Hybridization and population genetics of two macaque species in Sulawesi, Indonesia

This study investigates hybridization and population genetics of two species of macaque monkey in Sulawesi, Indonesia, using molecular markers from mitochondrial, autosomal, and Y-chromosome DNA. Hybridization is the interbreeding of individuals from different parental taxa that are distinguishable by one or more heritable characteristics. Because hybridization can affect population structure of the parental taxa, it is an important consideration for conservation management. On the Indonesian island of Sulawesi an explosive diversification of macaques has occurred; seven of 19 species in the genus Macaca live on this island. The contact zone of the subjects of this study, M. maura and M. tonkeana, is located at the base of the southwestern peninsula of Sulawesi. Land conversion in Sulawesi is occurring at an alarming pace; currently two species of Sulawesi macaque, one of which is M. maura, are classified as endangered species. Results of this study indicate that hybridization among M. maura and M. tonkeana has led to different distributions of molecular variation in mitochondrial DNA and nuclear DNA in the contact zone; mitochondrial DNA shows a sharp transition from M. maura to M. tonkeana haplotypes, but nuclear DNA from the parental taxa is homogenized in a narrow hybrid zone. Similarly, within M. maura divergent mitochondrial DNA haplotypes are geographically structured but population subdivision in the nuclear genome is low or absent. In M. tonkeana, mitochondrial DNA haplotypes are geographically structured and a high level of nuclear DNA population subdivision is present in this species. These results are largely consistent with a macaque behavioral paradigm of female philopatry and obligate male dispersal, suggest that introgression between M. maura and M. tonkeana is restricted to the hybrid zone, and delineate one conservation management unit in M. maura and at least two in M. tonkeana.     

Origin of the Sulawesi macaques (Cercopithecidae: Macaco) as suggested by mitochondrial DNA phylogeny

One of the sharpest biogeographical transitions in the world occurs between the Indonesian islands of Borneo and Sulawesi; this transition is demarcated by Wallace's line. Macaque monkeys represent an interesting anomaly to faunal distributions in this region as they occur on both sides of Wallace's line, with Macacafascicularis, M. nemestrina and other species to the west and seven Sulawesi species to the east. We have investigated macaque evolution and dispersal in the Sunda region and Sulawesi using phylogenetic analysis of mitochondrial DNA sequences. Female philopatry of macaques, which causes sharp geographic clustering of maternally inherited mitochondrial DNA haplotypes, makes mitochondrial phytogenies particularly useful for investigating ancient patterns of dispersal. Results of this study suggest the following: (1) M. fascicularis is not a sister taxon to any species of Sulawesi macaque; (2) haplotypes of some M. nemestrina have a sister relationship to northern and central Sulawesi macaques, while haplotypes of other M. nemestrina have a sister relationship to soudiern Sulawesi macaques; (3) Sulawesi was probably colonized by macaques twice, once to the base of the northern peninsula now occupied by M. hecki and once to the southwestern peninsula now occupied by M, mama; and (4) within north/central and southern Sulawesi, patterns of dispersal are largely consistent with contemporary and past geography of the island, with the exception of a geographically discontinuous relationship between M. nigra and a portion of M. tonkeana from a region in northwest central Sulawesi.     

Discrimination of macaques by macaques: the case of Sulawesi species

A series of work by the first author have demonstrated that many macaque species show a visual preference for the pictures of their own species when the monkeys actively press a lever to see the pictures. We expanded this study to Sulawesi macaques kept as a pet by local people with slight modification. All seven species of Sulawesi macaques were passively exposed to a variety of colored slides of Sulawesi macaques. The experimenter recorded the duration of visual fixation onto the pictures. Male monkeys of all the seven species clearly watched the pictures of their own species for longer duration than those of the other species. Such visual preference suggested that the seven Sulawesi macaques discriminate each other species and, thus, they may not be integrated into fewer number of species. This visual preference may work to prevent overall intergradation of the Sulawesi macaques who sometimes have hybrid zones only in limited areas. This preference was in general weaker in female monkeys. In one species,Macaca ochreata, females actively avoided to see the pictures of conspecifics. These results may be related to how female monkeys interact with other individuals.     

