New Guinea Highland Wild Dogs Are the Original New Guinea Singing Dogs
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New Guinea highland wild dogs are the original New Guinea singing dogs Suriani Surbaktia,1, Heidi G. Parkerb,1, James K. McIntyrec, Hendra K. Maurya, Kylie M. Cairnsd, Meagan Selvige, Margaretha Pangau-Adama,e, Apolo Safonpoa, Leonardo Numberia, Dirk Y. P. Runtuboia, Brian W. Davisf,2, and Elaine A. Ostranderb,2 aDepartment of Biology, Universitas Cenderawasih, Jayapura, Papua 99224, Indonesia; bNational Human Genome Research Institute, National Institutes of Health, Bethesda MD 20892; cNew Guinea Highland Wild Dog Foundation, Fernandina Beach, FL 32034; dCentre for Ecosystem Science, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, NSW 2052, Australia; eDepartment of Conservation Biology, University of Göttingen, 37073 Göttingen Germany; and fDepartment of Veterinary Integrative Biosciences, Texas A&M University College of Veterinary Medicine, College Station, TX 77843 Contributed by Elaine A. Ostrander, July 17, 2020 (sent for review April 16, 2020; reviewed by Klaus-Peter Koepfli, Fernando Racimo, and Robert D. Schnabel) New Guinea singing dogs (NGSD) are identifiable by their name- on the island. NGSD were first described following collection of sake vocalizations, which are unlike any other canid population. a specimen at an altitude of about 2,100 m in Central Province, Their novel behaviors and potential singular origin during dog PNG, in 1897 (9, 10). Originally classified as a distinct species, domestication make them an attractive, but elusive, subject for Canis hallstromi, their taxonomy remains controversial in part evolutionary and conservation study. Although once plentiful on due to the availability of only captive specimens for genetic the island of New Guinea (NG), they were presumed to currently analysis and debate regarding their origin (3, 10, 11). Though exist only in captivity. This conclusion was based on the lack of genetically similar to the dingo, the NGSD represents a distinct sightings in the lowlands of the island and the concurrent expan- sion of European- and Asian-derived dogs. We have analyzed the population, as evidenced by both morphology and behavior (12). first nuclear genomes from a canid population discovered during a Resulting from a very small founder population, no more than 200 recent expedition to the highlands of NG. The extreme altitude to 300 captive NGSD remain alive today, largely bred for con- (>4,000 m) of the highland wild dogs’ (HWD) observed range servation purposes. Therefore, the population of free-roaming and confirmed vocalizations indicate their potential to be a wild HWD may not only represent a significant evolutionary unit im- GENETICS NGSD population. Comparison of single-nucleotide polymorphism portant for conservation and management but possibly an im- genotypes shows strong similarity between HWD and the homoge- portant link to understanding dog domestication (3). neous captive NGSD, with the HWD showing significantly higher genetic diversity. Admixture analyses and estimation of shared hap- Significance lotypes with phylogenetically diverse populations also indicates the HWD is a novel population within the distinct evolutionary lineage New Guinea singing dogs (NGSD) are distinctive among the of Oceanic canids. Taken together, these data indicate the HWD Canidae because of their unique and characteristic vocalization, possesses a distinct potential to aid in the conservation of NGSD isolated habitat, and status as a rare representative of wild both in the wild and under human care. dogs. Their scarcity, combined with the knowledge that none have been captured or exported since the late 1970s, supports canine | genetic | conservation | SNP | genome the hypothesis that NGSD are extinct in the wild. We have analyzed the nuclear genome of the first dogs captured from he New Guinea singing dog (NGSD) is a rare canid living in the highlands of Papua in approximately 50 y. We provide Tthe New Guinea highlands that, in the wild, is the largest land DNA-based evidence for an ancestral relationship between predator on the island of New Guinea. The dogs produce a highland wild dogs (HWD) and captive NGSD suggesting that characteristic harmonic vocalization (1), described as a “wolf the founding population of the NGSD is not, in fact, extinct and howl with overtones of whale song” (2). For years conservation that HWD should be resourced for conservation efforts to re- biologists have concluded that the NGSD may be extinct or build this unique canid population. nearing extinction in the wild due to loss of habitat and the encroachment of mainland breed dogs and village dogs (1, 3, 4). Author contributions: S.S., H.G.P., J.K.M., B.W.D., and E.A.O. conceptualized the study; H.G.P., J.K.M., B.W.D., and E.A.O. designed research; S.S., H.G.P., J.K.M., and B.W.D. per- In this context, nuclear DNA studies of highland wild dogs formed investigation; J.K.M., H.K.M., M.S., and M.P.