Geographic isolation and elevational gradients promote diversification in an endemic shrew on Sulawesi
Graphical abstract
Introduction
Insular Southeast Asia holds an important place in the history of biogeography and indeed, in the history of evolutionary biology (Wallace, 1869, Wallace, 1876, Wallace, 1880). Early naturalists documented sharp zones of faunal turnover and remarkable levels of endemism (e.g., Huxley, 1868, Wallace, 1869, Dickerson, 1928, Taylor, 1934). Despite these early discoveries, the fauna of this megabiodiverse region remains poorly known in many respects, and modern expeditions frequently uncover new species of vertebrates, including mammals (e.g., Heaney et al., 2011, Heaney et al., 2014, Esselstyn et al., 2012, Esselstyn et al., 2013, Rowe et al., 2016). It is perhaps unsurprising then that the biogeographical factors that shaped the region’s current patterns of diversity and endemism remain incompletely understood (Lohman et al., 2011, Brown et al., 2013, Sheldon et al., 2015). Nevertheless, within-island diversification, facilitated by topographic complexity, is emerging as a significant contributor to the phylogenetic diversity of insular faunas (Heaney and Rickart, 1990, Heaney et al., 2011, Esselstyn et al., 2013, Hosner et al., 2013, Toussaint et al., 2014, Justiniano et al., 2015, Demos et al., 2016). Several studies have identified species endemic to single mountains or mountain ranges, with close relatives found in neighboring ranges (e.g., Heaney et al., 2011, Esselstyn et al., 2013, Justiniano et al., 2015). This suggests that unsuitable lowland habitats, competitive exclusion by closely related lowland species, or both represent long-term ecological barriers to dispersal for these taxa. Furthermore, elevational gradients on individual mountains may generate diversity if divergent natural selection promotes reproductive isolation and the formation of parapatric species. However, documented examples of this phenomenon are rare and often debatable (Caro et al., 2013, Demos et al., 2016).
The island of Sulawesi is large (11th largest globally), topographically complex (several mountains exceed 3000 m elevation), and shaped like a “K”, with its four peninsulas together comprising a greater land area than the island’s central core (Fig. 1). In addition, Sulawesi is a composite island, formed as no fewer than four (and perhaps seven or more) prehistoric landmasses collided between ∼25 and 2 Ma (Hall, 2002, Spakman and Hall, 2010, Hall, 2011). Moreover, because the individual landmasses constituting this proto-Sulawesi archipelago were divided further by periods of partial marine inundation (Whitten et al., 2002), the total number of prehistoric islands was even greater. As the centerpiece of the Wallacean biogeographic zone, Sulawesi has been colonized by faunal elements from up to three biologically diverse and distinctive areas: Sahul (Australia and New Guinea), Sunda (Borneo, Java, and Sumatra), and perhaps the Philippines (Stelbrink et al., 2012). Together, Sulawesi’s geographical characteristics and geological history provide numerous plausible mechanisms for generating high levels of species diversity and concordant phylogeographic patterns.
Early taxonomic work on Sulawesi’s vertebrate fauna showed that most species are endemic (e.g., Miller and Hollister, 1921a, Miller and Hollister, 1921b), but it was not until much later that biologists began to notice geographic patterns of endemism within the island. Fooden (1969) first noted that macaque hybrid zones correspond to natural geographic boundaries separating the peninsulas from the central core, and individual components of the north peninsula from each other. More recent genetic comparisons demonstrated that these boundaries are consistent for various lineages of amphibians, reptiles, and mammals, suggesting that genetic diversity in these lineages has been influenced by shared mechanisms (Evans et al., 2003a, Evans et al., 2003b, Evans et al., 2008, McGuire et al., 2007, Shekelle et al., 2010, Setiadi et al., 2011). These studies defined seven areas of endemism (AoEs; Fig. 1) on Sulawesi that correspond to the island’s central core, its east, southeast, and southwest peninsulas, and three areas on the north peninsula. However, some subsequent studies of Sulawesi taxa such as snails (von Rintelen et al., 2014), tarsiers (Driller et al., 2016), and bats (Campbell et al., 2007) have recorded geographic patterns only partially consistent with those observed in the monkeys and toads that defined Sulawesi’s original AoEs (Evans et al., 2003a). Evans (2012) reviewed available evidence and noted that in addition to the original AoE boundaries, several lineages are partitioned within the central core area, and the geographic position of these boundaries is shared by some lineages. Because AoEs on Sulawesi have been defined solely by shared phylogeographic patterns, the roles played by various plausible mechanisms (such as paleo-island geography, sea incursions, ecological barriers, and peninsular effects) in the formation of Sulawesi’s AoEs are not well understood. As such, the extent to which the AoE paradigm can be applied to the whole of Sulawesi’s biota remains unknown, and testing for the AoE pattern in additional organisms will help assess the importance of shared mechanisms of diversification, while also offering improved guidance to conservation efforts.
