Asian water buffalo: domestication,history and genetics

The domestic Asian water buffalo (Bubalus bubalis) is found on all five continents, with a global population of some 202 million. The livelihoods of more people depend on this species than on any other domestic animal. The two distinct types (river and swamp) descended from different wild Asian water buffalo (Bubalus arnee) populations that diverged some 900 kyr BP and then evolved in separate geographical regions. After domestication in the western region of the Indian subcontinent (ca. 6300 years BP), the river buffalo spread west as far as Egypt, the Balkans and Italy. Conversely, after domestication in the China/Indochina border region ca. 3000–7000 years BP, swamp buffaloes dispersed through south-east Asia and China as far as the Yangtze River valley. Molecular and morphological evidence indicates that swamp buffalo populations have strong geographic genetic differentiation and a lack of gene flow, but strong phenotypic uniformity. In contrast, river buffalo populations show a weaker phylogeographic structure, but higher phenotypic diversity (i.e. many breeds). The recent availability of a high-quality reference genome and of a medium-density marker panel for genotyping has triggered a number of genome-wide investigations on diversity, evolutionary history, production traits and functional elements. The growing molecular knowledge combined with breeding programmes should pave the way to improvements in production, environmental adaptation and disease resistance in water buffalo populations worldwide.     

Mitochondrial DNA diversity patterns in Pakistani buffalo

The Indian subcontinent is considered to be the likely centre of river buffalo domestication, based on population dynamics, archaeological evidence and genetic diversity. Recent studies on mitochondrial DNA diversity have drawn useful conclusions about the domestication history of Bubalus bubalis. The conclusions of these studies are, however, incomplete, unless samples can also be analysed from Pakistan, which contains the second largest buffalo population of the world. Here, we report the results of the first study on mitochondrial D-loop sequence diversity in five breeds of Pakistani buffalo. Analysis of sequence variations in 503-bp of the D-loop region of 123 animals revealed 52 haplotypes, including 40 singletons. Multidimensional display of breed pairwise F(ST) values revealed no strong clustering of breeds. Bayesian, maximum parsimony, neighbour joining and UPGMA trees revealed a topology consistent with domestication as well as subsequent introgression of multiple maternal lineages from the wild stocks. Reduced median network analysis provided evidence of population expansion from more than one set of haplotypes. The study also confirmed that Pakistani buffalo are of the river type. The observed mitochondrial D-loop sequence diversity suggests that Pakistani areas bordering India might have contributed to the initiation of domestication of the present-day river buffalo.     

Mitochondrial DNA analyses of Indian water buffalo support a distinct genetic origin of river and swamp buffalo

Water buffalo (Bubalus bubalis) is broadly classified into river and swamp categories, but it remains disputed whether these two types were independently domesticated, or if they are the result of a single domestication event. In this study, we sequenced the mitochondrial D-loop region and cytochrome b gene of 217 and 80 buffalo respectively from eight breeds/locations in northern, north-western, central and southern India and compared our results with published Mediterranean and swamp buffalo sequences. Using these data, river and swamp buffalo were distinguished into two distinct clades. Based upon the existing knowledge of cytogenetic, ecological and phenotypic parameters, molecular data and present-day distribution of the river and swamp buffalo, we suggest that these two types were domesticated independently, and that classification of the river and swamp buffalo as two related subspecies is more appropriate.     

Genetic characterization of the Indian cattle breeds,Ongole and Deoni (<Emphasis Type="Italic">Bos indicus</Emphasis>), using microsatellite markers – a preliminary study

Background  

Molecular characterization of cattle breeds is important for the prevention of germplasm erosion by cross breeding. The Indian zebu cattle have their significant role in evolution of present day cattle breeds and development of some of the exotic breeds. Microsatellites are the best available molecular tools for characterization of cattle breeds. The present study was carried out to characterize two Indian cattle breeds, Ongole and Deoni, using microsatellite markers.     

