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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拓扑测试和人口建模揭示了巴拿马地峡形成后大加勒比海的一条新的物种形成途径


最近的基因组分析强调了许多分类群中基因流动物种形成的普遍性，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为重要，因为快速移动的洋流、广阔的深水以及海平面上升和下降的周期性事件充当了软性和临时的异体屏障，促进了分歧和二次接触。在这些情况下，预计基因流动不会完全停止，而当代分布预计与历史分布不同。在这里，我们对 Pederson 的清洁虾 （Ancylomenes pedersoni） 进行了范围范围的采样，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，具有同种异体和同源分布。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建模（10 个位点频率重复 x 45 个进化模型 x 50 个模型模拟/复制 = 22,500 次模拟）相结合，以测试物种边界并重建预期为简单案例研究的进化历史。相反，我们的结果表明异体分化、次生接触、渗入和地方性杂交物种形成的历史，我们假设这是由巴拿马地峡的最终关闭和湾流在 ~350 万年前加强驱动的。 通过允许网状化的基于模型的方法恢复的这种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，考虑到当代分布，这是出乎意料的。通过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由地球历史上最具生物地理意义的事件之一引起的物种形成的新途径。