Genomic tests of the species-pump hypothesis: recent island connectivity cycles drive population divergence but not speciation in Caribbean crickets across the Virgin Islands

Harnessing the power of genomic scans, we test the debated ‘species pump’ hypothesis that implicates repeated cycles of island connectivity and isolation as drivers of divergence. This question has gone understudied given the limited resolution of past molecular markers for studying such dynamic phenomena. With an average of 32000 SNPs from the genome of 136 individuals from ten populations of a Caribbean flightless ground cricket species (Amphiacusta sanctaecrucis) and a complementary set of statistical approaches, we infer a stepping-stone colonization model and high levels of genetic differentiation across the Virgin Islands, which have been periodically inter-connected until 8 ka. Estimates of divergence times from models based on the site frequency spectrum coincide with a period of repeated connection and fragmentation of the islands at 75–130 ka. These results are consistent with a role of island connectivity cycles in promoting genomic divergence and indicate that the genetic distinctiveness of island populations has persisted despite subsequent and extended interisland connections identified from bathymetric data. We discuss these findings in the broader context of Caribbean biogeography, and more specifically why high levels of genomic divergence across the Virgin Islands associated with repeated connectivity cycles do not actually translate into species diversification.

本研究借助基因组扫描（genomic scans）技术，对存在争议的"物种泵假说（species pump hypothesis）"展开检验——该假说提出岛屿反复出现的连通与隔离循环是驱动物种分化的核心因素。由于过往用于研究此类动态演化现象的分子标记分辨率不足，该议题长期未得到充分探讨。本研究针对加勒比地区10个种群、共计136只无翅地蟋蟀（*Amphiacusta sanctaecrucis*）的基因组开展分析，平均每个个体获得32000个单核苷酸多态性位点（single nucleotide polymorphism, SNP），并结合一套互补的统计分析方法，推断出维尔京群岛间存在踏脚石定殖模式，且群岛间种群遗传分化程度较高——这些岛屿直到距今8000年前仍处于周期性连通状态。基于位点频率频谱（site frequency spectrum, SFS）构建的模型所估算的分化时间，与7.5万至13万年前岛屿反复连通与破碎化的时期高度吻合。上述结果支持岛屿连通循环可促进基因组分化的观点，同时表明尽管水深数据（bathymetric data）显示后续存在长期的跨岛连通事件，各岛屿种群的遗传独特性仍得以保留。本研究将这些发现置于加勒比生物地理学的更广阔框架下展开讨论，并具体探讨了为何维尔京群岛内与反复连通循环相关的高水平基因组分化，并未实际催生物种多样化。