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, 7 (8), e43277

Eco-geographical Diversification of Bitter Taste Receptor Genes (TAS2Rs) Among Subspecies of Chimpanzees (Pan Troglodytes)

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Eco-geographical Diversification of Bitter Taste Receptor Genes (TAS2Rs) Among Subspecies of Chimpanzees (Pan Troglodytes)

Takashi Hayakawa et al. PLoS One.

Abstract

Chimpanzees (Pan troglodytes) have region-specific difference in dietary repertoires from East to West across tropical Africa. Such differences may result from different genetic backgrounds in addition to cultural variations. We analyzed the sequences of all bitter taste receptor genes (cTAS2Rs) in a total of 59 chimpanzees, including 4 putative subspecies. We identified genetic variations including single-nucleotide variations (SNVs), insertions and deletions (indels), gene-conversion variations, and copy-number variations (CNVs) in cTAS2Rs. Approximately two-thirds of all cTAS2R haplotypes in the amino acid sequence were unique to each subspecies. We analyzed the evolutionary backgrounds of natural selection behind such diversification. Our previous study concluded that diversification of cTAS2Rs in western chimpanzees (P. t. verus) may have resulted from balancing selection. In contrast, the present study found that purifying selection dominates as the evolutionary form of diversification of the so-called human cluster of cTAS2Rs in eastern chimpanzees (P. t. schweinfurthii) and that the other cTAS2Rs were under no obvious selection as a whole. Such marked diversification of cTAS2Rs with different evolutionary backgrounds among subspecies of chimpanzees probably reflects their subspecies-specific dietary repertoires.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. A large-deletion variant involving the whole-gene deletions of cTAS2R43, cTAS2R46, cTAS2R63P, and cTAS2R64.
(A) Genomic organization around the large-deletion region based on CGSC 2.1.3/panTro3. An electrophoresis image shows PCR products of each cTAS2R with subject ID numbers at the top. Only subject 156 did not produce amplicons of cTAS2R43, cTAS2R46, and cTAS2R64. In this subject, cTAS2R63P, IntA, and IntB were also not amplified, whereas IntC was amplified (data not shown). (B) Using intC_F and int31-63_R as a PCR primer pair, only subject 153 and 156 produced amplicons of the expected size of 4,760 bp based on CGSC 2.1.3/panTro3. Subjects 153 and 156 were thought to be a heterozygote and a homozygote for the large-deletion variant, respectively. The sequences around the breakpoints of the large-deletion variant had similar arrangements of retrotransposons (AluJr, L1MEg, and L1ME3B), which were annotated with RepeatMasker (http://www.repeatmasker.org).
Figure 2
Figure 2. The subspecies distribution of the number of haplotypes in the 28 cTAS2Rs.
(A, B) The distribution of all haplotypes in the 4 subspecies. (C, D) The distribution of high-frequency haplotypes in western and eastern chimpanzees. Subspecies of a Nigerian-Cameroonian chimpanzee was identified only maternally due to a lack of information about the antecedents in captivity. The number of non-functional haplotypes (segregating pseudogenes and whole-gene deletions) is indicated in parentheses. High-frequency haplotypes were observed in more than one sampled chromosome.
Figure 3
Figure 3. Median-joining networks for cTAS2Rs.
Circles represent haplotypes. Hapn indicates haplotype n (Table S1). The letter (P) is added to pseudogenes. Color within the circle indicates each subspecies. Areas and numbers within color-coded parts of the circles indicate the numbers of sampled chromosomes. Numbers along branches indicate nucleotide positions of mutation between the haplotypes. Line styles of branches indicate mutation types of nucleotide changes.
Figure 4
Figure 4. The histogram and cumulative frequency curve of F ST in SNVs in the 28 cTAS2Rs.
This plot was composed from a total of 174 SNVs in western and eastern chimpanzees. Sampled chromosomes carrying whole-gene deletions were omitted from the calculation. Mutation types and amino acid positions of SNVs with higher F ST are shown. Ancestral and derived amino acids were estimated from the haplotype networks. The protein locations are also shown based on Sugawara et al. (EC, extracellular region; TM, transmembrane region; IC, intracellular region).

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References

    1. Gonder MK, Oates JF, Disotell TR, Forstner MR, Morales JC, et al. (1997) A new west African chimpanzee subspecies? Nature 388: 337. - PubMed
    1. Groves CP (2001) Primate taxonomy. Washington, D.C.: Smithsonian Institution Press.
    1. Oates JF, Groves CP, Jenkins PD (2009) The type locality of Pan troglodytes vellerosus (Gray, 1862), and implications for the nomenclature of West African chimpanzees. Primates 50: 78–80. - PubMed
    1. Morin PA, Moore JJ, Chakraborty R, Jin L, Goodall J, et al. (1994) Kin selection, social structure, gene flow, and the evolution of chimpanzees. Science 265: 1193–1201. - PubMed
    1. Nishida T, Wrangham RW, Goodall J, Uehara S (1983) Local differences in plant-feeding habits of chimpanzees between the Mahale Mountains and Gombe National Park, Tanzania. J Hum Evol 12: 467–480.

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Grant support

This work was financially supported by Grants-in-Aid for Scientific Research (21370109, 22247036, 22247037, 22650053, 22770233, 24370096, 24405018, 244270, and Global COE Program A06) from the Ministry of Education, Culture, Sports, Science, and Technology of Japan, the Environment Research and Technology Development Fund (D-1007) from the Ministry of the Environment of Japan, and grants from the Inamori Foundation to YG and from the Takeda Foundation for Science and the Suzuken Memorial Foundation to HI. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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