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, 448 (2), 242-9

Phylogeny of the Macaques (Cercopithecidae: Macaca) Based on Alu Elements

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Phylogeny of the Macaques (Cercopithecidae: Macaca) Based on Alu Elements

Jing Li et al. Gene.

Abstract

Genus Macaca (Cercopithecidae: Papionini) is one of the most successful primate radiations. Despite previous studies on morphology and mitochondrial DNA analysis, a number of issues regarding the details of macaque evolution remain unsolved. Alu elements are a class of non-autonomous retroposons belonging to short interspersed elements that are specific to the primate lineage. Because retroposon insertions show very little homoplasy, and because the ancestral state (absence of the SINE) is known, Alu elements are useful genetic markers and have been utilized for analyzing primate phylogenentic relationships and human population genetic relationships. Using PCR display methodology, 298 new Alu insertions have been identified from ten species of macaques. Together with 60 loci reported previously, a total of 358 loci are used to infer the phylogenetic relationships of genus Macaca. With regard to earlier unresolved issues on the macaque evolution, the topology of our tree suggests that: 1) genus Macaca contains four monophyletic species groups; 2) within the Asian macaques, the silenus group diverged first, and members of the sinica and fascicularis groups share a common ancestor; 3) Macaca arctoides are classified in the sinica group. Our results provide a robust molecular phylogeny for genus Macaca with stronger statistical support than previous studies. The present study also illustrates that SINE-based approaches are a powerful tool in primate phylogenetic studies and can be used to successfully resolve evolutionary relationships between taxa at scales from the ordinal level to closely related species within one genus.

Figures

Figure 1
Figure 1. PCR amplification analysis of Alu insertion polymorphisms in Macaca
Six gel electrophoresis results on Macaca species are shown with P. hamadryas as an outgroup. A: Amplification of locus Han1_b4, an Alu insertion specific to macaques. B: Amplification of locus Mni_d1t_60, an Alu insertion shared by all Asian macaques. C: Amplification of locus YRb2_13, an Alu insertion clustering the sinica group and the fascicularis group. D: Amplification of locus MS_b1_155, an Alu insertion specific to the silenus group. E: Amplification of locus MA_b1b_72, an Alu insertion specific to the sinica group. F. Amplification of locus MacYb5_25, an Alu insertion specific to the fascicularis group.
Figure 2
Figure 2. Macaque phylogenetic relationships derived from 358 Alu insertion polymorphisms
The amplification patterns of the Alu insertions were used to construct a dollo parsimony tree of macaque phylogenetic relationships using P. hamadryas as an outgroup and PAUP*4.0b10 program. The numbers above the branches indicate the percentage of bootstrap replicates (10,000 iterations) producing trees that including that node. The Numbers below the branches indicate the numbers of unambiguous insertions supporting each node. The numbers in red are insertions that are present in only one species. These loci are not parsimony informative. The significance level of each node is indicated by either * (P<0.05) or ** (P<0.001).
Figure 3
Figure 3. Potential confounding Alu insertions
Two examples of incongruent loci are shown. The upper part of the figure shows an adjacent independent insertion event occurring at locus MAb1_b_56. Picture (A) shows an agarose gel electrophoresis result with the final tree superimposed on the (B). Two arrows (red and blue) on the tree indicate Alu element insertion events. The two Alu elements independently insert in different lineages of macaque genomes. The integration sites are separated by 13-bp. The first AluY (red arrow) is shared by all macaque species; the second AluY (blue arrow) specifically inserted in M. arctoides genome. The bottom part of the figure shows an incomplete lineage sorting occurring at locus JH70. (C) is an agarose gel electrophoresis analysis of our macaque diversity panel. One Alu element is shared by members of sinica group and fascicularis group except for M. mulatta. (D) is the agarose gel electrophoresis result from four individual M. mulatta samples. It is polymorphic in the population of M. mulatta. ID 17573BRNY is the individual that was subjected to rhesus macaque reference genome (rheMac2).

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