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  1. Wells K, Lakim MB, Beaucournu JC
    Med Vet Entomol, 2011 Sep;25(3):311-9.
    PMID: 21219372 DOI: 10.1111/j.1365-2915.2010.00940.x
    The diversity of ectoparasites in Southeast Asia and flea-host associations remain largely understudied. We explore specialization and interaction patterns of fleas infesting non-volant small mammals in Bornean rainforests, using material from a field survey carried out in two montane localities in northwestern Borneo (Sabah, Malaysia) and from a literature database of all available interactions in both lowland and montane forests. A total of 234 flea individuals collected during our field survey resulted in an interaction network of eight flea species on seven live-captured small mammal species. The interaction network from all compiled studies currently includes 15 flea species and 16 small mammal species. Host specificity and niche partitioning of fleas infesting diurnal treeshrews and squirrels were low, with little difference in specialization among taxa, but host specificity in lowland forests was found to be higher than in montane forests. By contrast, Sigmactenus alticola (Siphonaptera: Leptopsyllidae) exhibited low host specificity by infesting various montane and lowland nocturnal rats. However, this species exhibited low niche partitioning as it was the only commonly recorded flea from rats on Borneo. Overall complementary specialization was of intermediate intensity for both networks and differed significantly from random association; this has important implications for specific interactions that are also relevant to the potential spread of vector-borne diseases.
  2. Vun VF, Mahani MC, Lakim M, Ampeng A, Md-Zain BM
    Genet. Mol. Res., 2011;10(1):368-81.
    PMID: 21365553 DOI: 10.4238/vol10-1gmr1048
    Little is known about the classification and phylogenetic relationships of the leaf monkeys (Presbytis). We analyzed mitochondrial DNA sequences of cytochrome b (Cyt b) and 12S rRNA to determine the phylogenetic relationships of the genus Presbytis. Gene fragments of 388 and 371 bp of Cyt b and 12S rRNA, respectively, were sequenced from samples of Presbytis melalophos (subspecies femoralis, siamensis, robinsoni, and chrysomelas), P. rubicunda and P. hosei. The genus Trachypithecus (Cercopithecidae) was used as an outgroup. The Cyt b NJ and MP phylogeny trees showed P. m. chrysomelas to be the most primitive, followed by P. hosei, whereas 12S rRNA tree topology only indicated that these two species have close relationships with the other members of the genus. In our analysis, chrysomelas, previously classified as a subspecies of P. melalophos, was not included in either the P. m. femoralis clade or the P. m. siamensis clade. Whether or not there should be a separation at the species level remains to be clarified. The tree topologies also showed that P. m. siamensis is paraphyletic with P. m. robinsoni, and P. m. femoralis with P. rubicunda, in two different clades. Cyt b and 12S rRNA are good gene candidates for the study of phylogenetic relationships at the species level. However, the systematic relationships of some subspecies in this genus remain unclear.
  3. Md-Zain BM, Mohamad M, Ernie-Muneerah MA, Ampeng A, Jasmi A, Lakim M, et al.
    Genet. Mol. Res., 2010;9(4):1987-96.
    PMID: 20927717 DOI: 10.4238/vol9-4gmr942
    Mitochondrial DNA cytochrome c oxidase II (COII) gene sequences of Malaysian Cercopithecidae were examined to ascertain their phylogenetic relationships. Colobinae were represented by the genera Presbytis, Trachypithecus and Nasalis, while the genus Macaca represented Cercopithecinae. DNA amplification and sequencing of the COII gene was performed on 16 samples. Symphalangus syndactylus (Hylobatidae) was used as the outgroup. Data were analyzed using both character (maximum parsimony) and distance (neighbor-joining) methods. Tree topologies indicated that Colobinae and Cercopithecinae have their own distinct monophyletic clade. This result was well supported by bootstrap values and genetic distances derived from the Kimura-2-parameter algorithm. Separation of Macaca nemestrina from M. fascicularis was also well supported by bootstrap values. In addition, tree topologies indicate a good resolution of the Colobinae phylogenetic relationships at the intergeneric level, but with low bootstrap support. The position of Nasalis remained problematic in both trees. Overall, COII is a good gene candidate for portraying the phylogenetic relationships of Malaysian primates at the inter- and intra-subfamily levels.