Taxonomic revision of shrews of the genus Crociduras from the Sunda Shelf and Sulawesi with description of two new species (Mammalia: Soricidae)

The skulls of 387 shrews of the genus Crocidura sampled in peninsular Malaysia, Sumatra, Borneo, Java and Sulawesi were submitted to principal component and stepwise discriminant analyses. These analyses helped to delineate morphological taxa in this species-rich genus of mammals. Most morphologic groups could be attributed to described species, except one taxon from Sumatra and one from Sulawesi, which are described and named as new. Most of the 21 species recognized in this paper are endemic to one major island. Although Sulawesi has never been connected to the mainland, it supports at least six species, followed by Sumatra (5–6 species), Java and the Malay Peninsula (4 spp) and Borneo (3 spp). C. monticola is apparently the only widespread species whose distribution range covers the entire Malay Archipelago except the Philippines and Sulawesi. In contrast, the continental C. fuliginosa enters only marginally into the Sunda Shelf: its southernmost record is on the Malay Peninsula. This interpretation is completely different from the classical view that C. fuliginosa is a cosmopolitan species occupying the whole of Southeast Asia. Identification keys, tables of measurements and discriminant functions provided in this work may aid in identification of the various species and subspecies of Crocidura living in the Malaya Archipelago.     

Assessing natural introgression in 2 biomedical model species, the rhesus macaque (Macaca mulatta) and the long-tailed macaque (Macaca fascicularis)

Rhesus macaque (Macaca mulatta) and long-tailed macaque (Macaca fascicularis) are the 2 most commonly used primate model species in biomedical sciences. Although morphological studies have revealed a weak hybridization at the interspecific contact zone, in the north of Indochina, a molecular study has suggested an ancient introgression from rhesus to long-tailed macaque into the Indo-Chinese peninsula. However, the gene flow between these 2 taxa has never been quantified using genetic data and theoretical models. In this study, we have examined genetic variation within and between the parapatric Chinese rhesus macaque and Indo-Chinese long-tailed macaque populations, using 13 autosomal, 5 sex-linked microsatellite loci and mitochondrial DNA sequence data. From these data, we assessed genetic structure and estimated gene flow using a Bayesian clustering approach and the "Isolation with Migration" model. Our results reveal a weak interspecific genetic differentiation at both autosomal and sex-linked loci, suggesting large population sizes and/or gene flow between populations. According to the Bayesian clustering, Chinese rhesus macaque is a highly homogeneous gene pool that contributes strongly to the current Indo-Chinese long-tailed macaque genetic makeup, whether or not current admixture is assumed. Coalescent simulations, which integrated the characteristics of the loci, pointed out 1) a higher effective population size in rhesus macaque, 2) no mitochondrial gene flow, and 3) unilateral and male-mediated nuclear gene flow of approximately 10 migrants per generation from rhesus to long-tailed macaque. These patterns of genetic structure and gene flow suggest extensive ancient introgression from Chinese rhesus macaque into the Indo-Chinese long-tailed macaque population.     

The endemic seven: Four decades of research on the Sulawesi macaques

The oceanic island of Sulawesi, Indonesia, has long been of interest to scholars, including one of the leading evolutionary thinkers of the nineteenth century: Alfred Russell Wallace. During his explorations of the Malay archipelago, Wallace 1 was particularly struck with the ecology of Sulawesi (formally Celebes), noting the depauperate, yet distinctive nature of its fauna. It was home to members of both Asian and Australian faunas. Today, the asymmetrical four‐armed island of Sulawesi is regarded as the center of Wallacea, a unique biogeographical zone where endemism levels are incredibly high. 2 Of the 127 mammals indigenous to Indonesia, 79 (62%) are endemic to Sulawesi. Among these are seven species of the genus Macaca, 3 the most geographically widespread and ecologically diverse of nonhuman primate genera. In this paper, I trace the history and development of the major research trends on these endemic primates over the last four decades since Fooden's 3 landmark 1969 publication. These research trends include origin, speciation, and taxonomy; socioecology and behavior; ecology and conservation; and, most recently, the human‐macaque interface.     

Evidence of gene flow between Sulawesi macaques

A pilot field study was conducted in Sulawesi (Indonesia) to assess the status of macaque populations on the island. Wild and captive animals were sampled, mainly in border areas between presumed different species. The five species investigated were Macaca maurus, M. tonkeana, M. hecki, M. nigrescens, and M. nigra, for which morphological and gene frequency data suggested the presence of hybridization zones. Some individuals within these zones showed intermediate or mosaic morphology between parental forms. These individuals also had intermediate gene frequencies for most of the polymorphic systems investigated. Karyotypes were identical in all species, and no cytogenetic barrier to hybridization existed between species. A review of the recent literature also provided evidence for hybridization between Sulawesi macaques. Clinical frequencies in both morphological and biomolecular traits perhaps can be best explained by the operation of gene flow between the various forms of macaques on the island. However, additional data are necessary before current classification schemes are revised. The unique opportunity and need of further study of Sulawesi macaques for a range of evolutionary questions is emphasized.     

