Keogh Sean M, Johnson Nathan A, Smith Chase H, Sietman Bernard E, Garner Jeffrey T, Randklev Charles R, Simons Andrew M
Gantz Family Collections Center, Field Museum of Natural History, Chicago, Illinois, USA.
Bell Museum of Natural History, University of Minnesota, St. Paul, Minnesota, USA.
Mol Ecol. 2025 Jan;34(1):e17572. doi: 10.1111/mec.17572. Epub 2024 Nov 14.
The isolated river drainages of eastern North America serve as a natural laboratory to investigate the roles of allopatry and secondary contact in the evolutionary trajectories of recently diverged lineages. Drainage divides facilitate allopatric speciation, but due to their sensitivity to climatic and geomorphological changes, neighboring rivers frequently coalesce, creating recurrent opportunities of isolation and contact throughout the history of aquatic lineages. The freshwater mussel Quadrula quadrula is widely distributed across isolated rivers of eastern North America and possesses high phenotypic and molecular variation across its range. We integrate sequence data from three genomes, including female- and male-inherited mitochondrial markers and thousands of nuclear encoded SNPs with morphology and geography to illuminate the group's divergence history. Across contemporary isolated rivers, we found continuums of molecular and morphological variation, following a pattern of isolation by distance. In contact zones, hybridization was frequent with no apparent fitness consequences, as advanced hybrids were common. Accordingly, we recognize Q. quadrula as a single cohesive species with subspecific variation (Q. quadrula rumphiana). Demographic modeling and divergence dating supported a divergence history characterized by allopatric vicariance followed by secondary contact, likely driven by river rearrangements and Pleistocene glacial cycles. Despite clinal range-wide variation and hybridization in contact zones, the process-based species delimitation tool delimitR, which considers demographic scenarios like secondary contact, supported the delimitation of the maximum number of species tested. As such, when interpreting species delimitation results, we suggest careful consideration of spatial sampling and subsequent geographic patterns of biological variation, particularly for wide-ranging taxa.
北美东部孤立的河流排水系统可作为一个天然实验室，用于研究异域性和二次接触在最近分化的谱系进化轨迹中的作用。排水分水岭促进异域物种形成，但由于它们对气候和地貌变化敏感，相邻河流经常合并，在水生谱系的整个历史中创造了反复出现的隔离和接触机会。淡水贻贝Quadrula quadrula广泛分布于北美东部的孤立河流中，并且在其分布范围内具有高度的表型和分子变异。我们整合了来自三个基因组的序列数据，包括雌性和雄性遗传的线粒体标记以及数千个核编码的单核苷酸多态性，并结合形态学和地理学数据来阐明该群体的分化历史。在当代孤立的河流中，我们发现分子和形态变异呈连续状态，遵循距离隔离模式。在接触区，杂交频繁，且没有明显的适合度后果，因为高级杂种很常见。因此，我们将Quadrula quadrula识别为一个具有亚种变异（Quadrula quadrula rumphiana）的单一凝聚物种。种群统计学建模和分化年代测定支持了一种分化历史，其特征是异域性地理隔离随后是二次接触，这可能是由河流重新排列和更新世冰川周期驱动的。尽管在接触区存在渐变的全范围变异和杂交，但考虑二次接触等种群统计学情景的基于过程的物种界定工具delimitR支持了所测试的最大物种数的界定。因此，在解释物种界定结果时，我们建议仔细考虑空间采样以及随后生物变异的地理模式，特别是对于分布广泛的分类群。
