European mountain systems played a crucial role in shaping the distribution of species and of their genetic diversity during the Quaternary's climatic changes with the establishment of allopatric patterns across main mountain ranges. Here we investigated the evolutionary history of flea beetles of the Longitarsus candidulus species-group showing an uncommon disjunct biogeographic pattern across the Apennine and the Pyrenees. We applied a multilocus molecular approach and multispecies coalescent models to establish a phylogenetic and systematic framework for this morphologically homogeneous species-group and to estimate the time of main cladogenetic events underlying the origin of the Apennine-Pyrenees pattern. We found strong support for the monophyly of the candidulus group with a sister relationship between L. laureolae and L. leonardii endemic to the Apennine and the Pyrenees mountains respectively. The timing of speciation events in the candidulus species-group coincide with two major climatic transitions during Early and Middle Pleistocene that resulted in significant environmental changes in Europe and suggest a scenario of allopatric isolation and divergence on distinct mountain ranges. The split between the thermophilic species L. candidulus and the ancestor of the temperate species L. laureolae and L. leonardii, estimated at ~ 3 Ma during the transition from Pliocene to Pleistocene, was probably triggered by their segregation in xerophilous and temperate habitats. The speciation between L. laureolae and L. leonardii, ~ 1 Ma during the Mid-Pleistocene Transition, can be explained by the establishment of unfavorable conditions in West Alps and Central Massif underlying the onset of the Apennine-Pyrenees disjunct pattern. Finally, the strict association between members of the candidulus group and distinct Thymelaeaceae plants suggests further studies to address the hypothesis that speciation in these flea beetles might have been also associated with Pleistocene range changes of their host plants.

中文翻译：

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亚平宁-比利牛斯山脉间断分布：长毛跳蚤甲虫（鞘翅目、叶甲科）揭示的不寻常的生物地理模式

第四纪气候变化期间，随着主要山脉异域分布模式的建立，欧洲山区系统在塑造物种分布及其遗传多样性方面发挥了至关重要的作用。在这里，我们研究了 Longitarsus candidulus 物种组的跳蚤甲虫的进化史，显示出亚平宁山脉和比利牛斯山脉罕见的分离生物地理模式。我们应用多位点分子方法和多物种合并模型为这个形态上同质的物种组建立系统发育和系统框架，并估计亚平宁-比利牛斯模式起源的主要分支发育事件的时间。我们发现了对candidulus组的单系性的有力支持，其中L. laureolae和L. leonardii分别是亚平宁山脉和比利牛斯山脉特有的姐妹关系。candidulus物种组中物种形成事件的时间与早更新世和中更新世期间的两次主要气候转变相吻合，这导致了欧洲的重大环境变化，并暗示了不同山脉上异域隔离和分化的情况。嗜热物种 L. candidulus 与温带物种 L. laureolae 和 L. leonardii 的祖先之间的分裂，估计在上新世到更新世过渡期间约 3 Ma，可能是由它们在干旱和温带生境中的隔离引发的。L. laureolae 和 L. leonardii 之间的物种形成，约 1Ma，发生在中更新世过渡期间，可以通过西阿尔卑斯山和中央地块在亚平宁-比利牛斯山脉分离模式开始时建立的不利条件来解释。最后，candidulus 组成员与不同的瑞香科植物之间的严格关联表明，需要进一步研究来解决这些跳甲虫的物种形成也可能与其寄主植物的更新世范围变化有关的假设。