Mitochondrial sequence-based evolutionary analysis of riverine–swamp hybrid buffaloes of India indicates novel maternal differentiation and domestication patterns

In this study, mitochondrial D-loop sequence data on riverine, swamp and hybrid buffaloes from India have been generated and compared with other reported Indian riverine, Chinese and Bangladeshi swamp buffalo populations. Sequence analysis revealed the presence of 132 haplotypes, with a haplotype diversity of 0.9611 ± 0.0045 and a nucleotide diversity of 0.04801 ± 0.00126. For the first time, the existence of riverine–swamp hybrids among the Indian Chilika buffalo population has been recorded, having 49 chromosomes, which was also confirmed by mitochondrial haplotype sharing between Chilika and Indian swamp as well as Chinese swamp buffalo populations in the network analysis. Phylogenetic analysis documents the sharing of reported pre-domestication haplogroups ‘SA1’, ‘SA2’, ‘SA3’ and ‘SB1’ between the Chilika and swamp buffalo populations of India, China and Bangladesh, an indication of the migration of swamp buffaloes towards Bangladesh and adjoining lower parts of India and north towards Chinese domestication sites. The results have also been supplemented by multidimension scaling, grouping Indian and Chinese swamp buffaloes more closely together with Bangladeshi buffaloes, but into a separate quadrant, whereas Chilika grouped away from other riverine as well as swamp buffaloes. These findings thus confirm the previous reports that the northeast region of India, close to the Indo-China border, is the point of evolution of swamp buffaloes with multiple sites of domestication.     

Origin of mitochondrial DNA diversity of domestic yaks

Background  

The domestication of plants and animals was extremely important anthropologically. Previous studies have revealed a general tendency for populations of livestock species to include deeply divergent maternal lineages, indicating that they were domesticated in multiple, independent events from genetically discrete wild populations. However, in water buffalo, there are suggestions that a similar deep maternal bifurcation may have originated from a single population. These hypotheses have rarely been rigorously tested because of a lack of sufficient wild samples. To investigate the origin of the domestic yak (Poephagus grunnies), we analyzed 637 bp of maternal inherited mtDNA from 13 wild yaks (including eight wild yaks from a small population in west Qinghai) and 250 domesticated yaks from major herding regions.     

Independent maternal origin of Chinese swamp buffalo (Bubalus bubalis)

To obtain more knowledge on the origin and genetic diversity of the swamp buffalo (Bubalus bubalis) in China, the complete mitochondrial D-loop sequences of 119 samples representing seven native types were compared. Two mitochondrial DNA (mtDNA) lineages (lineages A and B) were determined for the Chinese swamp buffalo. Examination of the diversity patterns suggest that lineage A has undergone a population expansion event. Divergence of lineages A and B was estimated at 18,000 years ago. Combined analyses of mtDNA sequences from Chinese, Indian, Brazilian/Italian and Southeast Asian/Australian buffalo samples showed independent domestication events in the swamp buffalo from China and the river buffalo from the India subcontinent. The spread of swamp and river buffalo from China and India respectively to mainland Southeast Asia suggests that Southeast Asia is a hybrid zone for buffalo. Our data support the hypothesis of the evolution of domesticated swamp and river buffalo from ancestral swamp-like animals. These ancestral animals were extensively distributed across mainland Asia and most likely are represented today by the wild Asian buffalo (Bubalus arnee).     

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

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.     

Analysis of mitochondrial D-loop region casts new light on domestic water buffalo (Bubalus bubalis) phylogeny

The phylogeny of water buffaloes (Bubalus bubalis) is still a matter of discussion, especially if the two types of domestic water buffalo (swamp and river) derived from different domestication events or if they are products of human selection. To obtain more insight, we analyzed the entire mitochondrial D-loop region of 80 water buffaloes of four different breeds, i.e., 19 swamp buffaloes (Carabao) and 61 river buffaloes (Murrah, Jafarabadi, and Mediterranean), sampled in Brazil and Italy. We detected 36 mitochondrial haplotypes with 128 polymorphic sites. Pooled with published data of South-East Asian and Australian water buffaloes and based on comprehensive median-joining network and population demography analyses we show evidence that both river and swamp buffaloes decent from one domestication event, probably in the Indian subcontinent. However, the today swamp buffaloes have an unravelled mitochondrial history, which can be explained by introgression of wild water buffalo mtDNA into domestic stocks. We are also discussing indications for an independent domestication of buffaloes in China.     