Whereas AoE patterns are inherently based on geographic distances, which have dominated discussions of within-island diversification on Sulawesi, elevational gradients provide potential alternative mechanisms of generating diversity and local endemism, as has been documented on other islands (e.g. Justiniano et al., 2015, Demos et al., 2016). Because studies that have investigated the AoE pattern on Sulawesi have not generally considered the elevational distribution of their focal lineage or its potential effect on geographic isolation and diversification, it is unclear whether elevational gradients serve as a cause of some reported AoE patterns of diversity, whether they act as an additional cause of diversification, or whether they have little influence on diversity and endemism.
Shrews of the genus Crocidura are represented on Sulawesi by six endemic species derived from two independent colonizations (Ruedi, 1995, Ruedi et al., 1998, Esselstyn et al., 2009). Among these shrews, Crocidura elongata offers a particularly promising opportunity to assess phylogeographic structure relative to AoE boundaries and along elevational gradients because it is widespread on the island, occurs from near sea level to the highest mountain areas that have been sampled, and its members are easily distinguished from other species by external characters (Ruedi, 1995). Here, we perform multi-locus population genetic, phylogenetic, and species delimitation analyses on C. elongata sampled from across Sulawesi to test if the species exhibits genetic structure associated with AoE boundaries, with elevational gradients, with both, or with neither.
Section snippets
Taxon sampling
Specimens of Crocidura elongata were collected from 15 sites contained in nine general localities. These localities are spread across Sulawesi and represent four of the island’s seven AoEs. Specimens are vouchered at the Field Museum of Natural History, Chicago (FMNH); Museum Victoria, Melbourne (NMV); Louisiana State University Museum of Natural Science, Baton Rouge (LSUMZ); Museum of Wildlife and Fish Biology, Davis (WFB); and Museum Zoologicum Bogoriense, Bogor (MZB). Our sampling includes
Alignment contents and sequence variation
All new DNA sequences were published as GenBank Accessions KY771329–KY772426 (Supplementary Appendix). Our cyt b alignment included 46 unique haplotypes from 75 individuals and was 1131 bases long with 25.6% missing data (841.5 bases sampled per individual). The concatenated alignment of all unphased nuclear loci was 9480 bases long with 18.8% missing data. Sequence lengths for phased nuclear loci were 450–793 bases, with the number of unique alleles ranging from 19 to 64 (Supplementary Table 4
Discussion and conclusions
Our analyses identified deep divergences (relative to those expected within a single species) among mitochondrial and multi-locus clades of Crocidura elongata, demonstrating that the current single-species classification obscures significant genetic structure in this taxon. Although our results were not entirely concordant, the analyses agreed in many respects. For instance, clusters identified in the Structure analyses (Fig. 4) generally corresponded to mitochondrial clades and, with a few
Acknowledgments
This work was funded by the National Science Foundation (DEB-1343517, DEB-1441634, and OISE-0965856) and National Geographic Society (9025-11). We thank Karen Rowe, James Patton, Carol Patton, Tri Haryoko, Heru Handika, Mardin Sarkam, and Alan Hitch for their contributions to specimen collection. We thank the Indonesian Ministry of Research and Technology (KEMENRISTEK), Lore Lindu National Park, and the BKSDA offices in Sulawesi Utara and Sulawesi Selatan for providing permits. The Field Museum
References (80)
- et al.
Contrasting patterns of genetic differentiation between endemic and widespread species of fruit bats (Chiroptera: Pteropodidae) in Sulawesi, Indonesia
Mol. Phylogenet. Evol.
(2007) Taxonomic revision of shrews of the genus Crocidura from the Sunda Shelf and Sulawesi with description of two new species (Mammalia: Soricidae)
Zool. J. Linn. Soc.
(1995)- et al.
Biogeography of Sulawesian shrews: testing for their origin with a parametric bootstrap on molecular data
Mol. Phylogenet. Evol.
(1998) - et al.
A comparison of Bayesian methods for haplotype reconstruction
Am. J. Hum. Genet.
(2003) - et al.
A new statistical method for haplotype reconstruction from population data
Am. J. Hum. Genet.
(2001) Comparison of Bayesian and maximum likelihood inference of population genetic parameters
Bioinformatics
(2006)- et al.
Maximum-likelihood estimation of migration rates and effective population numbers in two populations using a coalescent approach
Genetics
(1999) - et al.
Maximum likelihood estimation of a migration matrix and effective population sizes in n populations by using a coalescent approach
Proc. Natl. Acad. Sci. USA
(2001) - et al.