Detection of antibodies to selected human pathogens among wild and pet macaques (Macaca tonkeana) in Sulawesi, Indonesia.

Human-to-primate disease transmission can potentially cause significant morbidity and mortality among wild primate populations and thus constitutes an important conservation issue. Our cross-sectional study examines serological evidence of exposure to human pathogens among wild and pet macaques in Sulawesi. Serum samples taken from 11 pet and 15 wild macaques (Macaca tonkeana) were analyzed for antibodies to a panel of viruses commonly encountered in human populations. Antibodies to measles, influenza A, and parainfluenza 1 were detected in sera of both pet and wild macaques. Antibodies to parainfluenza 2 and 3 were found in the sera of wild macaques only. Possible routes of exposure, as well as implications for conservation are discussed.     

Biogeographic relationships of primates on South-East Asian islands

The number of primate species and genera on thirty-one south-east Asian islands west of the Wallace Line, including Sulawesi, is highly significantly related to surface area of the islands, as expected, but the z value (slope) of each relationship is low (0.21 for species). No association exists between number of taxa and distance to nearest mainland, or to nearest larger island. Excluding the non-Sunda Shelf islands only negligibly changes the relationships. A significant correlation exists between island size and median taxon's body mass, with taxa of 10 kg or more occurring on only the two largest islands. Hence, the primate community changes greatly with island size. The existence of several genera, but no congeners, on small islands, and a checkerboard distribution of the two nocturnal genera (Nycticebus and Tarsius), hints at interspecific competition as a cause of extinction. It is suggested that for comparative purposes, genera/area analyses might be more useful than species/area analyses, because genera are more taxonomically stable, perhaps more comparable across deeper taxa, and might be a better indication of degree of variability.     

Tree diversity and phytogeographical patterns of tropical high mountain rain forests in Central Sulawesi,Indonesia

Tropical high mountain forests in Lore Lindu National Park, Sulawesi, Indonesia, were described by their floristic composition and the importance of tree families (Family importance values, FIV), based on tree inventories conducted on 4 plots (each 0.24 ha) in old-growth forest stands at c. 1800 and 2400 m a.s.l. (mid- and upper montane elevations). To identify general patterns and regional peculiarities of the forests in the SE Asian and SW Pacific context, the biogeography of the tree species was analysed using distribution records. Out of the total of 87 tree species, only 18 species were found at both elevational zones. The discovery of new species and new distribution records (28% of the data set) highlights the deficiencies in the taxonomic and distribution data for Sulawesi. Sulawesi endemism rate was 20%. In the mid-montane Fagaceae–Myrtaceae forests, Lithocarpus spp. (Fagaceae) were overall important (4 spp. occupying around half of the total basal area) and the Myrtaceae the most species rich (8 spp.), thus showing typical features of Malesian montane forests. The upper montane conifer-Myrtaceae forest contained several high mountain tree taxa and showed affinity to the forests of New Guinea. The mountain flora comprised both eastern and western Malesian elements, with the nearest neighbouring islands Borneo and Maluku both sharing species with Sulawesi, reflecting the complex palaeogeography of the island. A separate analysis showed the mid-montane forest to possess greatest biogeographical affinity to Borneo/western Malesia, and the upper montane forest had a number of typical elements of Papuasia/eastern Malesia and the Phillipines, which may be a result of historical patterns in land connection and the emergence of mountain ranges.     

Resource partitioning in sympatric langurs and macaques in tropical rainforests of the central Western Ghats, south India

