Stop and Go - Waves of Tarsier Dispersal Mirror the Genesis of Sulawesi Island

Abstract

The Indonesian island of Sulawesi harbors a highly endemic and diverse fauna sparking fascination since long before Wallace's contemplation of biogeographical patterns in the region. Allopatric diversification driven by geological or climatic processes has been identified as the main mechanism shaping present faunal distribution on the island. There is both consensus and conflict among range patterns of terrestrial species pointing to the different effects of vicariant events on once co-distributed taxa. Tarsiers, small nocturnal primates with possible evidence of an Eocene fossil record on the Asian mainland, are at present exclusively found in insular Southeast Asia. Sulawesi is hotspot of tarsier diversity, whereby island colonization and subsequent radiation of this old endemic primate lineage remained largely enigmatic. To resolve the phylogeographic history of Sulawesi tarsiers we analyzed an island-wide sample for a set of five approved autosomal phylogenetic markers (ABCA1, ADORA3, AXIN1, RAG1, and TTR) and the paternally inherited SRY gene. We constructed ML and Bayesian phylogenetic trees and estimated divergence times between tarsier populations. We found that their arrival at the Proto-Sulawesi archipelago coincided with initial Miocene tectonic uplift and hypothesize that tarsiers dispersed over the region in distinct waves. Intra-island diversification was spurred by land emergence and a rapid succession of glacial cycles during the Plio-Pleistocene. Some tarsier range boundaries concur with spatial limits in other taxa backing the notion of centers of faunal endemism on Sulawesi. This congruence, however, has partially been superimposed by taxon-specific dispersal patterns.

Fig 1. Informal maps of Sulawesi and tarsier phylogenetic trees.

A) Malay Archipelago and distribution of extant tarsiers. Dotted lines: Western (Wallace Line, WL) and eastern boundary (Lydekker Line, LL) of the Wallacea region. Dashed line: Sunda Arc. B) Main tectonic sutures on Sulawesi [1]. Arrows point to topographically significant regions. C) Species ranges of distinct lineages. White continuous lines: Macaque and toad hybrid zones, white dotted lines: Toad ranges deviating from the nearest macaque hybrid zone [4]; Continuous black lines: Distribution of tarsier acoustic forms [9, 17], thick black lines and circle indicate the discontinuous range of T. wallacei [17], in black dotted areas, tarsier species boundaries are yet to be determined; White dashed line: population differentiation in a Sulawesian bat species, Thoopterus nigrescens [5]. D) Study sites on Sulawesi indicated by white dots (2001–2008; BAT: Batusuya; KAM: Kamarora; KOJ: Koja; LAO: Laone; MAK: Make; PEA: Peana; UWE: Uwemanje), black dots (2009–2010; BAN: Bantimurung; DUA: Duasaudara; KEN: Kendari; KOR: Korosule; LAB: Labanu; LUW: Luwuk; OGA: Ogatemuku) and coloured squares. Squares mark sites where only tarsier vocalizations were recorded (blue: T. dentatus-like, red: T. lariang-like). Colored labels mark populations with taxonomic affiliation (see color key at the top right). E) Time-calibrated multilocus Bayesian species tree with posterior probabilities (pp) above 0.5 for internal nodes and 95% confidence intervals on divergence time estimates indicated by grey node bars. Lower case letters correspond to node names in Table 2. Arrows at the time-scale point to the Sundaland/Sula-Spur collision at 23 MYA [1] and significant sea-level lowstands at 10 and 2.5 MYA [19].

Fig 2. Species- and gene tree.

A) Multilocus Bayesian species tree. Numbers at nodes indicate posterior probability values above 0.5. B) Genealogy of ten SRY-haplotypes from 59 males. Node support values of Bayesian/maximum likelihood analyses above/below nodes represent posterior probabilities (pp) and bootstrap values (%), respectively. Numbers behind the population label/sampling site correspond to the number of males carrying the respective haplotype. Each terminal branch represents a distinct SRY haplotype.

Fig 3. SRY haplotype network.

Shown are the statistical parsimony network based on 10 SRY-haplotypes obtained from 59 males and haplotype distribution on Sulawesi. The white circle indicates an inferred missing haplotype. Mutation steps are shown as hatch marks.

Fig 4. Waves of dispersal and geographical distribution of Sulawesi tarsiers.

White and black arrows symbolize our proposed dispersal routes of the two lowland lineages on Sulawesi. The dotted pattern indicates a possible origin of the extant Sulawesi tarsier population that is unknown so far.