Strong and stable geographic differentiation of swamp buffalo maternal and paternal lineages indicates domestication in the China/Indochina border region

Abstract

The swamp type of the Asian water buffalo is assumed to have been domesticated by about 4000 years BP, following the introduction of rice cultivation. Previous localizations of the domestication site were based on mitochondrial DNA (mtDNA) variation within China, accounting only for the maternal lineage. We carried out a comprehensive sampling of China, Taiwan, Vietnam, Laos, Thailand, Nepal and Bangladesh and sequenced the mtDNA Cytochrome b gene and control region and the Y-chromosomal ZFY, SRY and DBY sequences. Swamp buffalo has a higher diversity of both maternal and paternal lineages than river buffalo, with also a remarkable contrast between a weak phylogeographic structure of river buffalo and a strong geographic differentiation of swamp buffalo. The highest diversity of the swamp buffalo maternal lineages was found in south China and north Indochina on both banks of the Mekong River, while the highest diversity in paternal lineages was in the China/Indochina border region. We propose that domestication in this region was later followed by introgressive capture of wild cows west of the Mekong. Migration to the north followed the Yangtze valley as well as a more eastern route, but also involved translocations of both cows and bulls over large distances with a minor influence of river buffaloes in recent decades. Bayesian analyses of various migration models also supported domestication in the China/Indochina border region. Coalescence analysis yielded consistent estimates for the expansion of the major swamp buffalo haplogroups with a credibility interval of 900 to 3900 years BP. The spatial differentiation of mtDNA and Y-chromosomal haplotype distributions indicates a lack of gene flow between established populations that is unprecedented in livestock.

Whole Mitogenomes Reveal the History of Swamp Buffalo: Initially Shaped by Glacial Periods and Eventually Modelled by Domestication

“…The remaining 87 swamp buffalo haplotypes cluster into five divergent haplogroups (Hg.s), namely SA, SB, SC, SD and SE, with an overwhelming representation of SA (54.1%) and SB (40.4%). We largely confirm previous phylogenies 6, 10 , but also reveal the novel haplogroups SA3 and SB4 and many different subhaplogroups. Lineages SA and SB are divided into three (SA1 to SA3; SA1′2 as an ancestral node) and four (SB1-SB4; SB2′3′4 as an ancestral node) sublineages, respectively.…”

“…An analysis of the geographic distribution of swamp haplogroups in Southeast Asia, based on the control-region data currently available in previous literature 6 or deposited in GenBank (Supplementary Table S1) confirms the prevalence of SA or SB mtDNAs (>99%) and a geographic differentiation of subhaplogroups with contrasting geographic distributions of the subhaplogroups SA2, SB1, SB2 and SB3 (Supplementary Fig. S5).…”

“…S5). The rare haplogroup SC was previously reported to occur in Thailand, Bangladesh and sporadically in Southwest China, while SD and SE were found only in Thailand 6 . We confirmed the presence of SC in the Southwestern Chinese Dehong population, but the haplotypes SC and SE were also found in the Yibin and Poyanghu breeds from the Yangtze Valley (inset in Fig.…”

“…The remaining 5 haplotypes belong to the rare haplogroups SC (2), SD (2) or SE (1). The two river buffalo mitogenomes belong to clades R1 and R2 1, 6 .…”

“…Domestication of river buffalo most likely took place in the Indian subcontinent 15 , whereas swamp buffalo was proposed to originate from the border region between south China and north Indochina 6, 17 . However, the fragmentary buffalo mtDNA sequences from rDNA, COII, and cytochrome b loci reported to date 5–7, 18 , confound quantitative inferences of population history.…”