null distribution of F_ST is more realistic	步骤有些繁琐; 未考虑重组率对F_ST分布的影响 Somewhat complex; The effect of recombination rate on the distribution of F_ST is ignored	Malinsky et al, 2015; Wang et al, 2016
根据推断的最优种群统计模型构建不同重组率下F_ST的零分布检验观测F_ST的显著性 Significance test on observed F_ST using the null distribution of F_ST under different recombination rate according to the inferred best-fitting demographic model	构造F_ST零分布时使用的种群统计模型更符合现实场景; 考虑了重组率对F_ST分布的影响 The demographic model used to build the null distribution of F_ST is more realistic, and the effect of recombination rate on distribution of F_ST is considered	步骤繁琐 Complicated	目前尚无示例文献 No example reference is available yet

表1 不同分化基因组岛鉴定方法的比较

Table 1 Comparison of different methods for identifying genomic island of divergence

方法 Methods	优点 Pros	缺点 Cons	示例文献 Example references
基于经验的方法 Empirical approach
固定/近固定差异的局部聚集程度 Extent of regional clustering of fixed/nearly fixed differences	非常简单便捷 Very simple and convenient	未充分考虑种群统计的影响; 仅使用固定/近固定差异的分子标记进行分析, 忽略了基因组中大量的其他变异信息 The effect of population demography is not fully considered; Only fixed or nearly fixed differences are used in the analysis, with numerous differences in the genome ignored	Turner et al, 2005; Harr, 2006
F_ST百分位数 Percentile of F_ST	非常简单便捷 Very simple and convenient	未充分考虑种群统计的影响 The effect of population demography is not fully considered	Renaut et al, 2013; Poelstra et al, 2014; Ma et al, 2018; Battey, 2020
Z标准化后的F_ST (ZF_ST)大小 Value of Z-transformed F_ST (ZF_ST)	非常简单便捷 Very simple and convenient	未充分考虑种群统计的影响 The effect of population demography is not fully considered	Han et al, 2017; Wang et al, 2019; Choi et al, 2020; Behrens et al, 2021
根据实际数据重抽样构造F_ST零分布检验观测F_ST的显著性 Significance test on observed F_ST using the null distribution of F_ST built by resampling real data	简单便捷 Simple and convenient	未充分考虑种群统计的影响 The effect of population demography is not fully considered	Michel et al, 2005; Nadeau et al, 2012; Berg et al, 2015; Feulner et al, 2015; Larson et al, 2017; Mořkovský et al, 2018; Ackiss et al, 2020
基于模型的方法 Model-based approach
隐马尔科夫模型 Hidden Markov model (HMM)	简单便捷; 无需设置滑窗大小, 考虑了相邻分子标记之间的非独立性 Simple and convenient; No need to set the sliding window size, and the non-independence among neighboring markers is modeled	未充分考虑种群统计的影响; 每种隐含状态对应观测值的分布、高/低分化水平两种隐含状态互相的转移概率是否为0等方面的假设对鉴定结果有一定影响 The effect of population demography is not fully considered; The identification result is affected by the assumptions such as the distribution of observations corresponding to each hidden state and whether the transition probability between the two hidden states of high/low divergence is 0	Turner et al, 2005; Hofer et al, 2012; Soria-Carrasco et al, 2014; Marques et al, 2016; Morales et al, 2018
BayeScan	简单便捷 Simple and convenient	当研究对象中有经历过严重瓶颈效应的种群时, 鉴定结果存在较高的假阳性率 High false positive rate when studied population underwent a strong bottleneck	Michel et al, 2010; Andrew & Rieseberg, 2013; Larson et al, 2019; McCulloch et al, 2021
根据假定的种群动态场景构建不同杂合度下F_ST的零分布检验观测F_ST的显著性 Significance test on observed F_ST using the null distribution of F_ST under different heterozygosity according to the assumed population demographic scenario	简单便捷; 相关软件内置了不同种群动态场景 Simple and convenient; Different population demographic models are built in related softwares	假定的种群动态场景可能与现实场景相差甚远, 导致假阳性率较高 The assumed population demographic model may be very different from the real scenario, resulting in a high false positive rate	Michel et al, 2010; Tsumura et al, 2012; Bradbury et al, 2013; Hudson et al, 2013
根据推断的最优种群统计模型构建F_ST的零分布检验观测F_ST的显著性 Significance test on observed F_ST using the null distribution of F_ST according to the inferred best-fitting demographic model	构造F_ST零分布时使用的种群统计模型更符合现实场景 The demographic model used to build the null distribution of F_ST is more realistic	步骤有些繁琐; 未考虑重组率对F_ST分布的影响 Somewhat complex; The effect of recombination rate on the distribution of F_ST is ignored	Malinsky et al, 2015; Wang et al, 2016
根据推断的最优种群统计模型构建不同重组率下F_ST的零分布检验观测F_ST的显著性 Significance test on observed F_ST using the null distribution of F_ST under different recombination rate according to the inferred best-fitting demographic model	构造F_ST零分布时使用的种群统计模型更符合现实场景; 考虑了重组率对F_ST分布的影响 The demographic model used to build the null distribution of F_ST is more realistic, and the effect of recombination rate on distribution of F_ST is considered	步骤繁琐 Complicated	目前尚无示例文献 No example reference is available yet

