The Caribbean offers a unique opportunity to study evolutionary dynamics in insular mammals. However, the recent extinction of most Caribbean non-volant mammals has obstructed evolutionary studies, and poor DNA preservation associated with tropical environments means that very few ancient DNA sequences are available for extinct vertebrates known from the region’s Holocene subfossil record. The endemic Caribbean eulipotyphlan family Nesophontidae (“island-shrews”) became extinct ~ 500 years ago, and the taxonomic validity of many Nesophontes species and their wider evolutionary dynamics remain unclear. Here we use both morphometric and palaeogenomic methods to clarify the status and evolutionary history of Nesophontes species from Hispaniola, the second-largest Caribbean island. Principal component analysis of 65 Nesophontes mandibles from late Quaternary fossil sites across Hispaniola identified three non-overlapping morphometric clusters, providing statistical support for the existence of three size-differentiated Hispaniolan Nesophontes species. We were also able to extract and sequence ancient DNA from a ~ 750-year-old specimen of Nesophontes zamicrus, the smallest non-volant Caribbean mammal, including a whole-mitochondrial genome and partial nuclear genes. Nesophontes paramicrus (39-47 g) and N. zamicrus (~ 10 g) diverged recently during the Middle Pleistocene (mean estimated divergence = 0.699 Ma), comparable to the youngest species splits in Eulipotyphla and other mammal groups. Pairwise genetic distance values for N. paramicrus and N. zamicrus based on mitochondrial and nuclear genes are low, but fall within the range of comparative pairwise data for extant eulipotyphlan species-pairs. Our combined morphometric and palaeogenomic analyses provide evidence for multiple co-occurring species and rapid body size evolution in Hispaniolan Nesophontes, in contrast to patterns of genetic and morphometric differentiation seen in Hispaniola’s extant non-volant land mammals. Different components of Hispaniola’s mammal fauna have therefore exhibited drastically different rates of morphological evolution. Morphological evolution in Nesophontes is also rapid compared to patterns across the Eulipotyphla, and our study provides an important new example of rapid body size change in a small-bodied insular vertebrate lineage. The Caribbean was a hotspot for evolutionary diversification as well as preserving ancient biodiversity, and studying the surviving representatives of its mammal fauna is insufficient to reveal the evolutionary patterns and processes that generated regional diversity.

中文翻译：

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已灭绝的加勒比“岛鼩”的体型快速变化与岛内进化辐射有关。


加勒比地区为研究岛屿哺乳动物的进化动态提供了独特的机会。然而，最近大多数加勒比海非飞行哺乳动物的灭绝阻碍了进化研究，而与热带环境相关的DNA保存不良意味着从该地区的全新世亚化石记录中已知的已灭绝脊椎动物的古代DNA序列非常少。加勒比地区特有的真鼩科 Nesophontidae（“岛鼩鼱”）在约 500 年前就灭绝了，许多 Nesophonttes 物种的分类学有效性及其更广泛的进化动态仍不清楚。在这里，我们使用形态测量和古基因组学方法来阐明来自加勒比第二大岛屿伊斯帕尼奥拉岛的Nesophontes物种的地位和进化历史。对来自伊斯帕尼奥拉岛晚第四纪化石遗址的 65 个 Nesophontes 下颌骨进行主成分分析，确定了三个不重叠的形态簇，为三种尺寸差异的伊斯帕尼奥拉 Nesophontes 物种的存在提供了统计支持。我们还能够从约 750 年前的 Nesophontes zamicrus（最小的非飞行加勒比哺乳动物）样本中提取古代 DNA 并进行测序，包括整个线粒体基因组和部分核基因。 Nesophontes paramicrus (39-47 g) 和 N. zamicrus (~ 10 g) 最近在中更新世期间发生了分歧（平均估计分歧 = 0.699 Ma），与 Eulipotyphla 和其他哺乳动物群体中最年轻的物种分裂相当。基于线粒体和核基因的 N. paramicrus 和 N. zamicrus 的成对遗传距离值较低，但属于现存真伤寒菌种对的比较成对数据范围内。 我们的形态测量和古基因组分析相结合，为伊斯帕尼奥拉尼索弗特斯的多个共存物种和快速的体型进化提供了证据，这与伊斯帕尼奥拉现存的非飞行陆地哺乳动物的遗传和形态分化模式形成鲜明对比。因此，伊斯帕尼奥拉岛哺乳动物群的不同组成部分表现出截然不同的形态进化速度。与Eulipotyphla的模式相比，Nesophontes的形态进化也很快，我们的研究提供了小型岛脊椎动物谱系中体型快速变化的重要新例子。加勒比地区是进化多样化以及保护古代生物多样性的热点地区，研究其哺乳动物群的幸存代表不足以揭示产生区域多样性的进化模式和过程。