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. 2020 Mar 26;15(3):e0230014.
doi: 10.1371/journal.pone.0230014. eCollection 2020.

Identifying Genetic Relationships Among Tarsier Populations in the Islands of Bunaken National Park and Mainland Sulawesi

Free PMC article

Identifying Genetic Relationships Among Tarsier Populations in the Islands of Bunaken National Park and Mainland Sulawesi

Thalita Christiani Pingkan Sumampow et al. PLoS One. .
Free PMC article


Eastern tarsiers (Tarsius tarsier complex) are small nocturnal primates endemic to Sulawesi Island and small adjacent islands of Indonesia. In 2004, the hybrid biogeography hypothesis predicted this species complex might contain 16 or more taxa, each corresponding to a region of endemism, based on: 1) geological evidence of the development of the archipelago, 2) biological evidence in the form of concordant distributions of monkeys and toads, and 3) the distribution of tarsier acoustic groups. Since then, 11 tarsier species have been recognized, potentially leaving more to be described. Efforts to identify these cryptic species are urgently needed so that habitat conversion, pet trade, and cultural activities will not render some species extinct before they are recognized. We gathered data to test the hypothesis of cryptic tarsier species on three volcanic islands in Bunaken National Park, North Sulawesi, namely Bunaken, Manadotua, and Mantehage, during May-August 2018. We sequenced individuals at 5 nuclear genes (ABCA1, ADORA3, AXIN1, RAG, and TTR) and made comparisons to existing genotypes at 14 mainland sites. Bayesian phylogenetic analyses revealed that island populations are genetically identical in all 5 genes, and formed a clade separated from the mainland ones. The eastern tarsiers first diverged from the western tarsiers approximately 2.5 MYA. The three island populations diverged from mainland tarsiers approximately 2,000-150,000 YA, due to either human activities or natural rafting. This study provides information for tarsier conservation, advances the understanding of biogeography of Sulawesi, and contributes to Indonesian awareness of biodiversity. Further quantitative genetics research on tarsiers, especially the island populations, will offer significant insights to establish more efficient and strategic tarsier conservation actions.

Conflict of interest statement

The authors have declared that no competing interests exist.


Fig 1
Fig 1. The maps of Sulawesi and parts of North Sulawesi.
A) Sulawesi, the fourth largest island in Indonesia, hosts many endemic animals. The “hybrid biogeography hypothesis” (Shekelle and Leksono, 2004) suggests that there are at least 16 subregions of tarsier endemism throughout the island. B) Grand forest park Gunung Tumpa (blue circle), Duasudara Nature Reserve (green circle), and three islands in TNB: Bunaken (red circle), Manadotua (orange circle), Mantehage (yellow circle).
Fig 2
Fig 2. Bathymetry map of northern Sulawesi archipelago (from Shekelle and Salim, 2009).
The islands of Bunaken National Park (TNB) are in red box.
Fig 3
Fig 3. The approximate locations of tarsier sleeping sites on the study sites.
A) Bunaken, B) Manadotua, and C) Mantehage.
Fig 4
Fig 4. Origins of DNA sample from 17 populations of eastern tarsier.
Stars: this study (red: Bunaken; orange: Manadotua; yellow: Mantehage; see Fig 1). Black dots: Driller et al. (2015).
Fig 5
Fig 5. Multilocus Bayesian species tree.
Northern and southeastern Sulawesi populations are highlighted in red. (A) full tree; (B) distribution map of 17 populations of eastern tarsier; (C) detail view of the red box in the upper panel.
Fig 6
Fig 6. Time-calibrated multilocus Bayesian tree.
Numbers above nodes are posterior probability (pp) and 95% confidence intervals are indicated with purple bars. Lowercase letters indicate nodes’ names (see Table 3). Study populations are yellow highlighted.

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Grant support

TS received grants from USAID, Brad McRae Fellowship, NAU Landscape Conservation Initiative, and International Primatological Society. Participation by MS was facilitated by a grant from the Margot Marsh Biodiversity Foundation and a private donation by the Tjiasmanto Family. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.