Llaberia-Robledillo Mar, Lucas-Lledó José Ignacio, Balbuena Juan Antonio, Brabec Jan, Bilat Julia, Knudsen Rune, Seehausen Ole, Blasco-Costa Isabel
Cavanilles Institute of Biodiversity and Evolutionary Biology, University of Valencia, Valencia, Spain.
Department of Invertebrates, Natural History Museum of Geneva, Geneva, Switzerland.
Mol Ecol. 2025 Sep;34(17):e70039. doi: 10.1111/mec.70039. Epub 2025 Jul 16.
Postglacial environmental changes have influenced biodiversity and species evolution, yet the genomic and demographic responses of parasites remain underexplored. This study investigates the population genetics and demographic history of the flatworm Phyllodistomum umblae, a generalist trematode at the definitive host level infecting Coregonus spp. across perialpine and subarctic postglacial lakes. Additionally, we compare its demographic patterns to Proteocephalus fallax, a whitefish specialist tapeworm, to elucidate how ecological strategies shape evolutionary responses to environmental fluctuations. Genomic data from ddRAD sequencing revealed clear genetic differentiation in P. umblae between subarctic and perialpine regions, likely driven by geographic isolation during glacial cycles. Low genetic differentiation suggests hydrological connectivity and the parasite's ability to utilise several host species as definitive hosts. Demographic inference uncovered distinct evolutionary trajectories between P. umblae and Pr. fallax. During the Last Glacial Period (115-11 kya), P. umblae populations underwent declines, followed by rapid postglacial expansions after the Last Glacial Maximum (15-10 kya). In contrast, Pr. fallax exhibited older historical fluctuations, including pronounced bottlenecks during the Middle Pleistocene (~300 kya). Its populations remained stable during the LGP, likely due to host persistence in glacial refugia unavailable in earlier glaciation periods. These findings align with the taxon pulse concept within the Stockholm Paradigm, highlighting how glacial cycles triggered episodic population contractions and expansions. By integrating genomic and historical data, this study (1) underscores parasites as models for understanding ecological and evolutionary processes and (2) provides insights into biodiversity resilience and adaptation to past and future environmental changes.
冰期后的环境变化影响了生物多样性和物种进化,然而寄生虫的基因组和种群动态响应仍未得到充分研究。本研究调查了扁形虫Phyllodistomum umblae的种群遗传学和种群历史,它是一种在终末宿主层面上感染高山周边和亚北极冰期后湖泊中白鲑属鱼类的泛化吸虫。此外,我们将其种群动态模式与白鲑专性绦虫Proteocephalus fallax进行比较,以阐明生态策略如何塑造对环境波动的进化响应。来自ddRAD测序的基因组数据显示,亚北极和高山周边地区的P. umblae之间存在明显的遗传分化,这可能是由冰期循环期间的地理隔离驱动的。低遗传分化表明水文连通性以及该寄生虫利用多种宿主物种作为终末宿主的能力。种群动态推断揭示了P. umblae和Pr. fallax之间不同的进化轨迹。在末次冰期(约11.5 - 1.1万年前),P. umblae种群数量下降,随后在末次盛冰期(约1.5 - 1万年前)之后迅速进行冰期后扩张。相比之下,Pr. fallax表现出更古老的历史波动,包括在中更新世(约30万年前)出现明显的瓶颈期。其种群在末次冰期保持稳定,可能是由于宿主在早期冰期不存在的冰川避难所中得以存续。这些发现与斯德哥尔摩范式中的分类群脉冲概念一致,突出了冰期循环如何引发间歇性的种群收缩和扩张。通过整合基因组和历史数据,本研究(1)强调了寄生虫作为理解生态和进化过程的模型,(2)为生物多样性恢复力以及对过去和未来环境变化适应性提供了见解。