Evolution and domestication of the Bovini species

Domestication of the Bovini species (taurine cattle, zebu, yak, river buffalo and swamp buffalo) since the early Holocene (ca. 10 000 BCE) has contributed significantly to the development of human civilization. In this study, we review recent literature on the origin and phylogeny, domestication and dispersal of the three major Bos species – taurine cattle, zebu and yak – and their genetic interactions. The global dispersion of taurine and zebu cattle was accompanied by population bottlenecks, which resulted in a marked phylogeographic differentiation of the mitochondrial and Y-chromosomal DNA. The high diversity of European breeds has been shaped through isolation-by-distance, different production objectives, breed formation and the expansion of popular breeds. The overlapping and broad ranges of taurine and zebu cattle led to hybridization with each other and with other bovine species. For instance, Chinese gayal carries zebu mitochondrial DNA; several Indonesian zebu descend from zebu bull × banteng cow crossings; Tibetan cattle and yak have exchanged gene variants; and about 5% of the American bison contain taurine mtDNA. Analysis at the genomic level indicates that introgression may have played a role in environmental adaptation.     

Evaluating the potential for reintroducing the endangered wild water buffalo (Bubalus arnee) in Kanha National Park,central India

Reintroducing megafauna to their historic range is an effective strategy to halt their extinctions and restore ecosystems. Wild water buffalo (Bubalus arnee) is an endangered megaherbivore that is lost from 95% of its range. About 90% of its global population (less than 4000) resides within India, in two isolated populations: northeast and central India. The central Indian population is on the verge of extinction and warrants urgent conservation interventions. We assess the potential and provide a strategy for reintroducing buffaloes in Kanha National Park, India. Habitat suitability using the global occurrence of buffalo revealed low-lying grasslands with least human pressure found in Kanha (390 km²) to be suitable. Within this suitable range, we evaluated vegetation composition, forage biomass, and potential carrying capacity. Multidimensional ordination classified these suitable sites into moist and dry grassland clusters. Moist grasslands were found to better suit reintroduction due to lower grazing pressure, higher productivity, and availability of perennial water sources. Distinct matriarchal clades of swamp and river buffalo were observed. Within the river buffalo clade, Indian wild buffaloes formed a distinct cluster with close proximity between northeast and central Indian samples, suggesting northeast buffaloes could be sourced for a founding population in Kanha. Following IUCN guidelines, we discuss the reintroduction strategy that could sustain approximately 200 buffaloes in the area and subsequently expand to other suitable habitats in central India. If implemented as proposed, recovery of this lost ecosystem engineer will help to restore grasslands, and swamp habitats, as well as contribute to its global conservation efforts.     

Mapping of the transcription start site (TSS) and identification of SNPs in the bovine neuropeptide Y (NPY) gene

Background

The domestic goat is one of the important livestock species of India. In the present study we assess genetic diversity of Indian goats using 17 microsatellite markers. Breeds were sampled from their natural habitat, covering different agroclimatic zones.

Results

The mean number of alleles per locus (NA) ranged from 8.1 in Barbari to 9.7 in Jakhrana goats. The mean expected heterozygosity (He) ranged from 0.739 in Barbari to 0.783 in Jakhrana goats. Deviations from Hardy-Weinberg Equilibrium (HWE) were statistically significant (P < 0.05) for 5 loci breed combinations. The D_A measure of genetic distance between pairs of breeds indicated that the lowest distance was between Marwari and Sirohi (0.135). The highest distance was between Pashmina and Black Bengal. An analysis of molecular variance indicated that 6.59% of variance exists among the Indian goat breeds. Both a phylogenetic tree and Principal Component Analysis showed the distribution of breeds in two major clusters with respect to their geographic distribution.

Conclusion

Our study concludes that Indian goat populations can be classified into distinct genetic groups or breeds based on the microsatellites as well as mtDNA information.     

