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Ancient DNA of the Extinct Jamaican Monkey Xenothrix Reveals Extreme Insular Change Within a Morphologically Conservative Radiation

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Ancient DNA of the Extinct Jamaican Monkey Xenothrix Reveals Extreme Insular Change Within a Morphologically Conservative Radiation Ancient DNA of the extinct Jamaican monkey Xenothrix reveals extreme insular change within a morphologically conservative radiation Roseina Woodsa,b, Samuel T. Turveyc,1, Selina Bracea, Ross D. E. MacPheed, and Ian Barnesa aDepartment of Earth Sciences, Natural History Museum, London SW7 5BD, United Kingdom; bSchool of Biological Sciences, Royal Holloway University of London, Egham TW20 0EX, United Kingdom; cInstitute of Zoology, Zoological Society of London, London NW1 4RY, United Kingdom; and dDepartment of Mammalogy, American Museum of Natural History, New York, NY 10024 Edited by C. Owen Lovejoy, Kent State University, Kent, OH, and approved September 27, 2018 (received for review May 21, 2018) The insular Caribbean until recently contained a diverse mammal remain evolutionarily enigmatic, often with multiple competing fauna including four endemic platyrrhine primate species, all of noncongruent phylogenetic hypotheses derived from restricted which died out during the Holocene. Previous morphological morphological datasets (10, 11). Improved molecular sampling of studies have attempted to establish how these primates are extinct taxa is necessary to resolve these conflicts and reconstruct related to fossil and extant platyrrhines, whether they represent the evolution of insular biotas through time, and distinguish be- ancient or recent colonists, and whether they constitute a mono- tween morphologies representing adaptive responses to island phyletic group. These efforts have generated multiple conflicting environments versus those representing “primitive” traits lost from hypotheses, from close sister-taxon relationships with several continental representatives of diversifying clades. However, mo- different extant platyrrhines to derivation from a stem platyrrhine lecular study of extinct species from tropical islands is limited by lineage outside the extant Neotropical radiation. This diversity of preservation of DNA, which is greatly reduced by the high thermal opinion reflects the fact that Caribbean primates were morpho- age represented by hot, humid tropical conditions (12, 13). logically extremely unusual, displaying numerous autapomorphies Oceanic-type (noncontinental) islands have rarely been colo- and apparently derived conditions present across different plat- nized by terrestrial mammals, limiting investigation of evolu- yrrhine clades. Here we report ancient DNA data for an extinct tionary patterns and processes in one of the best-studied animal Caribbean primate: a limited-coverage entire mitochondrial ge- groups. The insular Caribbean is remarkable in this context, as it nome and seven regions of nuclear genome for the most morpho- contained a diverse late Quaternary terrestrial mammal fauna logically derived taxon, the Jamaican monkey Xenothrix mcgregori. including lipotyphlan insectivores, rodents, sloths, and primates. We demonstrate that Xenothrix is part of the existing platyrrhine However, most of these species disappeared during the world’s radiation rather than a late-surviving stem platyrrhine, despite its largest postglacial mammal extinction event, correlated with ar- unusual adaptations, and falls within the species-rich but morpho- rival of human colonists from the mid-Holocene onward, which logically conservative titi monkey clade (Callicebinae) as sister to led to complete loss of several Caribbean mammal groups, in- the newly recognized genus Cheracebus. These results are not con- cluding all of the endemic primates (6, 14). gruent with previous morphology-based hypotheses and suggest that even morphologically conservative lineages can exhibit phe- netic plasticity in novel environments like those found on islands. Significance Xenothrix and Cheracebus diverged ca. 11 Ma, but primates have been present in the Caribbean since 17.5–18.5 Ma, indicating that Until recently, the Caribbean contained a remarkable evolu- Caribbean primate diversity was generated by multiple over-water tionary radiation of mammals, including several highly unusual colonizations. primates; the oddest was the Jamaican monkey Xenothrix. Unfortunately, all of these primates are now extinct, and ef- biogeography | Callicebus | extinct mammal | island evolution | phylogeny forts to reconstruct their evolutionary history have had to use limited morphological information from incomplete subfossils. Despite generally poor preservation of DNA in ancient tropical slands are the home of spectacular evolutionary novelty and samples, we extracted the first ancient DNA from an extinct have long acted as “natural laboratories” that have inspired