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Uncovering endemism in a lake of invasive species introgression
Molecular Ecology ( IF 4.5 ) Pub Date : 2021-01-15 , DOI: 10.1111/mec.15801
Iva Popovic 1 , Louis Bernatchez 2
Affiliation  

Species distributions are rapidly being altered by human globalisation and movement. As species are moved across biogeographic boundaries, human‐mediated secondary contacts between historically allopatric taxa may promote hybridisation between closely related native and introduced species. The outcomes of hybridisation are diverse from strong reproductive barriers to gene flow to genome‐wide admixture that may enhance (Fitzpatrick et al., 2010; Mesgaran et al., 2016; Valencia‐Montoya et al., 2020) or impede (Kovach et al., 2016) invasive spread. For native species, introgressive hybridisation may disassemble locally adapted genomes, and in extreme cases, extensive asymmetric introgression may lead to the “genomic extinction” of endemic diversity (Rhymer & Simberloff, 1996; Todesco et al., 2016). Undoubtedly, introgressive hybridisation can rapidly alter the evolution of introduced and endemic populations and is a major conservation issue (Leitwein et al., 2020), with the greatest potential consequences on small, range‐restricted native populations where introduced species may reach higher relative densities (Currat et al., 2008). In this issue of Molecular Ecology, Blackwell et al. (2020) explore the history of divergence and admixture between the highly invasive Nile tilapia, Oreochromis niloticus, and a recently discovered Oreochromis lineage that is endemic to the coastal lakes of southern Tanzania. Oreochromis tilapias belong to the African cichlids and the most diverse family of vertebrates (Cichlidae), with almost 2000 species inhabiting the Great Lakes and river environments of Eastern Africa (Kocher, 2004; McGee et al., 2020). By analysing previously unrecognised cichlid diversity from southern lakes, Blackwell et al. (2020) provide novel evidence for how introgressive hybridisation with introduced species can alter native genetic makeup, illustrating the potential susceptibility of Tanzania's endemic biodiversity to genetic threats from introduced taxa.

Combining microsatellite genotyping and whole genome resequencing with morphological analyses, Blackwell et al. (2020) show that southern populations of Oreochromis korogwe within lakes Rutamba, Nambawala and Mitupa are genetically distinct from allopatric O. korogwe populations in northern Tanzania, as well as other Oreochromis congeners studied within the region. Furthermore, substantial divergence in morphological traits (e.g., body depth, fin dimensions and eye size) between genetically pure‐bred southern and northern O. korogwe populations implies possible ecological divergence and local adaptation to southern regions. Altogether, these results make a strong case to recognise newly discovered southern O. korogwe populations as a distinct evolutionarily significant unit that should be managed independently from northern ones.

Unfortunately, however, Blackwell et al. (2020) provide evidence that recent introductions of invasive Nile tilapia, O. niloticus, into isolated southern watersheds have resulted in repeated hybridisation with endemic O. korogwe populations at various degrees among sampled lakes. O. niloticus is a globally cultivated aquaculture species and is of prime importance for food security in Africa. Although native to Tanzania within the Lake Tanganyika catchment, deliberate translocations for inland aquaculture and accidental escapes have promoted O. niloticus establishment outside of its natural distribution (Shechonge et al., 2018). Today, the Nile tilapia has been introduced throughout Africa with potential negative effects on receiving communities, including habitat alternation and competitive displacement of native taxa (Canonico et al., 2005). O. niloticus also hybridises with multiple Oreochromis species where congeners are sympatric (Deines et al., 2014; Shechonge et al., 2018). Blackwell et al. (2020) infer that 6–29% of individuals sampled in southern lakes comprise hybrids, with levels of individual admixture from O. niloticus varying between 12 and 85% (genomic mean). These results suggest the presence of early‐generation hybrids or backcrossed individuals probably resulting from recent admixture. Moreover, whole genome sequencing on a subset of 12 individuals revealed that the impact of O. niloticus introgression is variable across the genome, whereby morphologically “pure” southern O. korogwe genomes are a mosaic of ancestry originating from introduced O. nilocitus, further confirming that hybrids are fertile and reproductively viable.