Evolution and diversity studies of innate immune genes in Indian buffalo (<Emphasis Type="Italic">Bubalus bubalis</Emphasis>) breeds using next generation sequencing

Indian buffalo (Bubalus bubalis) breeds are acknowledged for their disease resistance power, hardiness and considerable milk production. River buffaloes are more disease resistance despite of tropical environment of India than cattle breeds of the world. The genetic polymorphisms of innate immune genes play a prominent role in disease susceptibility of livestock. Here in our study, we mainly focused on SNPs in ten selected candidate innate immune genes viz CHGA, CHGB, CHGC, Slc11a1, Slc11a2, DEFB1, BNBD4, BNBD5, LAP and TAP among three most economically important Indian buffalo breeds viz., Jaffrabadi, Mehsani and Murrah using amplicon sequencing on Ion torrent PGM sequencing platform. Polymorphism identification using by GATK tool of Unified Genotyper revealed 274, 245 and 224 high quality SNPs in Jaffrabadi, Mehsani and Murrah buffalo breeds, respectively as well as 168 common SNPs among these three breeds and uniquely detected SNPs were 31, 15 and 37 SNPs in Jaffrabadi, Mehsani and Murrah breeds respectively. Consequences of non-synonymous SNPs were analysed using several computational tools viz., I-Mutant, SIFT, PolyPhen and PROVEAN which identified three deleterious nsSNPs. This wealth of sequence information will be productive for conservation studies, selective breeding and designing future strategies for identifying disease associations.     

DNA fingerprinting of Pakistani buffalo breeds (Nili-Ravi, Kundi) using microsatellite and cytochrome b gene markers

Cytochrome b gene markers have been proved as an efficient and powerful tool for breed characterization and species identification of buffaloes. This study represents the substantial analysis of mitochondrial DNA variation in Pakistani buffalo breeds and provides information about their genetic diversity. In this study partial amplification of cytochrome b gene of 1,061 bp was done and sequencing results showed ten haplotypes. Comparing all fifty samples from two buffalo breeds of Pakistan, fifteen polymorphic sites were observed out of which, twelve codons 42, 71, 118, 120, 199, 235, 269, 297, 318, 327, 350, 355 of mitochondrial cytochrome b gene are monomorphic which translate same amino acids as in the reference protein sequence due to silent mutation while different in DNA sequence. Similarly three codons 163, 246, 337 of mitochondrial cytochrome b are polymorphic and different from the reference sequence with respect to DNA as well as protein sequence. For the further confirmation a panel of nine microsatellite markers was used with high polymorphism information content (PIC). The frequency distribution of these alleles varies from three to eight allele at locus CSSM66 and ILST029 respectively. The results obtained from this study may contribute to the establishment of routine genotyping service of buffalo breeds for buffalo farmers for animal forensic application in case of any dispute. Additionally this study may help for breed characterization and phylogeny of aforementioned breeds of buffalo.     

Genetic diversity of mitochondrial cytochrome b gene in swamp buffalo

The swamp buffalo (Bubalus carabanensis) is mainly bred for meat, transport and rice cultivation in China and Southeast Asian countries. In the current study, we investigated the genetic diversity, maternal origin and phylogenetic relationship of swamp buffalo by analyzing 1,786 mitochondrial cytochrome b (cytb) sequences from China, Vietnam, Laos, Thailand, India and Bangladesh. Our results indicated that the swamp buffalo can be divided into two major lineages (SA and SB with the sublineages) and three rare lineages (SC, SD and SE), which showed strong geographic differentiation. The SA1 lineage represented a major domestication event, which involved population expansion. Regions III and V showed higher haplotype diversity than the other regions, indicating that the regions of Southwest China and IndoChina are potential domestication centers for the swamp buffalo. In addition, the swamp buffalo showed a closer phylogenetic relationship to tamaraw. In conclusion, our findings revealed a high level of genetic diversity and the phylogenetic pattern of the swamp buffalo.     