图2 种群内核苷酸多样性(πw)、种群间核苷酸序列分化/绝对分化指标(πb或dXY)、固定指数(FST)和相对节点深度(RND)图示。X、Y为两个正在分化的种群/物种, O为外类群。物种树(黑色)内是示例基因的基因树(灰色)。此处物种树和基因树的大小均与示例基因突变率μ成正比, μ1 > μ2。T1、T3为X与Y、O与XY祖先的种群分化时间/成种时间, T2、T4为X与Y、O与XY祖先的示例基因分化时间。πwX、πwY、dXY (即πb)为X种群内、Y种群内、X与Y种群间两两配对序列的平均核苷酸差异。FST可表示为1-πw/πb或类似形式。RND校正了μ对序列分化的影响。dout是O与X、Y的dOX和dOY的均值。基因1和基因2的dXY相等, 但基因2的πw更小, 因此其FST更高(A和B)。基因2和基因3的FST、T2、T4和RND均相等, 但μ不同, 基因3的dXY更小(B和C)。改自Cruickshank和Hahn (2014)和Rosenzweig等(2016)。

Fig. 2 Illustration of within-population nucleotide diversity (πw), between-population sequence divergence/absolute divergence (πb or dXY), fixation index (FST) and relative node depth (RND). X and Y are two diverging populations or species. The gene tree (grey) of an example gene is contained within the species tree (black). The sizes of species tree and gene tree displayed are both directly proportional to the mutation rate (μ) of the example gene, μ1> μ2. T1 and T3 are the divergence time or speciation time between X and Y, and between O and the ancestor of X and Y, respectively. T2 and T4 are the divergence time of example gene between X and Y, and between O and the ancestor of X and Y, respectively. πwX, πwY, and absolute divergence (dXY) represent the average number of nucleotide differences of pairwise sequences within X, within Y, and between X and Y, respectively. FST is calculated as 1-πw/πb or similar formulas. RND is an estimate of sequence divergence with the effect of μ corrected. dout is the average of absolute divergence between O and X and between O and Y. dXY of gene 1 is the same as that of gene 2, but FST of gene 2 is higher due to lower πw (A and B). There are no differences in FST, T2, T4, and RND between gene 2 and gene 3, but dXY of gene 3 is lower due to lower μ (B and C). Adapted from Cruickshank & Hahn (2014) and Rosenzweig et al (2016).

图3 可导致分化基因组岛形成的不同进化过程示意图。X、Y为两个正在分化的种群/物种。第二种机制中(B), 近缘物种Z向X有基因渐渗, 其他机制中Z向X或Y均无基因渐渗(A、C、D、E)。每个物种树内包含两个示例基因的基因树, 彩色基因树表示示例基因是经历了对应进化过程的位点或紧密连锁位点, 灰色基因树表示弱连锁或不连锁的中性位点。物种树下的图表示每种机制两类位点FST、dXY (假设基因组中μ无异质性)和RND (无需对μ的异质性做出假设)的差异。改自Cruickshank和Hahn (2014)和Han等(2017)。

Fig. 3 Schematic diagram illustrating different evolutionary processes that could lead to the formation of genomic island of divergence. X and Y are two diverging populations or species. Z is a related species, from which some genetic materials are introgressed into X in scenario (B) in contrast to the other four scenarios (A, C, D, E). The gene trees of two example genes are contained within the species tree (black). The colored gene tree represents the locus underlying the corresponding evolutionary process or its tightly linked loci, and the grey gene tree represents the loosely linked or unlinked loci. The graphs below species trees show the difference of FST, dXY (on the assumption of no variation of μ), and RND (without the assumption of no variation of μ) between two kinds of loci under various evolutionary processes. Adapted from Cruickshank & Hahn (2014) and Han et al (2017).

图4 分化基因组岛形成机制解析逻辑流程图。FSTsym和FSTallo分别表示姊妹种同域种群对、异域种群对的FST。此图仅展示了关键证据(辅助性证据见正文)。

Fig. 4 Flow chart illustrating the logic of discerning the mechanism contributing to genomic islands of divergence. FSTsym and FSTallo are abbreviations for FST of sympatric and allopatric populations of focal sister species, respectively. Here, only the key pieces of evidence are listed (see text for complementary evidence).

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