The growing availability of genomic data for invasive species and closely related lineages (Bay et al., 2019; Valencia‐Montoya et al., 2020) suggests that the consequences of introgressive hybridisation are highly variable across the genome and thus difficult to predict (Abbott et al., 2013). For closely related native and introduced taxa, such as Oreochromis congeners, understanding hybridisation outcomes is further complicated by recent divergence histories and genome‐wide ancestral polymorphisms that may obscure signatures of contemporary introgression (Popovic et al., 2020). Applying a phylogenomic approach, Blackwell et al. (2020) partly disentangle these processes. They quantified admixture history between Oreochromis species using a tree weighting approach that counts alternative species topologies estimated from consecutive genomic intervals, where discordant phylogenies can result from ongoing lineage sorting or introgressive hybridisation (Martin & Van Belleghem, 2017). While the consensus species topology grouping northern and southern O. korogwe as sister taxa was the dominant genomic relationship, discordant topologies showed multiple frequency peaks and localised clustering, especially within three linkage groups (Figure 1). Although gene tree discordance can occur through incomplete lineage sorting, a substantial excess in the topology grouping invasive O. niloticus together with native southern O. korogwe suggests their recent admixture. In contrast, similar patterns were not apparent when O. korogwe from a northern waterbody, where O. niloticus is not introduced, were compared with O. niloticus. Thus, by leveraging knowledge of species distributions and utilising multispecies comparisons, Blackwell et al. (2020) show that O. niloticus introgression is heterogeneous across the southern O. korogwe genome and that admixture probably occurred after their split from northern O. korogwe (Figure 1). Another intriguing outcome of the genome scans was that southern O. korogwe shared similar regions of low differentiation with a parapatric congener, Oreochromis urolepis, highlighting the possibility of historical hybridisation and the complex nature of endemic demographic histories within the southern lakes.

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FIGURE 1
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Females of Oreochromis species sampled in Tanzania and genome‐wide species relationships inferred with TWISST. (a) Northern lineage Oreochromis korogwe from the Pangani region; (b) southern lineage O. korogwe sampled from lakes Rutamba, Nambawala and Mitupa; (c) parapatric congener O. urolepis; and (d) invasive Nile tilapia, O. niloticus. (e) Phylogenomic species relationships across 23 linkage groups, where colours corresponding to relative weightings for three alternative species topologies; modified figure 5g from Blackwell et al. (2020). Genomic regions (e.g., LG7, LG8, LG17) showing high relative weightings for the green discordant topology grouping native southern O. korogwe with invasive O. niloticus (ACBD) are consistent with O. niloticus introgression into the southern O. korogwe native genetic background. The consensus species phylogeny (ABCD) and the alternative discordant topology (ADBC) for the four taxa are shown in yellow and purple

It is now accepted that hybridisation is a prominent feature of the evolutionary process, with many species experiencing periodic contact and gene flow throughout their evolutionary histories (Roux et al., 2016). Indeed, and somewhat in sharp contrast with the reported negative effects of contemporary hybridisation during species invasions, it is clear that historical introgressive hybridisation and admixture have played a crucial role in the explosive adaptive radiations that characterise the evolution of cichlid diversity in Africa (Kagawa & Seehausen, 2020; McGee et al., 2020; Meier et al., 2017). Such complex speciation histories are already difficult to resolve and recent admixture between introduced and native taxa may exacerbate the problem. Blackwell et al. (2020) overcome this challenge by focusing on the least admixed regions of the southern O. korogwe genome to characterise their divergence from northern populations. The authors estimate that northern and southern O. korogwe lineages have been diverging for ~140,000 years as isolated populations, suggesting that their present day disjunct distributions (~500 km apart) probably resulted from natural long‐distance colonisations or historical range contractions. Importantly, the genetic and morphological distinctiveness of southern O. korogwe from northern populations supports the recognition of this lineage as an evolutionarily significant unit of conservation. With clear signatures of genome‐wide introgression and no apparent signs of hybridisation at the morphological level for sequenced southern individuals, Blackwell et al. (2020) present an example of how invasive introgression can quickly alter native genetic backgrounds, with potential impacts on their local adaptation.