In a competitive sympatric association, coexisting species may try to reduce interspecific interactions as well as competition for similar resources by several ecological and behavioral practices. We studied resource utilization of three sympatric primate species namely, lion-tailed macaques (Macaca silenus), bonnet macaques (M. radiata) and Hanuman langurs (Semnopithecus entellus) in a tropical rainforest of the central Western Ghats, south India. We studied resource use, tree-height use, foraging height, substrate use when consuming animal prey and interspecific interactions. The results revealed that across the year, there was very limited niche overlap in diet between each species-pair. Each primate species largely depended on different plant species or different plant parts and phenophases from shared plant species. Primate species used different heights for foraging, and the two macaque species searched different substrates when foraging on animal prey. We also recorded season-wise resource abundance for the resources shared by these three primate species. While there was low dietary overlap during the dry season (a period of relatively low resource abundance), there was high dietary overlap between the two macaque species during the wet season (a period of high resource abundance for the shared resources). We observed only a few interspecific interactions. None of these were agonistic, even during the period of high niche overlap. This suggests that the sympatric primate species in this region are characterized by little or no contest competition. Unlike in some other regions of the Western Ghats, the lack of interspecific feeding competition appears to allow these primates, especially the macaques, to remain sympatric year-round.     

Agonistic screams differ among four species of macaques: the significance of motivation-structural rules

We compared screams of four species of macaques (rhesus monkey, Macaca mulatta; pigtailed monkey, M. nemestrina; Sulawesi crested black macaque, M. nigra; stumptailed macaque, M. arctoides) with respect to predictions of Morton's motivation-structural rules (Morton 1977, American Naturalist, 111, 855-869). We examined screams produced by victims of attack that involved contact aggression (pulling, pushing, slapping, grappling and biting) from a higher-ranking opponent. For each macaque species, we digitized 100 screams from females 3 years of age or older and measured acoustic features of each call. We used discriminant function analysis to determine whether the 400 vocalizations could be assigned to the correct caller species on the basis of their acoustic structure. Calls were assigned to the correct species at a significantly higher rate (93.5%) than expected by chance (25%). Each of the four macaque species used acoustically distinct screams in a shared context. While the differences in the macaque species' vocalizations suggest no simple correlation between immediate context and the acoustic forms of screams, there was general correspondence between the acoustic structure predicted by motivation-structural rules and inferences about the internal state of the vocalizer derived from the typical intensity of aggressive patterns that characterize each of the four species. Copyright 2000 The Association for the Study of Animal Behaviour.     

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

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.     

Hematological values and parasite fauna in free-rangingMacaca hecki and theM. hecki/M. tonkeana hybrid group of Sulawesi Island, Indonesia

Hematological values and parasitological fauna of free-rangingMacaca hecki and the hybrid group betweenM. hecki/M. tonkeana of Sulawesi Island, Indonesia, were investigated. The hematological values, especially the red cell number (RBC), were lower than those of other macaque species, indicating that Sulawesi macaques are slightly anemic. Several parasites including Plasmodium sp., trombiculid mites, andTrichuris trichiura were identified. Although infection by Plasmodium was observed with considerable frequency, no clear relationship between its infection and the occurrence of anemia was found. Trombiculid mites and eggs ofAnatrichosoma sp. were detected in foci of the ears of most monkeys. The infection with a trombiculid mite is the first recorded occurrence in free-ranging wild Sulawesi macaques. Gastrointestinal parasites were identified from their eggs in fecal samples, where five species of nematoda and one trematoda species were found.     

Diversification of Sulawesi macaque monkeys: decoupled evolution of mitochondrial and autosomal DNA

Abstract. In macaque monkeys, females are philopatric and males are obligate dispersers. This social system is expected to differently affect evolution of genetic elements depending on their mode of inheritance. Because of this, the geographic structure of molecular variation may differ considerably in mitochondrial DNA (mtDNA) and in autosomal DNA (aDNA) in the same individuals, even though these genomes are partially co-inherited. On the Indonesian island of Sulawesi, macaque monkeys underwent an explosive diversification as a result of range fragmentation. Today, barriers to dispersal have receded and fertile hybrid individuals can be found at contact zones between parapatric species. In this study, we examine the impact of range fragmentation on Sulawesi macaque mtDNA and aDNA by comparing evolution, phylogeography, and population subdivision of each genome. Our results suggest that mtDNA is paraphyletic in some species, and that mtDNA phylogeography is largely consistent with a pattern of isolation by distance. Autosomal DNA, however, is suggestive of fragmentation, in that interspecific differentiation across most contact zones is significant but intraspecific differentiation between contact zones is not. Furthermore, in mtDNA, most molecular variation is partitioned between populations within species but in aDNA most variation is partitioned within populations. That mtDNA has a different geographic structure than aDNA (and morphology) in these primates is a probable consequence of (1) a high level of ancestral polymorphism in mtDNA, (2) differences between patterns of ancestral dispersal of matrilines and contemporary dispersal of males, and (3) the fact that female philopatry impedes gene flow of macaque mtDNA.     