I Caribbean primate, which reveals that, instead of being dis- evolutionary thinking (1–3). For example, the biota of the insular tantly related to living Neotropical monkeys, Xenothrix is ac- Caribbean has been extensively studied to test competing hy- EVOLUTION tually an extremely derived titi monkey that underwent major potheses for island colonization by vicariance, land bridges, or body-plan modification after colonizing an island environment. over-water dispersal and to reconstruct ecological drivers and The date of the split between Xenothrix and other titi monkeys evolutionary dynamics of morphological differentiation under also reveals that primates colonized the Caribbean more novel environments (2, 3). Insular taxa frequently exhibit unusual than once. morphologies that differ markedly from continental taxa (4), which can represent either evolutionary responses to unique Author contributions: R.W., S.T.T., R.D.E.M., and I.B. designed research; R.W. and S.B. ecological conditions on islands or “ancestral” traits of ancient performed research; R.D.E.M. and I.B. contributed new reagents/analytic tools; R.W., lineages with relict distributions (5, 6). Morphological characters S.T.T., S.B., and I.B. analyzed data; and R.W., S.T.T., R.D.E.M., and I.B. wrote the paper. have been of limited usefulness for reconstructing evolutionary The authors declare no conflict of interest. histories of many morphologically unusual island taxa, and the This article is a PNAS Direct Submission. advent of molecular phylogenetic methods has overturned Published under the PNAS license. morphology-based hypotheses about the affinities of several Data deposition: Sequence data have been submitted to GenBank, https://www.ncbi.nlm. insular lineages (7–9). nih.gov/genbank (accession nos. MK073942–MK073960). Most island systems have experienced high levels of human- 1To whom correspondence should be addressed. Email: [email protected]. caused biodiversity loss (6), and many unusual insular taxa are This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. now extinct and represented only by incomplete subfossil re- 1073/pnas.1808603115/-/DCSupplemental. mains. In the absence of molecular analyses, such taxa can Published online November 12, 2018. www.pnas.org/cgi/doi/10.1073/pnas.1808603115 PNAS | December 11, 2018 | vol. 115 | no. 50 | 12769–12774 Downloaded by guest on September 25, 2021 Primates of the Caribbean The oldest Caribbean primate, Paralouatta marianae, is known from an astragalus dated to ca. 17.5–18.5 Ma (Early Miocene) based on associated invertebrates and sequence stratigraphy at Domo de Zaza, central Cuba. This fossil provides the earliest constrained age for regional presence of primates (15). Recent discovery of a tick in mid-Tertiary amber, containing blood cells similar to those of primates but not other Caribbean mammals, has been interpreted as evidence of possible primate occurrence on Hispaniola from at least 15 Ma and possibly 30–45 Ma (16). All other Caribbean primates [Antillothrix bernensis and Insu- lacebus toussaintiana from Hispaniola, Paralouatta varonai from Cuba, and Xenothrix mcgregori from Jamaica (6, 17, 18)] are known from late Quaternary cave deposits. Several taxa persisted into the Holocene and were contemporaneous with prehistoric human settlers (6, 14). Xenothrix was apparently the last surviving Caribbean primate: a direct accelerator mass spectrometry (AMS) date of 1477 ± 34 B.P. gives an estimated last-occurrence date of ca. 900 B.P. (19), and European accounts of otherwise unknown primate-like animals from Jamaica suggest possible his- torical survival (20). An outstanding aspect of Caribbean primates is their mor- phological uniqueness. All were clearly platyrrhines, but they exhibit features and character combinations that are rare or absent in living taxa. Uniqueness is particularly noteworthy in Xenothrix, described as “the most enigmatic of all South Amer- ican fossil monkeys” (21) (Fig. 1). Xenothrix lacks third molars, potentially representing a derived resemblance to callitrichids (marmosets). However, dental reduction in callitrichids is pos- sibly associated with body-size reduction (22), whereas Xenothrix was comparable in size to the much larger Cebus (capuchins). Another highly unusual autapomorphy of Xenothrix is size dis- proportion of cheek teeth, with the first molars much larger than the second (17). Other features that, in combination, differen- tiate Xenothrix from other platyrrhines exist in the shape of the mandible, size of orbit, and volume of maxillary sinuses (23). The postcranial morphology of Xenothrix is comparably unusual, re- vealing it was a slow-moving arboreal quadruped, a locomotory adaptation unique in recent platyrrhines (20). Other Caribbean monkeys exhibit similarly distinctive characters (e.g., evidence of semiterrestriality in P. varonai), which further complicates mor- phological
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