Invasive species hybridisation with native taxa has long been recognised as a major conservation issue (Rhymer & Simberloff, 1996). Yet, genome‐enabled studies of aquatic invasive species and especially anthropogenic hybrid zones are still rare relative to the scope of the problem. While a number of cichlid genomes have recently been sequenced (McGee et al., 2020; Ronco et al., 2020), O. niloticus is among the few invasive species for which a linkage‐informed genome assembly has been developed (Conte et al., 2019; Tao et al., 2021). Enabled by high‐quality genomic resources, the study by Blackwell et al. (2020) provides clear evidence for the evolutionary distinctiveness between southern and northern O. korogwe populations, as well as the occurrence of recent introgressive hybridisation from invasive O. niloticus. The use of 13 microsatellites, however, does not offer genome‐wide resolution needed to rigorously evaluate the proportion of various hybrid classes among admixed individuals. Additionally, few resequenced individuals (n = 3 per group) and low genomic coverage (5×) limits the accuracy of differentiation estimates. More comprehensive genomic investigations would provide deeper understanding of both the evolutionary history of O. korogwe as well as the dynamics of hybridisation. Modelling approaches that allow inferences of historical demography would improve estimates of divergence times and the role of possible past hybridisation events in shaping O. korogwe diversity (Fraïsse et al., 2021; Rougemont et al., 2020). Similarly, new methods that take advantage of haplotype information could be used to examine recent histories of gene flow, selection, and the evolutionary outcomes of hybridisation (either positive or negative) at local genomic scales that may inform the timing of anthropogenic admixture that is relevant for addressing conservation issues (Leitwein et al., 2020).

As new genomic studies of introduced species elucidate the frequency and consequences of anthropogenic hybridisation (Blackwell et al., 2020), they also raise ethical and practical considerations for endemic species conservation. The management of hybridising taxa is a contentious topic (Allendorf et al., 2001; Hamilton & Miller, 2016; Jackiw et al., 2015), with some authors advocating for a gene‐level framework for managing introgressed populations and tracking the dispersal of invasive genes through novel habitats (Crispo et al., 2011; Petit, 2004). Indeed, incorporating genomic tools into invasive species management will be essential for quantifying the risks of introgressive swamping in small and isolated endemic populations. For the case of tilapia species, restocking of O. niloticus and other commercially significant taxa for aquaculture could facilitate introductions into new waterways, and the widespread genetic impact of O. niloticus introductions is evident in the finding of a O. placidus × O. nilticus hybrid in the relatively poorly studied Ruvuma catchment (Blackwell et al., 2020). With the possibility that northern O. korogwe populations are also genetically distinct from each other, the evolution of more unrecognised diversity in Tanzanian watersheds could be influenced by hybridisation with introduced lineages. While understanding admixture timing and the processes modulating genomic introgression rates will require more in‐depth analyses of hybrid genomes, the study by Blackwell et al. (2020) illustrates how genomic data from few sampled individuals can uncover endemic lineages at risk of losing diversity and provides a first glimpse of how anthropogenic hybridisation has shaped their evolution.



中文翻译:

在入侵物种渗入的湖泊中发现地方病

人类的全球化和运动正在迅速改变物种的分布。随着物种跨过生物地理边界的迁移,历史上的异源分类单元之间的人类介导的次要接触可能会促进密切相关的本地物种与引进物种之间的杂交。杂交的结果从强大的生殖障碍到基因流动再到可能增强的全基因组混合(Fitzpatrick等人,2010 ; Mesgaran等人,2016 ; Valencia-Montoya等人,2020)或受阻(Kovach等人,等,2016年)侵入性传播。对于原生物种,渗入杂交可能会分解局部适应的基因组,在极端情况下,广泛的不对称渗入可能导致地方性多样性的“基因组灭绝”(Rhymer&Simberloff,1996; Todesco等,2016)。毫无疑问,渗入杂交可以迅速改变引进种群和特有种群的进化,这是一个主要的保护问题(Leitwein等,2020),对范围有限的小型本地种群的潜在影响最大,在这些种群中,引入的物种可能会达到较高的相对密度。 (Currat等,2008)。在本期《分子生态学》中,Blackwell等人。(2020年)探索高度入侵的尼罗罗非鱼(Oreochromis niloticus)和最近发现的坦桑尼亚南部沿海湖泊特有的Oreochromis血统之间的分歧和混合历史。罗非鱼(Oreochromis tilapias)属于非洲丽鱼科动物和最多样化的脊椎动物家族(丽鱼科),有近2000种生活在东非的大湖和河流环境中(Kocher,2004 ; McGee et al。,2020)。通过分析南部湖泊以前无法识别的丽鱼科鱼多样性,Blackwell等人。(2020年)提供了新证据,证明与外来物种的渐渗杂交会如何改变原生遗传构成,从而说明坦桑尼亚特有生物多样性对外来物种的遗传威胁的潜在敏感性。

