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. 2004 Dec;2(12):e442.
doi: 10.1371/journal.pbio.0020442. Epub 2004 Dec 7.

Phylogeography and genetic ancestry of tigers (Panthera tigris)

Shu-Jin Luo  1 , Jae-Heup Kim, Warren E Johnson, Joelle van der Walt, Janice Martenson, Naoya Yuhki, Dale G Miquelle, Olga Uphyrkina, John M Goodrich, Howard B Quigley, Ronald Tilson, Gerald Brady, Paolo Martelli, Vellayan Subramaniam, Charles McDougal, Sun Hean, Shi-Qiang Huang, Wenshi Pan, Ullas K Karanth, Melvin Sunquist, James L D Smith, Stephen J O'Brien
Affiliations

Phylogeography and genetic ancestry of tigers (Panthera tigris)

Shu-Jin Luo et al. PLoS Biol. 2004 Dec.

Abstract

Eight traditional subspecies of tiger (Panthera tigris),of which three recently became extinct, are commonly recognized on the basis of geographic isolation and morphological characteristics. To investigate the species' evolutionary history and to establish objective methods for subspecies recognition, voucher specimens of blood, skin, hair, and/or skin biopsies from 134 tigers with verified geographic origins or heritage across the whole distribution range were examined for three molecular markers: (1) 4.0 kb of mitochondrial DNA (mtDNA) sequence; (2) allele variation in the nuclear major histocompatibility complex class II DRB gene; and (3) composite nuclear microsatellite genotypes based on 30 loci. Relatively low genetic variation with mtDNA,DRB,and microsatellite loci was found, but significant population subdivision was nonetheless apparent among five living subspecies. In addition, a distinct partition of the Indochinese subspecies P. t. corbetti in to northern Indochinese and Malayan Peninsula populations was discovered. Population genetic structure would suggest recognition of six taxonomic units or subspecies: (1) Amur tiger P. t. altaica; (2) northern Indochinese tiger P. t. corbetti; (3) South China tiger P. t. amoyensis; (4) Malayan tiger P. t. jacksoni, named for the tiger conservationist Peter Jackson; (5) Sumatran tiger P. t. sumatrae; and (6) Bengal tiger P. t. tigris. The proposed South China tiger lineage is tentative due to limited sampling. The age of the most recent common ancestor for tiger mtDNA was estimated to be 72,000-108,000 y, relatively younger than some other Panthera species. A combination of population expansions, reduced gene flow, and genetic drift following the last genetic diminution, and the recent anthropogenic range contraction, have led to the distinct genetic partitions. These results provide an explicit basis for subspecies recognition and will lead to the improved management and conservation of these recently isolated but distinct geographic populations of tigers.

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Conflict of interest statement

The authors have declared that no conflicts of interests exist.

Figures

Figure 1
Figure 1. Historic and Current Geographic Distribution of Tigers Corresponding to the Eight Traditional Subspecies Designation
Geographic origin of samples and sample size (circles or squares) from each location are indicated (see Table 3 for sources). Three-letter codes (TIG, ALT, etc.) are indicated subspecies abbreviations. Dotted lines are approximate boundaries between tiger subspecies studied here. The Isthmus of Kra divides the traditional Indochinese tigers into the northern Indochinese tigers P. t. corbetti I and the Malayan tigers P. t. corbetti II based on the present study. We propose the Malayan tiger subspecies, COR II, be named P. t. jacksoni, to honor Peter Jackson, the former Chair of the IUCN's Cat Specialist Group who has contributed significantly to worldwide tiger conservation.
Figure 2
Figure 2. Schematic of P. tigris mtDNA
The position of PCR primers used for amplification of Cymt specific sequences and alignment of the homologous Numt sequence (outer, dashed line) in tiger mitochondria. Fifteen Cymt-specific primer sets spanning 6,026 bp of mtDNA were designed and screened for polymorphism in tigers (inner, solid line). Five indicated segments showed no variation among fifteen tigers that represented five traditional subspecies and therefore were excluded from further analysis. The ten variable segments (4,078 bp) were amplified in 100 tiger individuals. Primer sequences are listed in Table 1. Diamonds indicate polymorphic mtDNA segments; brackets indicate monomorphic mtDNA segments among tigers that were excluded from phylogenetic analysis.
Figure 3
Figure 3. Phylogenetic Relationships among Tigers from mtDNA Haplotypes
(A) Phylogenetic relationships based on MP among the tiger mtDNA haplotypes from the combined 4,078 bp mitochondrial sequence (Table 2). Branches of the same color represent haplotypes of the same subspecies. Trees derived from ME and ML analyses have identical topologies. Numbers above branches represent bootstrap support from 100 replicates using the MP method, followed by bootstrap values using the ME-ML analyses (only those over 70% are indicated). Numbers below branches show number of MP steps per number of homoplasies from a strict consensus tree. Numbers in parentheses represent numbers of individuals sharing the same haplotype. MP analysis using heuristic search and tree-bisection-reconnection branch-swapping approach results in two equally most-parsimonious trees and the one resembling the ME and ML trees is shown here (tree length = 60 steps; CI = 0.900). The ME tree is constructed with PAUP using Kimura two-parameter distances (transition to transversion ratio = 2) and NJ algorithm followed by branch-swapping procedure (ME = 0.0142). The ML approach is performed using a TrN (Tamura-Nei) +I (with proportion of invariable sites) model, and all nodes of the ML tree were significant (a consensus of 100 trees, –Ln likelihood = 5987.09). (B) Statistical parsimony network of tiger mtDNA haplotypes based on 4,078 mtDNA sequences constructed using the TCS program (Clement et al. 2000). The area of the circle is approximately proportional to the haplotype frequency, and the length of connecting lines is proportional to the exact nucleotide differences between haplotypes with each unit representing one nucleotide substitution. Missing haplotypes in the network are represented by dots. Haplotype codes and the number of individuals (in parentheses) with each haplotype are shown (see Table 2).
Figure 4
Figure 4. Phylogenetic Relationships among the Individual Tigers from Composite Microsatellite Genotypes of 30 Loci
Branches of the same color represent tiger individuals of the same subspecies. The NJ tree, which is based on Dps and Dkf with the (1 – ps/kf) option in MICROSAT (Minch et al. 1995), generated similar topologies, and only the Dps tree is shown here. Numbers are individual Pti codes (Table 3). Bootstrap values over 50% are shown on the divergence node.
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