Ancient DNA Suggests Single Colonization and Within-Archipelago Diversification of Caribbean Caviomorph Rodents

Reconstructing the evolutionary history of island biotas is complicated by unusual morphological evolution in insular environments. However, past human-caused extinctions limit the use of molecular analyses to determine origins and affinities of enigmatic island taxa. The Caribbean formerly contained a morphologically diverse assemblage of caviomorph rodents (33 species in 19 genera), ranging from similar to 0.1 to 200kg and traditionally classified into three higher-order taxa (Capromyidae/Capromyinae, Heteropsomyinae, and Heptaxodontidae). Few species survive today, and the evolutionary affinities of living and extinct Caribbean caviomorphs to each other and to mainland taxa are unclear: Are they monophyletic, polyphyletic, or paraphyletic? We use ancient DNA techniques to present the first genetic data for extinct heteropsomyines and heptaxodontids, as well as for several extinct capromyids, and demonstrate through analysis of mitogenomic and nuclear data sets that all sampled Caribbean caviomorphs represent a well-supported monophyletic group. The remarkable morphological and ecological variation observed across living and extinct caviomorphs from Cuba, Hispaniola, Jamaica, Puerto Rico, and other islands was generated through within-archipelago evolutionary radiation following a single Early Miocene overwater colonization. This evolutionary pattern contrasts with the origination of diversity in many other Caribbean groups. All living and extinct Caribbean caviomorphs comprise a single biologically remarkable subfamily (Capromyinae) within the morphologically conservative living Neotropical family Echimyidae. Caribbean caviomorphs represent an important new example of insular mammalian adaptive radiation, where taxa retaining ancestral-type characteristics coexisted alongside taxa occupying novel island niches. Diversification was associated with the greatest insular body mass increase recorded in rodents and possibly the greatest for any mammal lineage.

Automated summary

This study uses ancient DNA techniques to show that Caribbean caviomorphs form a well-supported monophyletic group, with their remarkable morphological and ecological variation resulting from evolutionary radiation post a single Early Miocene colonization event. The living and extinct caviomorphs in the Caribbean are part of a biologically remarkable subfamily within the living Neotropical family Echimyidae, representing an important example of insular mammalian adaptive radiation where ancestral-type characteristics coexisted with taxa occupying novel island niches. The diversification of Caribbean caviomorphs is associated with the largest insular body mass increase observed in rodents and possibly any mammal lineage.