Blackwell等人将微卫星基因分型和整个基因组重测序与形态分析相结合。(2020)表明,在鲁坦巴湖,南巴瓦拉湖和米图帕湖中南部的Oreochromis korogwe种群与坦桑尼亚北部的异型O. korogwe种群以及该地区研究的其他Oreochromis同系物在遗传上是不同的。此外,在基因纯种的南部和北部O之间,形态特征(例如,体深,鳍大小和眼大小)存在很大差异。 Korogwe人口意味着可能的生态差异和对南部地区的局部适应。总之,这些结果为识别新近发现的南部O提供了有力的依据。 korogwe种群是一个明显的重要进化单元,应独立于北部种群进行管理。

然而不幸的是,Blackwell等人。(2020)提供了证据,入侵性尼罗河罗非鱼,O 尼罗罗非鱼(Niloticus)进入孤立的南部流域,导致与地方性O的反复杂交。采样湖中不同程度的 科罗格威种群。Ø 尼罗罗非鱼是全球养殖的水产养殖品种,对于非洲的粮食安全至关重要。尽管坦Tang尼喀湖流域内的坦桑尼亚原产于内陆,但因内陆水产养殖和意外逃生而进行的有意易位促使其在自然分布范围之外建立了罗非鱼(Shechonge等,2018)。如今,尼罗罗非鱼已被引入整个非洲,对接收社区有潜在的负面影响,包括生境的改变和原生类群的竞争性迁移(Canonico等,2005)。Ø 尼罗罗非鱼还与同种同源的多种Oreochromis物种杂交(Deines等,2014 ; Shechonge等,2018)。Blackwell等。(2020)推断出在南部湖泊样本个体的6-29%包括杂种,与来自个体的混合水平Ó 罗非鱼在12%至85%(基因组平均值)之间变化。这些结果表明,早期杂交种或回交个体的存在可能是由于最近的掺混所致。此外,对12个个体的一个子集进行全基因组测序揭示了O的影响。 罗非鱼基因渗入是整个基因组,由此在形态学“纯”南部可变Ò korogwe基因组是起源于O的祖先的马赛克。 nilocitus,进一步证实了杂种育和生殖可行的。

入侵物种和密切相关世系的基因组数据的可用性不断提高(Bay等,2019 ; Valencia-Montoya等,2020)表明,渐渗杂交的后果在整个基因组中差异很大,因此很难预测(Abbott等人,2013)。对于紧密相关的本地和引进的类群,例如Oreochromis同源物,由于最近的分歧历史和全基因组祖先多态性可能会使当代渗入的特征模糊不清,因此对杂交结果的理解变得更加复杂(Popovic et al。,2020)。应用系统生物学方法,Blackwell等。(2020年)部分解开这些过程。他们使用树加权方法对Oreochromis物种之间的混合历史进行了量化,该加权方法计算了从连续基因组间隔估计的替代物种拓扑,其中不连续的系统发育可能来自正在进行的谱系分选或渐渗杂交(Martin&Van Belleghem,2017)。虽然共识种拓扑分组北部和南部的Ø Korogwe由于姐妹类群是主要的基因组关系,不一致的拓扑显示出多个频率峰值和局部聚类,尤其是在三个连锁群中(图1)。尽管基因树不一致可能会通过不完全的谱系排序而发生,但在拓扑入侵O的拓扑分组中却大大超出了。 罗非鱼加上本土南部Ø korogwe建议他们最近的混合物。相反,当O时,相似的模式并不明显。 科罗圭从北部的水体,其中Ò。未引入 niloticus,与O进行了比较。 罗非鱼。因此,通过利用物种分布的知识并利用多物种比较,Blackwell等人。(2020)显示,Ö 尼罗罗非鱼的渗入在整个O南部是异质的。 Korogwe基因组及其混合物可能是在它们从O北部分裂后发生的。 korogwe(图1)。基因组扫描的另一个耐人寻味的结果是,南方Ø korogwe与同胞同源动物Oreochromis urolepis共享了相似的低分化区域,强调了历史杂交的可能性以及南部湖泊中地方人口历史的复杂性。

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图1
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雌性尼罗在坦桑尼亚采样品种,并与TWISST推断全基因组的物种关系。(a)潘加尼地区的北部血统Oreochromis korogwe;(b)从Rutamba,Nambawala和Mitupa湖取样的南部血统O. korogwe;(c)亲族同源物O. urolepis;和(d)侵入尼罗罗非鱼,尼罗罗非鱼。(e)跨越23个连锁群的植物学物种关系,其中颜色对应于三种替代物种拓扑的相对权重;Blackwell等人的改良图形5g。(2020年)。基因组区域(例如,LG7,LG8,LG17)显示绿色不和谐拓扑的相对权重较高O.科罗圭有创尼罗罗非鱼(ACBD)是一致尼罗罗非鱼渗入到南部O.科罗圭原生遗传背景。黄色和紫色显示了四个类群的共有物种系统发育(ABCD)和替代不和谐拓扑(ADBC)