BEAST 2: a software platform for bayesian evolutionary analysis
PLoS Comput. Biol.
(2014) - et al.
Evolutionary processes of diversification in a model island archipelago
Annu. Rev. Ecol. Evol. Syst.
(2013)
Rapid evolution of animal mitochondrial DNA
Proc. Natl. Acad. Sci. USA
Ecological speciation along an elevational gradient in a tropical passerine bird?
J. Evol. Biol.
JModelTest 2: more models, new heuristics and parallel computing
Nat. Methods
Local endemism and within-island diversification of shrews illustrate the importance of speciation in building Sundaland mammal diversity
Mol. Ecol.
Distribution of Life in the Philippines
OrthoMaM v8: a database of orthologous exons and coding sequences for comparative genomics in mammals
Mol. Biol. Evol.
The ade4 package: implementing the duality diagram for ecologists
J. Stat. Softw.
Stop and go – waves of tarsier dispersal mirror the genesis of Sulawesi Island
PLoS ONE
Structure HARVESTER: a website and program for visualizing Structure output and implementing the Evanno method
Conserv. Genet. Resour.
MUSCLE: multiple sequence alignment with high accuracy and high throughput
Nucl. Acids Res.
Evolutionary novelty in a rat with no molars
Biol. Lett.
Carving out turf in a biodiversity hotspot: multiple unrecognized shrew species co–occur on Java Island, Indonesia
Mol. Ecol.
Do geological or climatic processes drive speciation in dynamic archipelagos? The tempo and mode of diversification in Southeast Asian shrews
Evolution
Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study
Mol. Ecol.
Coalescent-based analysis of demography: applications to biogeography on Sulawesi
Phylogenetics of fanged frogs: testing biogeographcial hypotheses at the interface of the Asian and Australian faunal zones
Syst. Biol.
Monkeys and toads define areas of endemism on Sulawesi
Evolution
A coalescent framework for comparing alternative models of population structure with genetic data: evolution of Celebes toads
Biol. Lett.
Inference of population structure: extensions to linked loci and correlated allele frequencies
Genetics
SeqPHASE: a web tool for interconverting PHASE input/output files and FASTA sequence alignments
Mol. Ecol. Resour.
Taxonomy and Evolution of the Monkeys of Celebes (Primates: Cercopithecidae)
A simple, fast and accurate method to estimate large phylogenies by maximum likelihood
Syst. Biol.
Cenozoic geological and plate tectonic evolution of SE Asian and the SW Pacific: computer–based reconstructions and animations
J. Asian Earth Sci.
Australia–SE Asia collision: plate tectonics and crustal flow
Geol. Soc. Lond. Spec. Publ.
Evolutionary history of endemic Sulawesi squirrels constructed from UCEs and mitogenomes sequenced from museum specimens
BMC Evol. Biol.
Seven new species and a new subgenus of forest mice (Rodentia: Muridae: Apomys) from Luzon Island, Fieldiana
Life Earth Sci.
Two new species of Philippine forest mice (Apomys, Muridae, Rodentia) from Lubang and Luzon Islands, with a redescription of Apomys sacobianus Johnson, 1962
Proc. Biol. Soc. Wash.
Correlations of clades and clines: geographic, elevational, and phylogenetic distribution patterns among Philippine mammals
Water barriers and intra-island isolation contribute to diversification in the insular Aethopyga sunbirds (Aves: Nectariniidae)
J. Biogeogr.
On the distribution of the Alectoromorphae and Heteromorphae
Proc. Zool. Soc. Lond.
Cited by (16)
Molecular phylogenetics and systematics of two enteric helminth parasites (Baylisascaris laevis and Diandrya vancouverensis) in the Vancouver Island marmot (Marmota vancouverensis)
2022, International Journal for Parasitology: Parasites and WildlifeCitation Excerpt :Island biogeography is a major driver of speciation, with geographically isolated ecosystems providing hotspots of endemism. The dynamic factors that promote speciation and persistence of insular endemics include neutral models of evolution as well as adaptation to habitat-specific selection pressures (Whitehead and Jones, 1969; Eldridge et al., 2018). Isolated populations can diverge over generations by chance fluctuation in allele frequencies when gene flow is interrupted.
Integrative methods reveal multiple drivers of diversification in rice paddy snakes
2024, Scientific ReportsEnvironment-dependent influence of fruit size upon the distribution of the Malesian archipelagic flora
2023, Plants People PlanetIntegrative Methods Reveal Multiple Drivers of Diversification in Rice Paddy Snakes
2023, Research Square
- 1
Present address: Department of Biology, Siena College, Loudonville, NY 12211, USA.