Ancient DNA and high-resolution chronometry reveal a long-term human role in the historical diversity and biogeography of the Bahamian hutia

www.nature.com/scientificreports OPEN Ancient DNA and high-resolution chronometry reveal a long-term human role in the historical diversity and biogeography of the Bahamian hutia Jessica A. Oswald1,2*, Julie M. Allen2,3, Michelle J. LeFebvre1, Brian J. Stucky1, Ryan A. Folk1,4, Nancy A. Albury5, Gary S. Morgan6, Robert P. Guralnick1 & David W. Steadman1 Quaternary paleontological and archaeological evidence often is crucial for uncovering the historical mechanisms shaping modern diversity and distributions. We take an interdisciplinary approach using multiple lines of evidence to understand how past human activity has shaped long-term animal diversity in an island system. Islands afford unique opportunities for such studies given their robust fossil and archaeological records. Herein, we examine the only non-volant terrestrial mammal endemic to the Bahamian Archipelago, the hutia Geocapromys ingrahami. This capromyine rodent once inhabited many islands but is now restricted to several small cays. Radiocarbon dated fossils indicate that hutias were present on the Great Bahama Bank islands before humans arrived at AD ~800–1000; all dates from other islands post-date human arrival. Using ancient DNA from a subset of these fossils, along with modern representatives of Bahamian hutia and related taxa, we develop a fossil-calibrated phylogeny. We found little genetic divergence among individuals from within either the northern or southern Bahamas but discovered a relatively deep North-South divergence (~750 ka). This result, combined with radiocarbon dating and archaeological evidence, reveals a pre-human biogeographic divergence, and an unexpected human role in shaping Bahamian hutia diversity and biogeography across islands. The modern diversity and distribution of species are due to both natural factors across geological time, and human activities during the Quaternary. Humans have caused extinctions and contraction/fragmentation of ranges in countless species, while at the same time benefiting other species through introductions, habitat modification, and domestication. Long appreciated as places to study evolution, extinction, biogeography, and archaeology1–3, many islands also provide excellent settings to evaluate the relative roles of climate and associated habitat change versus human activities in shaping modern plant and animal communities e.g.4,5. In the West Indies, for example, the record of vertebrates from archaeological (cultural) and paleontological (non-cultural) sites reveals substantial extinction (species-level loss) and extirpation (population-level loss) of species since the late Quaternary. Some of these losses are thought to be related to the major changes in sea level, land area, and climate during the Pleistocene-Holocene Transition (the PHT; ~15,000 to 9,000 BP6–9). Even more extinction and extirpation of West Indian reptiles, birds, and mammals took place after human arrival ~7,000 BP10–13. For example, Cuba and Hispaniola were the world’s last refuge for ground sloths, which became extinct ~4,500 BP; their continental relatives, on the other hand, went extinct about 6,000 years earlier, at the end of the Pleistocene4. An endemic Jamaican monkey survived until only ~900 BP12. The Bahamian Archipelago (The Bahamas + The Turks & Caicos Islands) extends from near Florida southeastward toward eastern Cuba and Hispaniola (modern day Haiti and Dominican Republic; Fig. 1). Islands of the 1 Florida Museum of Natural History, University of Florida, Gainesville, FL, 32611, USA. 2Biology Department, University of Nevada Reno, Reno, NV, 89557, USA. 3Illinois Natural History Survey, University of Illinois UrbanaChampaign, Urbana, IL, 61801, USA. 4Department of Biological Sciences, Mississippi State University, Starkville, MS, 39762, USA. 5National Museum of The Bahamas, Marsh Harbour, Abaco, Bahamas. 6New Mexico Museum of Natural History, 1801 Mountain Road NW, Albuquerque, NM, 87104, USA. *email: Scientific Reports | (2020) 10:1373 | https://doi.org/10.1038/s41598-020-58224-y 1 www.nature.com/scientificreports/ www.nature.com/scientificreports Figure 1. The Bahamian Archipelago. The lightest shade of blue represents the carbonate banks. On the Little Bahamas Bank, for example, are the islands of Grand Bahama and Abaco. Major islands on the Great Bahama Bank include Andros, New Providence, Eleuthera, and Long Island. The Crooked-Acklins Bank sustains Crooked and Acklins islands. Islands such as Mayaguana and Inagua were never connected to any other islands regardless of sea levels. The Lucayans colonized the Bahamas either from Cuba and/or from Hispaniola. Historically, Bahamian hutia occurred across the Bahamas. Today hutias are restricted to a few small islands (indicated by red arrows) including Little Wax Cay (1), Warderick Wells Cay (2), and East Plana Cay (labeled). Stars indicate the successful sampling localities for the ancient DNA portion of this study. The earliest archaeological site that shows hutia exploitation is from Major’s Landing on Crooked Island42, which is under the star on Crooked Island. The genetic break found in our data is indicated by the black bar between Long Island and Crooked and Acklins Islands (see Results). To make this figure, we cropped the bathymetry data layer from Eakins and Sharma71 to the Caribbean region using ArcMap version 10.172. Bahamian Archipelago lie atop shallow-water carbonate banks that are separated by deep water. While islands on a given bank were connected to each other during lowered sea levels of Quaternary glacial intervals, the banks themselves remained isolated from each other. The sea-level-controlled expansion and contraction of land area on these banks through Quaternary glacial-interglacial cycles14 has strongly influenced the archipelago’s terrestrial plant and animal communities15. During glacially lowered sea levels, Bahamian islands were not connected to North America or to neighboring Cuba and Hispaniola, although the Great Bahama Bank (GBB) was only 20 km away from Cuba during glacial intervals7 (Fig. 1). All colonization of the archipelago by terrestrial organisms therefore had to involve trans-oceanic dispersal. The geographic proximity of the Bahamian Archipelago and Cuba likely underlies their high number of shared extinct, extirpated, and extant species between these islands. Human colonization of the Bahamian Archipelago occurred fairly recently (AD ~800-1100), making it feasible to distinguish human impacts on biodiversity from those that occurred at the PHT. The Bahamian Archipelago sustains only a single species of endemic non-volant mammal, the Bahamian hutia (Geocapromys ingrahami; Family Echimyidae, Subfamily Capromyinae16). The broader group of capromyine rodents are found in the Greater Antilles, Cayman Islands, Bahamas, and Swan Islands, although more than 50% of these species have been lost during the Holocene17–20. The oldest capromyine fossils are from the ear (...truncated)