Does rafting promote contemporary gene flow? Global and regional patterns of population genetic diversity and structure on the false limpet Siphonaria lateralis in the Southern Ocean

IF 2.4 3区 环境科学与生态学 Q2 ECOLOGY Frontiers in Ecology and Evolution Pub Date : 2024-09-09 DOI:10.3389/fevo.2024.1441397
Constanza Millán-Medina, Marcelo Lizama, Thomas Saucède, Elie Poulin, Nicolás I. Segovia, Claudio González-Wevar
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Abstract

Rafting has been proposed as an effective mechanism for species without free-living pelagic larvae to achieve long-distance dispersal, theoretically preventing population differentiation over wide distributional ranges. Moreover, rafting has been advocated as a main dispersal mechanism for marine invertebrates with sub-Antarctic distributions, because of abundant buoyant kelps, driven by the Antarctic Circumpolar Current. Nonetheless, little attention has been given to the role of rafting to establish regular gene flow across the sub-Antarctic, and the geographic and temporal scales at which it occurs. Aiming to unravel these major questions about the extent of genetic connectivity across the Southern Ocean (SO), we studied the pulmonate limpet Siphonaria lateralis, a benthic species with encapsulated larvae, found on the rocky intertidal of sub-Antarctic islands and southern South America. Since S. lateralis is closely associated with D. antarctica, dispersal by rafting is plausible, as revealed by the absence of phylogeographic structure across the sub-Antarctic. We sampled 116 individuals from eight localities across the SO, and used 5,515 SNPs obtained through Genotyping-by-Sequencing, to determine contemporary genetic diversity, structure, and gene flow at two spatial scales; global, across the SO, and regional, within Kerguelen. Results identified substantial genetic structure, differentiating Patagonia, Falklands/Malvinas Islands, South Georgia and the Kerguelen archipelago, and low levels of contemporary gene flow. The most notable genetic differentiation was found between Patagonia/Falklands and South Georgia/Kerguelen. Structure was also significant between Patagonia and the Falkland/Malvinas Islands. Conversely, South Georgia and Kerguelen exhibited closer genetic affinity, and indications of recent but limited gene flow. Moreover, historical gene flow estimates between the four populations were low. At regional scale, noteworthy genetic structure persisted, and gene flow was insufficient to prevent genetic differentiation within Kerguelen. Consequently, rafting’s potential may be overestimated as a contemporary mechanism promoting gene flow across the SO, as these events may be sporadic, irregular, and unpredictable for marine invertebrates lacking a larval dispersal stage, since contemporary dispersal events don’t seem to facilitate high gene flow at both scales. Accordingly, other oceanographic factors or processes may hinder the establishment of species associated with macroalgae, and as consequence, contemporary genetic connectivity in the sub-Antarctic.
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漂流是否会促进当代基因流动?南大洋假瓣藻种群遗传多样性和结构的全球和区域模式
漂流被认为是没有自由生活的浮游幼虫的物种实现远距离扩散的有效机制,理论上可以防止大分布范围内的种群分化。此外,由于南极环极洋流的推动,海洋无脊椎动物具有丰富的浮力,因此漂流被认为是分布在亚南极地区的海洋无脊椎动物的主要扩散机制。然而,人们很少关注漂流在整个亚南极地区建立有规律基因流动的作用,以及漂流发生的地理和时间尺度。为了揭示这些有关南大洋遗传连接程度的重大问题,我们研究了南极洲岛屿和南美洲南部潮间带岩石上的底栖物种Siphonaria lateralis。由于S. lateralis与D. antarctica密切相关,因此通过筏式传播是可信的,这一点从整个亚南极地区缺乏系统地理结构中可以看出。我们从整个南极洲的八个地点采集了 116 个个体,并通过基因分型测序技术获得了 5,515 个 SNPs,以确定两个空间尺度上的当代遗传多样性、结构和基因流:全球尺度(整个南极洲)和区域尺度(凯尔盖朗岛内)。研究结果表明,巴塔哥尼亚、福克兰群岛/马尔维纳斯群岛、南乔治亚岛和凯尔盖朗群岛之间存在巨大的遗传结构差异,当代基因流动水平较低。最显著的遗传分化出现在巴塔哥尼亚/福克兰群岛和南乔治亚岛/凯尔盖朗群岛之间。巴塔哥尼亚和福克兰/马尔维纳斯群岛之间的结构也很明显。相反,南乔治亚岛和凯尔盖朗岛之间的遗传亲缘关系更近,有迹象表明最近有基因流动,但数量有限。此外,四个种群之间的历史基因流估计值较低。在区域范围内,值得注意的遗传结构依然存在,基因流动不足以阻止凯尔盖朗岛内的基因分化。因此,对于缺乏幼虫扩散阶段的海洋无脊椎动物来说,漂流可能是零星的、不规则的和不可预测的,因为当代的扩散事件似乎并不能促进两个尺度上的高基因流。因此,其他海洋学因素或过程可能会阻碍与大型藻类有关的物种的建立,从而阻碍亚南极地区的当代遗传连接。
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来源期刊
Frontiers in Ecology and Evolution
Frontiers in Ecology and Evolution Environmental Science-Ecology
CiteScore
4.00
自引率
6.70%
发文量
1143
审稿时长
12 weeks
期刊介绍: Frontiers in Ecology and Evolution publishes rigorously peer-reviewed research across fundamental and applied sciences, to provide ecological and evolutionary insights into our natural and anthropogenic world, and how it should best be managed. Field Chief Editor Mark A. Elgar at the University of Melbourne is supported by an outstanding Editorial Board of international researchers. This multidisciplinary open-access journal is at the forefront of disseminating and communicating scientific knowledge and impactful discoveries to researchers, academics and the public worldwide. Eminent biologist and theist Theodosius Dobzhansky’s astute observation that “Nothing in biology makes sense except in the light of evolution” has arguably even broader relevance now than when it was first penned in The American Biology Teacher in 1973. One could similarly argue that not much in evolution makes sense without recourse to ecological concepts: understanding diversity — from microbial adaptations to species assemblages — requires insights from both ecological and evolutionary disciplines. Nowadays, technological developments from other fields allow us to address unprecedented ecological and evolutionary questions of astonishing detail, impressive breadth and compelling inference. The specialty sections of Frontiers in Ecology and Evolution will publish, under a single platform, contemporary, rigorous research, reviews, opinions, and commentaries that cover the spectrum of ecological and evolutionary inquiry, both fundamental and applied. Articles are peer-reviewed according to the Frontiers review guidelines, which evaluate manuscripts on objective editorial criteria. Through this unique, Frontiers platform for open-access publishing and research networking, Frontiers in Ecology and Evolution aims to provide colleagues and the broader community with ecological and evolutionary insights into our natural and anthropogenic world, and how it might best be managed.
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