-A. performed field work; S.S., J.K.M., (HWD) from New Guinea, so named based on their habitat H.K.M., L.N., B.W.D., and E.A.O. provided resources; H.G.P. curated data; H.G.P. analyzed combined with the initial observation of a “wild dog” on Mount data; S.S., J.K.M., A.S., D.Y.P.R., and E.A.O. supervised the project; S.S., A.S., D.Y.P.R., M.P.-A., Scratchley in 1897 (5), which share striking morphologic simi- and E.A.O. were responsible for project administration; H.G.P., J.K.M., K.M.C., and E.A.O. created visualization; and H.G.P., J.K.M., K.M.C., B.W.D., and E.A.O. wrote the paper with larity to both the NGSD and dingo, are of interest. However, assistance from M.S. because of their secretive nature and propensity to live at high Reviewers: K.K., Smithsonian Conservation Biology Institute; F.R., University of Copenha- altitudes distant from villages, HWD are rarely observed. In- gen; and R.D.S., University of Missouri. deed, prior to 2016 they were photographed only twice (1989 and Competing interest statement: E.A.O. is a coauthor with the dog10K Consortium on a 2012) (2, 6). Although there was a report of a population of 2019 review article; R.D.S. is a member of the consortium. J.K.M. heads and directs the New Guinea Highland Wild Dog Foundation, which funded the field work for the project. HWD in the HeLa Province of Papua New Guinea (PNG) in He personally was funded by PT Freeport Indonesia. 2009, it was based on several assumptions and no animals were This open access article is distributed under Creative Commons Attribution-NonCommercial- ever sighted (7). NoDerivatives License 4.0 (CC BY-NC-ND). The dogs of Oceania, unique populations found in Australia, 1S.S. and H.G.P. contributed equally to this work. New Zealand, and the islands nations of Melanesia, Micronesia, 2To whom correspondence may be addressed. Email: [email protected] or eostrand@ and Polynesia, originated from East Asian dog populations, with mail.nih.gov. archaeological evidence supporting their arrival at least 3.5 kya This article contains supporting information online at https://www.pnas.org/lookup/suppl/ (8). However, the dispersal timing of NGSD to New Guinea doi:10.1073/pnas.2007242117/-/DCSupplemental. remains uncertain due to lack of archaeological evidence found First published August 31, 2020. www.pnas.org/cgi/doi/10.1073/pnas.2007242117 PNAS | September 29, 2020 | vol. 117 | no. 39 | 24369–24376 Downloaded by guest on September 30, 2021 The need to study this presumably archaic lineage of dog is haplotype sharing with captive NGSDs and dingoes, but not with threefold. First, it is critical to determine if the captive NGSD any modern breed dogs. However, the background level of are from the same population as the HWD or, alternatively, if sharing with non-Asian breeds is significantly higher in the HWD the NGSD is truly extinct in the wild. Second, the primary aim of than in captive NGSD or dingoes (Wilcoxon P value < 2.2e-16) the NGSD Conservation Society (https://ngsdconservation.org/ (SI Appendix, Fig. S1). home/) is to maintain as much genetic variation within the We used the phased haplotypes to assign regions of the HWD population as possible. This is extremely challenging given the genome to the most similar group representing an ancestral limited gene pool of the captive NGSD which descend from only population using RFmix (Fig. 2). By assigning each allele to eight partially related founders (3, 13). If the existing HWD does exactly one of these representative populations based on hap- indeed represent the predecessor population of the famed lotype, we estimate that 72% of the HWD genome is most like NGSD, it is imperative that it be protected. Breeding programs captive NGSD or dingoes, the representative groups for Oceanic should be established to infuse what is expected to be compar- populations (Fig. 3A). This is in stark contrast to the village dogs atively robust genetics of the free-breeding HWD into the ge- of New Guinea which share 87% of their genome with breed netically compromised captive NGSD population, for which dogs and only 13% with the Oceanic dogs. An even weaker inbreeding coefficients have been estimated at >0.50 (14). Fi- Oceanic signature is evident in village dogs from Vietnam (11%) nally, truly wild populations of dogs are rare, including the dingo and Namibia (<1%). The Australian cattle dog, a historically and potentially the HWD, highlighting the need for rapid and hybrid breed population, shows 1.5% Oceanic dog heritage using well-organized conservation plans. the same metrics. The HWD is predicted to share only 28% of its In 2016, an expedition led by the New Guinea Highland Wild genome with breed dogs.