  4. Moyle RG, Manthey JD, Hosner PA, Rahman M, Lakim M, Sheldon FH
    PeerJ, 2017;5:e3335.
    PMID: 28533979 DOI: 10.7717/peerj.3335
    Topographically complex regions often contain the close juxtaposition of closely related species along elevational gradients. The evolutionary causes of these elevational replacements, and thus the origin and maintenance of a large portion of species diversity along elevational gradients, are usually unclear because ecological differentiation along a gradient or secondary contact following allopatric diversification can produce the same pattern. We used reduced representation genomic sequencing to assess genetic relationships and gene flow between three parapatric pairs of closely related songbird taxa (Arachnothera spiderhunters, Chloropsis leafbirds, and Enicurus forktails) along an elevational gradient in Borneo. Each taxon pair presents a different elevational range distribution across the island, yet results were uniform: little or no gene flow was detected in any pairwise comparisons. These results are congruent with an allopatric "species-pump" model for generation of species diversity and elevational parapatry of congeners on Borneo, rather than in situ generation of species by "ecological speciation" along an elevational gradient.
  5. Chua VL, Smith BT, Burner RC, Rahman MA, Lakim M, Prawiradilaga DM, et al.
    Mol Phylogenet Evol, 2017 Aug;113:139-149.
    PMID: 28545973 DOI: 10.1016/j.ympev.2017.05.016
    The mountains of Borneo are well known for their high endemicity and historical role in preserving Southeast Asian rainforest biodiversity, but the diversification of populations inhabiting these mountains is poorly studied. Here we examine the genetic structure of 12 Bornean montane passerines by comparing complete mtDNA ND2 gene sequences of populations spanning the island. Maximum likelihood and Bayesian phylogenetic trees and haplotype networks are examined for common patterns that might signal important historical events or boundaries to dispersal. Morphological and ecological characteristics of each species are also examined using phylogenetic generalized least-squares (PGLS) for correlation with population structure. Populations in only four of the 12 species are subdivided into distinct clades or haplotype groups. Although this subdivision occurred at about the same time in each species (ca. 0.6-0.7Ma), the spatial positioning of the genetic break differs among the species. In two species, northeastern populations are genetically divergent from populations elsewhere on the island. In the other two species, populations in the main Bornean mountain chain, including the northeast, are distinct from those on two isolated peaks in northwestern Borneo. We suggest different historical forces played a role in shaping these two distributions, despite commonality in timing. PGLS analysis showed that only a single characteristic-hand-wing index-is correlated with population structure. Birds with longer wings, and hence potentially more dispersal power, have less population structure. To understand historical forces influencing montane population structure on Borneo, future studies must compare populations across the entirety of Sundaland.
  6. Abdul-Latiff MA, Ruslin F, Fui VV, Abu MH, Rovie-Ryan JJ, Abdul-Patah P, et al.
    Zookeys, 2014.
    PMID: 24899832 DOI: 10.3897/zookeys.407.6982
    Phylogenetic relationships among Malaysia's long-tailed macaques have yet to be established, despite abundant genetic studies of the species worldwide. The aims of this study are to examine the phylogenetic relationships of Macaca fascicularis in Malaysia and to test its classification as a morphological subspecies. A total of 25 genetic samples of M. fascicularis yielding 383 bp of Cytochrome b (Cyt b) sequences were used in phylogenetic analysis along with one sample each of M. nemestrina and M. arctoides used as outgroups. Sequence character analysis reveals that Cyt b locus is a highly conserved region with only 23% parsimony informative character detected among ingroups. Further analysis indicates a clear separation between populations originating from different regions; the Malay Peninsula versus Borneo Insular, the East Coast versus West Coast of the Malay Peninsula, and the island versus mainland Malay Peninsula populations. Phylogenetic trees (NJ, MP and Bayesian) portray a consistent clustering paradigm as Borneo's population was distinguished from Peninsula's population (99% and 100% bootstrap value in NJ and MP respectively and 1.00 posterior probability in Bayesian trees). The East coast population was separated from other Peninsula populations (64% in NJ, 66% in MP and 0.53 posterior probability in Bayesian). West coast populations were divided into 2 clades: the North-South (47%/54% in NJ, 26/26% in MP and 1.00/0.80 posterior probability in Bayesian) and Island-Mainland (93% in NJ, 90% in MP and 1.00 posterior probability in Bayesian). The results confirm the previous morphological assignment of 2 subspecies, M. f. fascicularis and M. f. argentimembris, in the Malay Peninsula. These populations should be treated as separate genetic entities in order to conserve the genetic diversity of Malaysia's M. fascicularis. These findings are crucial in aiding the conservation management and translocation process of M. fascicularis populations in Malaysia.
