Traditions in spider monkeys are biased towards the social domain

Cross-site comparison studies of behavioral variation can provide evidence for traditions in wild species once ecological and genetic factors are excluded as causes for cross-site differences. These studies ensure behavior variants are considered within the context of a species' ecology and evolutionary adaptations. We examined wide-scale geographic variation in the behavior of spider monkeys (Ateles geoffroyi) across five long-term field sites in Central America using a well established ethnographic cross-site survey method. Spider monkeys possess a relatively rare social system with a high degree of fission-fusion dynamics, also typical of chimpanzees (Pan troglodytes) and humans (Homo sapiens). From the initial 62 behaviors surveyed 65% failed to meet the necessary criteria for traditions. The remaining 22 behaviors showed cross-site variation in occurrence ranging from absent through to customary, representing to our knowledge, the first documented cases of traditions in this taxon and only the second case of multiple traditions in a New World monkey species. Of the 22 behavioral variants recorded across all sites, on average 57% occurred in the social domain, 19% in food-related domains and 24% in other domains. This social bias contrasts with the food-related bias reported in great ape cross-site comparison studies and has implications for the evolution of human culture. No pattern of geographical radiation was found in relation to distance across sites. Our findings promote A. geoffroyi as a model species to investigate traditions with field and captive based experiments and emphasize the importance of the social domain for the study of animal traditions.Research at Barro Colorado Island was supported by grants from the National Science Foundation (SBR-9711161), the Leakey Foundation, the Department of Anthropology, University of California, Berkeley (www.berkeley.edu) and a Short-term Fellowship from the Smithsonian Tropical Research Institute (www.stri.org). Research at Corcovado National Park's Sirena Biological Station was supported by NSF award 0233248 (with R. Sussman), the Wenner-Gren Foundation, the Leakey Foundation, the American Society of Primatologists (www.asp.org), and Washington University in St. Louis (www.wustl.edu). Funds for Sirena's field lab facility were provided to L. E. Gilbert (Univ. of Texas at Austin) by NSF BSR 8315399 and a matching WWF grant, and funds for updating Sirena's trail system and installation of spatial reference system were provided by the Mellon Foundation through the Institute of Latin American Studies at UT Austin. Research at Santa Rosa and Punta Laguna was supported by The British Academy (www.britac.ac.uk), the Wenner-Gren Foundation (www.wennergren.org), the Leakey Foundation (www.leakeyfoundation.org) and the North of England Zoological Society (www.chesterzoo.org). CJS was supported by a Gladstone bursary from the University of Chester (www.chester.ac.uk) and by the Santander University Scheme (www.santander.co.uk). Research at Runaway Creek was supported by the Natural Sciences and Engineering Research Council of Canada. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript

Conservation Genetics of the Philippine Tarsier: Cryptic Genetic Variation Restructures Conservation Priorities for an Island Archipelago Primate

Acknowledgments We thank the Philippine Department of Environment and Natural Resources for facilitating research, sample collection, and export permits (in particular T. M. Lim, C. Custodio, J. deLeon, and A. Tagtag) necessary for this and related research. Sampling protocols were approved by the University of Kansas Animal Care and Use Committee (IACUC 158-01 to RMB) and protocols to capture, sedate, and harvest ear biopsies from wild tarsiers were approved by the Dartmouth Animal Care and Use Committee (IACUC 10-11-12 and 11-06-06AT to NJD). Thanks are due to J. Quilang for assistance with data and comments on the manuscript. We thank N. Antoque, J. Cantil, and V. Yngente for assistance in the field and anonymous reviewers for comments on previous versions of the manuscript.Author Contributions Conceived and designed the experiments: RMB JAW CDS JAE MS MLD ACD. Performed the experiments: RMB MRMD LVD INA JAE NJD PSO AL MLD ACD CDS. Analyzed the data: KVO AJB CDS. Contributed reagents/materials/analysis tools: RMB KVO AJB CDS JAE LVD GLM. Wrote the paper: RMB JAW CDS JAE MS GLM. Obtained permission and executed field surveys: RMB MRMD LVD MS INA JAE NJD PSO GLM AL MLD ACD CDS.Establishment of conservation priorities for primates is a particular concern in the island archipelagos of Southeast Asia, where rates of habitat destruction are among the highest in the world. Conservation programs require knowledge of taxonomic diversity to ensure success. The Philippine tarsier is a flagship species that promotes environmental awareness and a thriving ecotourism economy in the Philippines. However, assessment of its conservation status has been impeded by taxonomic uncertainty, a paucity of field studies, and a lack of vouchered specimens and genetic samples available for study in biodiversity repositories. Consequently, conservation priorities are unclear. In this study we use mitochondrial and nuclear DNA to empirically infer geographic partitioning of genetic variation and to identify evolutionarily distinct lineages for conservation action. The distribution of Philippine tarsier genetic diversity is neither congruent with expectations based on biogeographical patterns documented in other Philippine vertebrates, nor does it agree with the most recent Philippine tarsier taxonomic arrangement. We identify three principal evolutionary lineages that do not correspond to the currently recognized subspecies, highlight the discovery of a novel cryptic and range-restricted subcenter of genetic variation in an unanticipated part of the archipelago, and identify additional geographically structured genetic variation that should be the focus of future studies and conservation action. Conservation of this flagship species necessitates establishment of protected areas and targeted conservation programs within the range of each genetically distinct variant of the Philippine tarsier.Support for fieldwork was provided by the University of Kansas Biodiversity Institute and Department of Ecology and Evolutionary Biology (to RMB, CDS, and JAE), the National Geographic Society (NGS 8446-08 to RMB, JAW, MS and INA), funds from the Primate Action Fund (to MS), Ewha Womans University (Ewha Global Top5 Grant 2013 to MS), the David and Lucile Packard Foundation (Fellowship in Science and Engineering no. 2007-31754, to NJD), and U.S. National Science Foundation (DEB 0743491 to RMB). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.Yeshttp://www.plosone.org/static/editorial#pee

