The tropical Andes are an important natural laboratory to understand speciation in many taxa. Here we examined the evolutionary history of parasites of the Leishmania braziliensis species complex based on whole-genome sequencing of 67 isolates from 47 localities in Peru. We first show the origin of Andean Leishmania as a clade of near-clonal lineages that diverged from admixed Amazonian ancestors, accompanied by a significant reduction in genome diversity and large structural variations implicated in host–parasite interactions. Within the Andean species, patterns of population structure were strongly associated with biogeographical origin. Molecular clock and ecological niche modeling suggested that the history of diversification of the Andean lineages is limited to the Late Pleistocene and intimately associated with habitat contractions driven by climate change. These results suggest that changes in forestation over the past 150,000 y have influenced speciation and diversity of these Neotropical parasites. Second, genome-scale analyses provided evidence of meiotic-like recombination between Andean and Amazonian Leishmania species, resulting in full-genome hybrids. The mitochondrial genome of these hybrids consisted of homogeneous uniparental maxicircles, but minicircles originated from both parental species. We further show that mitochondrial minicircles—but not maxicircles—show a similar evolutionary pattern to the nuclear genome, suggesting that compatibility between nuclear-encoded mitochondrial genes and minicircle-encoded guide RNA genes is essential to maintain efficient respiration. By comparing full nuclear and mitochondrial genome ancestries, our data expand our appreciation on the genetic consequences of diversification and hybridization in parasitic protozoa.

热带安第斯山脉是了解许多分类群物种形成的重要自然实验室。在这里，我们基于来自秘鲁 47 个地区的 67 个分离株的全基因组测序，研究了巴西利什曼原虫物种复合体寄生虫的进化历史。我们首先展示安第斯利什曼原虫的起源作为从混合的亚马逊祖先分化而来的近克隆谱系的进化枝，伴随着基因组多样性的显着减少和与宿主 - 寄生虫相互作用有关的大结构变异。在安第斯物种中，种群结构模式与生物地理起源密切相关。分子钟和生态位模型表明，安第斯血统的多样化历史仅限于晚更新世，并且与气候变化导致的栖息地收缩密切相关。这些结果表明，过去 150,000 年的造林变化影响了这些新热带寄生虫的物种形成和多样性。其次，基因组规模分析提供了安第斯和亚马逊利什曼原虫之间减数分裂样重组的证据种，产生全基因组杂种。这些杂种的线粒体基因组由同质的单亲大环组成，但小环起源于两个亲本物种。我们进一步表明线粒体小环——但不是大环——显示出与核基因组相似的进化模式，这表明核编码的线粒体基因和小环编码的引导 RNA 基因之间的相容性对于维持有效呼吸至关重要。通过比较完整的核和线粒体基因组祖先，我们的数据扩大了我们对寄生原生动物多样化和杂交的遗传后果的认识。