  7. Liedigk R, Kolleck J, Böker KO, Meijaard E, Md-Zain BM, Abdul-Latiff MA, et al.
    BMC Genomics, 2015 Mar 21;16:222.
    PMID: 25887664 DOI: 10.1186/s12864-015-1437-0
    BACKGROUND: Long-tailed macaques (Macaca fascicularis) are an important model species in biomedical research and reliable knowledge about their evolutionary history is essential for biomedical inferences. Ten subspecies have been recognized, of which most are restricted to small islands of Southeast Asia. In contrast, the common long-tailed macaque (M. f. fascicularis) is distributed over large parts of the Southeast Asian mainland and the Sundaland region. To shed more light on the phylogeny of M. f. fascicularis, we sequenced complete mitochondrial (mtDNA) genomes of 40 individuals from all over the taxon's range, either by classical PCR-amplification and Sanger sequencing or by DNA-capture and high-throughput sequencing.

    RESULTS: Both laboratory approaches yielded complete mtDNA genomes from M. f. fascicularis with high accuracy and/or coverage. According to our phylogenetic reconstructions, M. f. fascicularis initially diverged into two clades 1.70 million years ago (Ma), with one including haplotypes from mainland Southeast Asia, the Malay Peninsula and North Sumatra (Clade A) and the other, haplotypes from the islands of Bangka, Java, Borneo, Timor, and the Philippines (Clade B). The three geographical populations of Clade A appear as paraphyletic groups, while local populations of Clade B form monophyletic clades with the exception of a Philippine individual which is nested within the Borneo clade. Further, in Clade B the branching pattern among main clades/lineages remains largely unresolved, most likely due to their relatively rapid diversification 0.93-0.84 Ma.

    CONCLUSIONS: Both laboratory methods have proven to be powerful to generate complete mtDNA genome data with similarly high accuracy, with the DNA-capture and high-throughput sequencing approach as the most promising and only practical option to obtain such data from highly degraded DNA, in time and with relatively low costs. The application of complete mtDNA genomes yields new insights into the evolutionary history of M. f. fascicularis by providing a more robust phylogeny and more reliable divergence age estimations than earlier studies.

  8. Merckx VS, Hendriks KP, Beentjes KK, Mennes CB, Becking LE, Peijnenburg KT, et al.
    Nature, 2015 Aug 20;524(7565):347-50.
    PMID: 26266979 DOI: 10.1038/nature14949
    Tropical mountains are hot spots of biodiversity and endemism, but the evolutionary origins of their unique biotas are poorly understood. In varying degrees, local and regional extinction, long-distance colonization, and local recruitment may all contribute to the exceptional character of these communities. Also, it is debated whether mountain endemics mostly originate from local lowland taxa, or from lineages that reach the mountain by long-range dispersal from cool localities elsewhere. Here we investigate the evolutionary routes to endemism by sampling an entire tropical mountain biota on the 4,095-metre-high Mount Kinabalu in Sabah, East Malaysia. We discover that most of its unique biodiversity is younger than the mountain itself (6 million years), and comprises a mix of immigrant pre-adapted lineages and descendants from local lowland ancestors, although substantial shifts from lower to higher vegetation zones in this latter group were rare. These insights could improve forecasts of the likelihood of extinction and 'evolutionary rescue' in montane biodiversity hot spots under climate change scenarios.
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