现在人们普遍认为杂交是进化过程的显着特征,许多物种在整个进化过程中都经历着周期性的接触和基因流动(Roux等,2016)。确实,与现代杂交报道的物种入侵期间的负面影响形成鲜明对比的是,很明显,历史渐渗性杂交和混合在表征非洲丽鱼科鱼多样性演变的爆炸性适应性辐射中起着至关重要的作用(Kagawa& Seehausen,2020 ; McGee等,2020 ; Meier等,2017)。如此复杂的物种形成历史已经很难解决,而且引入的和本地的分类单元之间最近的混合可能加剧了这一问题。Blackwell等。(2020)克服集中在南部的至少混合区这一挑战Ø korogwe基因组来表征其与北方种群的差异。笔者估计,北部和南部Ø。作为孤立的种群, korogwe血统已经分化了约14万年,这表明它们今天的分离分布(相距约500公里)可能是自然的长距离定居或历史范围的缩小造成的。重要的是,南方的遗传和形态独特性北部种群的O. korogwe支持将这一血统视为保护的进化上重要的单位。Blackwell等人具有明显的全基因组渗入特征,并且在形态学水平上没有明显的杂交迹象。(2020)提出了侵入性渗入如何快速改变天然遗传背景,并对其本地适应性产生潜在影响的一个例子。

长期以来,将入侵物种与本地分类单元杂交是一个主要的保护问题(Rhymer&Simberloff,1996)。然而,相对于问题的范围,对水生入侵物种尤其是人为杂交区的基因组研究仍然很少。虽然一些鲷基因组最近已被测序(McGee等人,。2020 ;龙科等人,2020),Ö 尼罗罗非鱼是为之开发了连锁信息基因组组装的少数入侵物种之一(Conte等人,2019 ; Tao等人,2021)。Blackwell等人的研究得到了高质量基因组资源的支持。(2020年)为南方和北方之间的进化显着性明确的证据Ø korogwe种群,以及入侵性O的最近渐渗杂交的发生。 尼罗罗非鱼。但是,使用13个微卫星无法提供全基因组分辨率,而该分辨率不能严格评估混合个体中各种杂种类别的比例。此外,很少重新排序的个体( 每组n = 3)和低基因组覆盖率(5倍)限制了分化估计的准确性。更全面的基因组研究将提供对O的进化史的更深入了解。 Korogwe以及杂交的动力。可以推论历史人口统计学的建模方法将改善发散时间的估计以及过去可能发生的杂交事件在塑造O中的作用 korogwe多样性(Fraïsse等,2021; Rougemont等,2020)。同样,可以利用利用单倍型信息的新方法来检查最近的基因流历史,选择以及在本地基因组规模上杂交的进化结果(阳性或阴性),这些信息可能会提示相关的人为混合时间解决保护问题(Leitwein等,2020)。

随着对引入物种的新基因组研究阐明了人为杂交的频率和后果(Blackwell等人,2020年),它们也引起了地方性物种保护的伦理和实践考虑。杂交类群的管理是一个有争议的话题(Allendorf等,2001; Hamilton&Miller,2016; Jackiw等,2015),一些作者提倡建立基因水平的框架来管理渗入种群并追踪其分布。通过新的生境入侵基因(Crispo等人,2011; Petit,2004)。确实,将基因组学工具纳入入侵物种管理对于量化小而孤立的地方性种群渗入性沼泽的风险至关重要。对于罗非鱼品种的情况下,放养的Ø 尼罗罗非鱼和其他在水产养殖上具有商业意义的分类单元可能有助于将其引入新的水道,并促进O的广泛遗传影响。在发现O的过程中很明显地引入了 niloticus 侧柏 ×  O。相对较少的Ruvuma集水区中的 Nilticus杂种(Blackwell等,2020)。随着北的可能性 Korogwe种群在遗传上也彼此不同,坦桑尼亚流域更多未被认识到的多样性的演变可能会受到与引进血统的杂交的影响。Blackwell等人的研究虽然了解混合物的时机和调节基因组渗入速率的过程将需要对杂交基因组进行更深入的分析。(2020年)说明了来自少数被采样个体的基因组数据如何发现存在丧失多样性风险的地方谱系,并提供了人为杂交如何影响其进化的第一印象。

更新日期:2021-02-15
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