Recent genomic analyses have highlighted the prevalence of speciation with gene flow in many taxa and have underscored the importance of accounting for these reticulate evolutionary processes when constructing species trees and generating parameter estimates. This is especially important for deepening our understanding of speciation in the sea where fast moving ocean currents, expanses of deep water, and periodic episodes of sea level rise and fall act as soft and temporary allopatric barriers that facilitate both divergence and secondary contact. Under these conditions, gene flow is not expected to cease completely while contemporary distributions are expected to differ from historical ones. Here we conduct range-wide sampling for Pederson’s cleaner shrimp (Ancylomenes pedersoni), a species complex from the Greater Caribbean that contains three clearly delimited mitochondrial lineages with both allopatric and sympatric distributions. Using mtDNA barcodes and a genomic ddRADseq approach, we combine classic phylogenetic analyses with extensive topology testing and demographic modeling (10 site frequency replicates x 45 evolutionary models x 50 model simulations/replicate = 22,500 simulations) to test species boundaries and reconstruct the evolutionary history of what was expected to be a simple case study. Instead, our results indicate a history of allopatric divergence, secondary contact, introgression, and endemic hybrid speciation that we hypothesize was driven by the final closure of the Isthmus of Panama and the strengthening of the Gulf Stream Current ~3.5 million years ago. The history of this species complex recovered by model-based methods that allow reticulation differs from that recovered by standard phylogenetic analyses and is unexpected given contemporary distributions. The geologically and biologically meaningful insights gained by our model selection analyses illuminate what is likely a novel pathway of species formation not previously documented that resulted from one of the most biogeographically significant events in Earth’s history.

中文翻译：

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拓扑测试和人口统计模型揭示了巴拿马地峡形成后大加勒比海的新物种形成途径


最近的基因组分析强调了许多类群中物种形成随基因流的普遍存在，并强调了在构建物种树和生成参数估计时考虑这些网状进化过程的重要性。这对于加深我们对海洋物种形成的理解尤其重要，因为快速移动的洋流、广阔的深水以及海平面升降的周期性事件充当了软性和临时的异域屏障，促进了分歧和二次接触。在这些条件下，基因流动预计不会完全停止，而当代分布预计将不同于历史分布。在这里，我们对佩德森清洁虾（Ancylomenes pedersoni）进行了范围广泛的采样，这是一种来自大加勒比地区的物种复合体，包含三个明确界定的线粒体谱系，具有异域和同域分布。使用 mtDNA 条形码和基因组 ddRADseq 方法，我们将经典的系统发育分析与广泛的拓扑测试和人口统计建模（10 个位点频率重复 x 45 个进化模型 x 50 个模型模拟/重复 = 22,500 次模拟）相结合，以测试物种边界并重建物种的进化历史。预计这将是一个简单的案例研究。相反，我们的结果表明了异域分化、次生接触、渗入和地方性混合物种形成的历史，我们假设这些历史是由巴拿马地峡的最终闭合和约 350 万年前墨西哥湾流的加强所驱动的。 通过基于模型的方法恢复的该物种复合体的历史与通过标准系统发育分析恢复的历史不同，并且考虑到当代分布，这是意想不到的。我们的模型选择分析获得的具有地质和生物学意义的见解阐明了可能是一种以前未记录过的物种形成的新途径，该途径是由地球历史上最具生物地理学意义的事件之一产生的。