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

Abstract

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 Macaca fmcicularis, 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 phylogenies particularly useful for investigating ancient patterns of dispersal. Results of this study suggest the following: (1) M. farcicularis 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 southern 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. maura; 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. n@a and a portion of M. tonkeana from a region in northwest central Sulawesi.

Sex-Linked Inheritance in Macaque Monkeys: Implications for Effective Population Size and Dispersal to Sulawesi

“…For these reasons, we also suspect that paraphyly of Sulawesi macaque mtDNA reported by Evans et al (1999) based on data from another region of the mtDNA is better attributed to homoplasy, as has been suggested (Deinard and Glen Smith 2001), than to recombination.…”

“…: A signal of recombination was detected in mtDNA of papionin monkeys (Piganeau et al 2004;Tsaousis et al 2005), including M. nemestrina (R. Setyadji, B. Suryobroto, T. Watanabe, and O. Takenaka, unpublished data; Evans et al 1999), Sulawesi macaques (Evans et al 1999), baboons (Newman et al 2004), and mandrills (Telfer et al 2003). After correction for multiple tests, one of four indirect tests for recombination used by Piganeau et al (2004) support recombination in the mtDNA data in this study from Borneo M. nemestrina (probability of the null hypothesis of no recombination (P no recomb ) ¼ 0.216, 0.015, 0.768, and .0.001 according to LDr 2 , LDD9, geneconv, and Max x 2 statistic tests).…”

“…These sex differences predict strong population subdivision of mtDNA with little or no subdivision of aDNA, deep mtDNA coalescence times, and frequent mtDNA paraphyly among species, and discordant genealogical rela- -N e of aDNA, xDNA, mtDNA, and yDNA as a function of (A) sex ratio skew and (B) the probability of female dispersal. In B, a finite island model of subdivided populations of constant size is assumed with a population size of 10,000 individuals, 10 subpopulations, and a male probability of migration equal to 0.1. tionships between mtDNA and yDNA-and this has been observed in multiple studies (Melnick and Pearl 1987;Melnick 1988;Melnick and Hoelzer 1992;Melnick et al 1993;Hoelzer et al 1994;Evans et al 1999Evans et al , 2001Evans et al , 2003Tosi et al 2000Tosi et al , 2002Tosi et al , 2003Newman et al 2004). Female philopatry and obligate male migration is a common social system in mammals (Greenwood 1980;Dobson 1982;Johnson 1986), though less so in humans (Seielstad et al 1998), and molecular variation provides an effective tool for exploring the impact of natural selection and demography on aDNA, the sex chromosomes, and mtDNA (Nachman 1997;Bachtrog and Charlesworth 2002;Stone et al 2002;Berlin and Ellegren 2004;Hellborg and Ellegren 2004;Wilder et al 2004;Hammer et al 2008).…”

Habitat Fragmentation and Biodiversity: Testing for the Evolutionary Effects of Refugia

“…However, our work on Chitaura grasshoppers in Sulawesi (Walton et al 1997;Bridle et al 2001) used divergence in different types of markers-morphology, color patterns, and mtDNA to locate the positions of two contact zones in northern Sulawesi, and compare their positions with those of macaques given by Evans et al (1999). These data revealed that, in contrast to the conclusion stated by Evans et al (2003;p.…”

“…This has been modeled by Irwin (2002) who showed that the sampling of such a marker can lead to erroneous inferences of past fragmentation. To avoid such artifacts, it is important to survey multiple marker loci or to examine concordance between genetic and phenotypic variation, as Evans et al (1999Evans et al ( , 2001) have done in their previous studies of macaques.…”