Rapid size change associated with intra-island evolutionary radiation in extinct Caribbean “island-shrews”

Abstract

Background: 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. Results: 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 sizedifferentiated Hispaniolan Nesophontes species. We were also able to extract and sequence ancient DNA from a~750-yearold 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. Conclusions: 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.

Ancient mitogenomics elucidates diversity of extinct West Indian tortoises

“…Ten of the 17 subfossil Chelonoidis samples produced high-quality data representing nearly the entire mitochondrial genome (15,288–15,350 bp length, coverage: ninefold to 482-fold; Table S1 ). This is an excellent yield for aDNA from tropical environments 19 , 45 , especially when it is considered that some specimens were from open unsheltered sites (Table 1 ).…”

Complex plumages spur rapid color diversification in island kingfishers (Aves: Alcedinidae)

“…The “island rule” predicts that large bodied colonists evolve to be smaller on islands than their mainland congeners (dwarfism) and vice versa for smaller-bodied colonists to evolve to be large (gigantism). While less commonly assessed, these shifts in phenotype when moving to islands are likely accompanied by bursts in phenotypic evolutionary rate (Millien, 2006; Thomas et al, 2009; Woods et al, 2020). Another common feature of evolution on islands is the tendency for convergent evolution “island syndrome”), for example, in life history traits (Covas, 2012; Losos et al, 1998; Novosolov et al, 2013), behavior (Buglione et al, 2019; Roff, 1994), and morphology (Clegg and Owens, 2002; Wright et al, 2016).…”