The borderlands and possible hybrids between three species of macaques,M. nigra,M. nigrescens,andM. hecki,in the northern peninsula of Sulawesi

The borderlands between three species of macaques,Macaca nigra, M. nigrescens, andM. hecki, which live on the northern peninsula of Sulawesi were surveyed mainly via observations of pet monkeys kept by local people. The borderlands between these species could be delineated. Some monkeys of peculiar appearance and/or with mixtures of the external characteristics of two species were found in the borderlands between the respective pairs of species. However, such possibly hybrid monkeys were seen or originated only in the very limited areas where the species might come into contact with each other.     

Monkeys and toads define areas of endemism on Sulawesi

Abstract.— Ecological or geological phenomena can impose limits on geographic diversification that cause biogeographical patterns of distantly related but sympatrically occurring taxa to be similar. Concordant patterns of diversity facilitate conservation management because strategic designation of protected areas can capture complementary rather than redundant components of variation. Here we demonstrate that on the biodiverse Indonesian island of Sulawesi, seemingly idiosyncratic distributions of diversity in endemic monkeys (Macaca species) and toads (Bufo celebensis) are actually virtually identical on a fine geographic scale. It appears that range fragmentation has generated seven multi-taxon areas of genetic endemism, each of which should be targeted for conservation. Joint consideration of molecular phylogeography, morphology, and demography helps resolve apparent contradictions in paraphyletic macaque mitochondrial DNA and in undifferentiated toad morphology, and facilitates an understanding of biogeography and conservation genetics of Sulawesi fauna.     

The flea genus Sigmactenus (Siphonaptera: Leptopsyllidae): three new taxa from Sulawesi, updated identification key, and distribution map for all known species and subspecies

One new species and two new subspecies of fleas are described. These are S. sulawesiensis n. sp. from North and Central Sulawesi, S. alticola pilosus n. ssp. from Central Sulawesi, and S. alticola crassinavis n. ssp. from North Sulawesi. All three of these new taxa are ectoparasites of native, endemic murine rodents. Two of the new taxa, S. sulawesiensis and S. alticola crassinavis, coexist on the same mountain, Gunung Moajat, in North Sulawesi. The related S. alticola alticola, which becomes the nominate subspecies, parasitises the murine rodent Maxomys alticola in northern Borneo (Sabah) and it is hypothesized that Sigmactenus first colonized Sulawesi as an ectoparasite of ancestral Maxomys, or perhaps Rattus, as these murines dispersed from southeast Asia to Sulawesi; 15 endemic murine rodent species belonging to these two genera are known to currently inhabit Sulawesi. An identification key and distribution map are included for all known species and subspecies of Sigmactenus. In addition to the three new taxa and S. a. alticola, these include: S. celebensis from South Sulawesi, S. timorensis from Timor, S. toxopeusi from New Guinea, and S. werneri from the Philippines (Mindanao and Negros).     

Neglected seed dispersers: endozoochory by Javan lutungs (Trachypithecus auratus) in Indonesia

Leaf monkeys are known to be leaf eaters, and thus, their potential role as seed dispersers has been neglected. However, they do also feed on fruits. To examine the role of leaf monkeys as endozoochorous seed dispersers, we studied the Javan lutung (Trachypithecus auratus) in Indonesia. We compared multiple aspects of seed dispersal processes (amount and diversity of seeds ingested, dispersal distance, and germination rate) of lutungs with that of the sympatric long‐tailed macaque (Macaca fascicularis). Over the study period, 54 percent of the lutung feces contained intact seeds, which was equivalent to the macaque feces contained seeds (62%). Seeds of at least six plant species were detected in the lutung feces, which was less than those found in the macaque feces (>19 plant species). The main species of seeds defecated by both lutungs and macaques was Ficus spp. (seed size: 0.7 mm). Seed shadow, estimated from travel distance (range: 1–299 m) and gut passage rate (24–96 h), had a unimodal‐distribution with a peak at 51–100 m, and was shorter than that reported in published accounts of macaques and other similar and smaller sized frugivores. Finally, germination rates of Ficus spp. seeds ingested by both lutungs and macaques were lower than that of the control seeds. These results imply that the dispersal effectiveness of lutungs would be lower than that of the sympatric primate frugivores. However, at a population level, lutungs could play a significant role as seed dispersers for the small‐seeded species, and therefore, more research into their frugivorous habits is warranted.