Evaluation of genetic diversity and population structure of west‐central Indian cattle breeds

Evaluations of genetic diversity in domestic livestock populations are necessary to implement region‐specific conservation measures. We determined the genetic diversity and evolutionary relationships among eight geographically and phenotypically diverse cattle breeds indigenous to west‐central India by genotyping these animals for 22 microsatellite loci. A total of 326 alleles were detected, and the expected heterozygosity ranged from 0.614 (Kenkatha) to 0.701 (Dangi). The mean number of alleles among the cattle breeds ranged from 7.182 (Khillar) to 9.409 (Gaolao). There were abundant genetic variations displayed within breeds, and the genetic differentiation was also high between the Indian cattle breeds, which displayed 15.9% of the total genetic differentiation among the different breeds. The genetic differentiation (pairwise F_ST) among the eight Indian breeds varied from 0.0126 for the Kankrej–Malvi pair to 0.2667 for Khillar–Kenkatha pair. The phylogeny, principal components analysis, and structure analysis further supported close grouping of Kankrej, Malvi, Nimari and Gir; Gaolao and Kenkatha, whereas Dangi and Khillar remained at distance from other breeds.     

Complete mitogenome reveals genetic divergence and phylogenetic relationships among Indian cattle (Bos indicus) breeds

Indigenous cattle of India belong to the species, Bos indicus and they possess various adaptability and production traits. However, little is known about the genetic diversity and origin of these breeds. To investigate the status, we sequenced and analyzed the whole mitochondrial DNA (mtDNA) of seven Indian cattle breeds. In total, 49 single-nucleotide variants (SNVs) were identified among the seven breeds analyzed. We observed a common synonymous SNV in the COII gene (m.7583G?>?A) of all the breeds studied. The phylogenetic analysis and genetic distance estimation showed the close genetic relationship among the Indian cattle breeds, whereas distinct genetic differences were observed between Bos indicus and Bos taurus cattle. Our results indicate a common ancestor for European Zwergzebu breed and South Indian cattle. The estimated divergence time demonstrated that the Bos indicus and Bos taurus cattle lineages diverged 0.92 million years ago. Our study also demonstrates that ancestors of present zebu breeds originated in South and North India separately ～30,000 to 20,000 years ago. In conclusion, the identified genetic variants and results of the phylogenetic analysis may provide baseline information to develop appropriate strategies for management and conservation of Indian cattle breeds.     

Y‐chromosomal variation confirms independent domestications of swamp and river buffalo

Y‐chromosomal variation in the water buffalo was analysed by sequencing of DBY, ZFY and SRY gene segments. A clear separation of the paternal lineages of the river and swamp types parallels the differences between their maternal lineages and nuclear DNA. Sequence divergence was found to be comparable to the divergence of taurine cattle and zebu, and this divergence predated domestication, confirming that river and swamp buffalo originated from different wild populations. Within a sample of 23 Thai swamp buffaloes, we identified four haplotypes with different geographical distributions, two of which were shared by Thai wild buffaloes.     

A genome-wide scan for signatures of directional selection in domesticated pigs

Background

Animal domestication involved drastic phenotypic changes driven by strong artificial selection and also resulted in new populations of breeds, established by humans. This study aims to identify genes that show evidence of recent artificial selection during pig domestication.

Results

Whole-genome resequencing of 30 individual pigs from domesticated breeds, Landrace and Yorkshire, and 10 Asian wild boars at ~16-fold coverage was performed resulting in over 4.3 million SNPs for 19,990 genes. We constructed a comprehensive genome map of directional selection by detecting selective sweeps using an F_ST-based approach that detects directional selection in lineages leading to the domesticated breeds and using a haplotype-based test that detects ongoing selective sweeps within the breeds. We show that candidate genes under selection are significantly enriched for loci implicated in quantitative traits important to pig reproduction and production. The candidate gene with the strongest signals of directional selection belongs to group III of the metabolomics glutamate receptors, known to affect brain functions associated with eating behavior, suggesting that loci under strong selection include loci involved in behaviorial traits in domesticated pigs including tameness.

Conclusions

We show that a significant proportion of selection signatures coincide with loci that were previously inferred to affect phenotypic variation in pigs. We further identify functional enrichment related to behavior, such as signal transduction and neuronal activities, for those targets of selection during domestication in pigs.

Electronic supplementary material

The online version of this article (doi:10.1186/s12864-015-1330-x) contains supplementary material, which is available to authorized users.