The nature and extent of diversity in the plankton has fascinated scientists for over a century. Initially, the discovery of many new species in the remarkably uniform and unstructured pelagic environment appeared to challenge the concept of ecological niches. Later, it became obvious that only a fraction of plankton diversity had been formally described, because plankton assemblages are dominated by understudied eukaryotic lineages with small size that lack clearly distinguishable morphological features. The high diversity of the plankton has been confirmed by comprehensive metabarcoding surveys, but interpretation of the underlying molecular taxonomies is hindered by insufficient integration of genetic diversity with morphological taxonomy and ecological observations. Here we use planktonic foraminifera as a study model and reveal the full extent of their genetic diversity and investigate geographical and ecological patterns in their distribution. To this end, we assembled a global data set of ~7600 ribosomal DNA sequences obtained from morphologically characterised individual foraminifera, established a robust molecular taxonomic framework for the observed diversity, and used it to query a global metabarcoding data set covering ~1700 samples with ~2.48 billion reads. This allowed us to extract and assign 1 million reads, enabling characterisation of the structure of the genetic diversity of the group across ~1100 oceanic stations worldwide. Our sampling revealed the existence of, at most, 94 distinct molecular operational taxonomic units (MOTUs) at a level of divergence indicative of biological species. The genetic diversity only doubles the number of formally described species identified by morphological features. Furthermore, we observed that the allocation of genetic diversity to morphospecies is uneven. Only 16 morphospecies disguise evolutionarily significant genetic diversity, and the proportion of morphospecies that show genetic diversity increases poleward. Finally, we observe that MOTUs have a narrower geographic distribution than morphospecies and that in some cases the MOTUs belonging to the same morphospecies (cryptic species) have different environmental preferences. Overall, our analysis reveals that even in the light of global genetic sampling, planktonic foraminifera diversity is modest and finite. However, the extent and structure of the cryptic diversity reveals that genetic diversification is decoupled from morphological diversification, hinting at different mechanisms acting at different levels of divergence.

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浮游有孔虫的全球遗传多样性揭示了浮游生物隐秘物种形成的结构

一个多世纪以来，浮游生物多样性的性质和程度一直让科学家们着迷。最初，在非常均匀和非结构化的远洋环境中发现许多新物种似乎对生态位的概念提出了挑战。后来，很明显，只有一小部分浮游生物多样性被正式描述，因为浮游生物组合主要由未经充分研究的小尺寸真核细胞谱系主导，缺乏明显可区分的形态特征。浮游生物的高度多样性已通过全面的元条形码调查得到证实，但由于遗传多样性与形态分类学和生态观察的整合不足，阻碍了对潜在分子分类学的解释。在这里，我们使用浮游有孔虫作为研究模型，揭示其遗传多样性的全部范围，并研究其分布的地理和生态模式。为此，我们组装了从形态特征的个体有孔虫中获得的约 7600 个核糖体 DNA 序列的全球数据集，为观察到的多样性建立了强大的分子分类框架，并用它来查询覆盖约 1700 个样本的全球元条形码数据集，其中约24.8 亿阅读量。这使我们能够提取和分配 100 万个读数，从而能够表征全球约 1100 个海洋站的群体遗传多样性结构。我们的抽样表明，最多存在 94 个不同的分子操作分类单元 (MOTU)，其分歧水平表明生物物种。遗传多样性仅使通过形态特征识别的正式描述的物种数量增加一倍。此外，我们观察到遗传多样性在形态种上的分配是不均匀的。只有 16 个形态种掩盖了具有进化意义的遗传多样性，并且表现出遗传多样性的形态种比例向极地方向增加。最后，我们观察到 MOTU 的地理分布比形态种更窄，并且在某些情况下，属于相同形态种（隐秘种）的 MOTU 具有不同的环境偏好。总体而言，我们的分析表明，即使根据全球遗传采样，浮游有孔虫多样性也是有限的。然而，神秘多样性的程度和结构揭示了遗传多样化与形态多样化脱钩，暗示不同的分化水平发挥着不同的机制。