Abstract
BackgroundThe 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.ResultsPrincipal 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.ConclusionsOur 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.
Highlights
The Caribbean offers a unique opportunity to study evolutionary dynamics in insular mammals
Our combined morphometric-genetic framework provides a robust new baseline for interpreting morphological variation seen in subfossil samples of nesophontid islandshrews from the large Caribbean island of Hispaniola, and our complementary analyses clarify levels of both taxonomic diversity and evolutionary differentiation within this recently extinct island mammal fauna, providing a template for future investigation of biodiversity patterns observed in environmental archives
We were able to compare ancient DNA data for the largest-bodied and smallest-bodied representatives of Hispaniola’s radiation of Nesophontes species, and the rapid rate of morphological evolution that we demonstrate in our palaeogenomic analyses of Hispaniolan Nesophontes is remarkable
Summary
The Caribbean offers a unique opportunity to study evolutionary dynamics in insular mammals. 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. We use both morphometric and palaeogenomic methods to clarify the status and evolutionary history of Nesophontes species from Hispaniola, the second-largest Caribbean island. It is necessary to determine the extent to which variation in faunal samples from environmental archives represents specieslevel differentiation, as opposed to intraspecific variation within or between conspecific populations This can require both genetic and/or morphometric approaches [1,2,3,4], as well as comparative understanding from extant taxa about levels of variation expected within related living populations [5, 6]. Islands have experienced disproportionately high levels of human-caused extinction during recent millennia, with many extinct taxa known only from morphologically incomplete and molecularly degraded specimens preserved in the recent fossil or zooarchaeological records, hindering investigation of taxonomic baselines and evolutionary patterns [12,13,14]
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