Data from: Conservation genetics of the Philippine tarsier: cryptic genetic variation restructures conservation priorities for an island archipelago primate

Establishment of conservation priorities for primates is a particular concern in the island archipelagos of Southeast Asia, where rates of habitat destruction are among the highest in the world. Conservation programs require knowledge of taxonomic diversity to ensure success. The Philippine tarsier is a flagship species that promotes environmental awareness and a thriving ecotourism economy in the Philippines. However, assessment of its conservation status has been impeded by taxonomic uncertainty, a paucity of field studies, and a lack of vouchered specimens and genetic samples available for study in biodiversity repositories. Consequently, conservation priorities are unclear. In this study we use mitochondrial and nuclear DNA to empirically infer geographic partitioning of genetic variation and to identify evolutionarily distinct lineages for conservation action. The distribution of Philippine tarsier genetic diversity is neither congruent with expectations based on biogeographical patterns documented in other Philippine vertebrates, nor does it agree with the most recent Philippine tarsier taxonomic arrangement. We identify three principal evolutionary lineages that do not correspond to the currently recognized subspecies, highlight the discovery of a novel cryptic and range-restricted subcenter of genetic variation in an unanticipated part of the archipelago, and identify additional geographically structured genetic variation that should be the focus of future studies and conservation action. Conservation of this flagship species necessitates establishment of protected areas and targeted conservation programs within the range of each genetically distinct variant of the Philippine tarsier

Tarsier_Convert_input

Tarsier microsatelite

Phylogeographic relationships of <i>Tarsius syrichta</i> (see Appendix S1 for taxonomic summary) estimated from a combined, partitioned, RAxML ML analysis of mitochondrial (12S, CytB, ND2) gene fragments.

<p>Black circles at nodes correspond to ML bootstraps ≥70% and Bayesian PP ≥95%.</p

Uncorrected mitochondrial sequence divergence (%) among Philippine tarsier (<i>Tarsius syrichta</i>) evolutionary lineages shown below diagonal.

<p>Percentages on the diagonal represent intraspecific (or within clade) genetic diversity. Mean inferred migration rates (inferred in BAYESASS) between regionally partitioned diversity shown above diagonal. Migration rates above the 0.05 threshold bolded for emphasis.</p

DISTRUCT visualization of STRUCTURE analyses (A) assigning individuals to major population groupings (genetically distinct evolutionary lineages) for Philippine tarsier demes (<i>K</i> = 2 and 3 populations).

<p>Mindanao faunal region (B; see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0104340#pone-0104340-g001" target="_blank">Fig. 1</a>, inset) with sampling (17 sites, 66 individuals) labeled with letters corresponding to full localities listed in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0104340#pone.0104340.s002" target="_blank">Appendix S2</a>, protected areas shaded red. SplitsTree gene network (C; numbers at internodes = ML bootstrap replicates), and results of GMYC analyses (red asterisks denote lineages delineated by the Yule-coalescent), with numbers at tips corresponding to individual samples in Structure plots (A) and cluster shading corresponding to islands on map (B).</p

Microsatellite variation in 66 individuals of <i>Tarsius syrichta</i> from 17 localities (Fig. 2).

<p>Abbreviations include: <i>N</i>, number of samples; <i>H</i>_O, observed heterozygosity; <i>H</i>_E, expected heterozygosity; <i>L</i>_P, number of polymorphic loci; <i>F</i>_IS inbreeding coefficient.</p

Models of evolution selected by AIC and applied for partitioned, phylogeographic analyses¹.

1<p>The model GTR + Γ was used for partitioned RAxMLHPC analyses.</p