Xingbo Zhao

Patterns of East Asian pig domestication, migration, and turnover revealed by modern and ancient DNA

The establishment of agricultural economies based upon domestic animals began independently in many parts of the world and led to both increases in human population size and the migration of people carrying domestic plants and animals. The precise circumstances of the earliest phases of these events remain mysterious given their antiquity and the fact that subsequent waves of migrants have often replaced the first. Through the use of more than 1,500 modern (including 151 previously uncharacterized specimens) and 18 ancient (representing six East Asian archeological sites) pig (Sus scrofa) DNA sequences sampled across East Asia, we provide evidence for the long-term genetic continuity between modern and ancient Chinese domestic pigs. Although the Chinese case for independent pig domestication is supported by both genetic and archaeological evidence, we discuss five additional (and possibly) independent domestications of indigenous wild boar populations: one in India, three in peninsular Southeast Asia, and one off the coast of Taiwan. Collectively, we refer to these instances as “cryptic domestication,” given the current lack of corroborating archaeological evidence. In addition, we demonstrate the existence of numerous populations of genetically distinct and widespread wild boar populations that have not contributed maternal genetic material to modern domestic stocks. The overall findings provide the most complete picture yet of pig evolution and domestication in East Asia, and generate testable hypotheses regarding the development and spread of early farmers in the Far East.

Early Holocene chicken domestication in northern China

Significance Ancient DNA analysis is a powerful tool to reveal the geographical origins of domesticated species. Here we obtained ancient mtDNA sequences from the earliest archaeological chicken bones from northern China as early as 10,000 y ago. Combined analyses of our ancient sequences with a large dataset of published modern and ancient chicken mtDNA sequences suggest that northern China was likely one of several regions of chicken domestication and provide further insights into the process of human-mediated spread of chickens across the globe. Our results not only suggest that the oldest archaeological chicken bones recovered so far are indeed from ancestors of domestic chickens, but also provide further evidence for one of the earliest, mixed agricultural complexes in the world. Chickens represent by far the most important poultry species, yet the number, locations, and timings of their domestication have remained controversial for more than a century. Here we report ancient mitochondrial DNA sequences from the earliest archaeological chicken bones from China, dating back to ∼10,000 B.P. The results clearly show that all investigated bones, including the oldest from the Nanzhuangtou site, are derived from the genus Gallus, rather than any other related genus, such as Phasianus. Our analyses also suggest that northern China represents one region of the earliest chicken domestication, possibly dating as early as 10,000 y B.P. Similar to the evidence from pig domestication, our results suggest that these early domesticated chickens contributed to the gene pool of modern chicken populations. Moreover, our results support the idea that multiple members of the genus Gallus, specifically Gallus gallus and Gallus sonneratii contributed to the gene pool of the modern domestic chicken. Our results provide further support for the growing evidence of an early mixed agricultural complex in northern China.

Reply to Peters et al.: Further discussions confirm early Holocene chicken domestication in northern China

Peters et al. (1) raise several questions about early chicken domestication in northern China (2), including the claim that the climate would have been unsuitable for red jungle fowl. However, northern China was much warmer and more humid with much more extensive forest coverage during the early Holocene, as shown by the presence of buffalo bones (3) at Nanzhuagtou and macaque remains at Cishan (4), providing potential habitat for wild jungle fowl. We would also like to note that, in contrast to the claim by Peters et al., the data in reference 2 of ref. 1 indicate warmer conditions already during the early Holocene.

Reply to Peng et al.: Archaeological contexts should not be ignored for early chicken domestication

Peng et al. (1) question the evidence for early chicken domestication in Northern China (2) based on ancient DNA sequences obtained from archaeological bones. They point out that the sequences used in ref. 2 contain the primer sequences, and therefore haplotype recombinations were introduced. Although they are correct that the primer sequences were unintentionally included in the analyzed sequences, a reanalysis of the data reduced to the fragment between the primers shows that all conclusions drawn in the original publication (2) are also supported by the revised dataset.

Exploring the origin of domesticated pigs in the Yellow River area using information from ancient DNA

The origin of domesticated pigs is of interest to the general public. Technology to analyze ancient DNA can provide direct scientific evidence to address this question. It has been reported that modern Chinese pigs were domesticated in an independent pattern in the area of the middle and lower reaches of the Yellow River; however, ancient pig samples from the upper reaches of the Yellow River have never been tested. In this study, 14 unearthed ancient pig samples were collected from three archaeological sites in the upper and middle reaches of the Yellow River. Using DNA extraction, PCR amplification and DNA sequencing, these ancient samples were analyzed and compared with gene information from ancient pig samples from the middle and lower reaches of the Yellow River and from modern wild boars and domesticated pigs. We succeeded in generating a 179 bp sequence of mitochondrial D-loop from five ancient pig samples respectively, including three samples from the Qinglongquan archaeological site in Hubei Province and two samples from the Lajia archaeological site in Qinghai Province. Sequence alignment analysis indicated that ancient samples from Qinglongquan and Lajia were sorted into different haplotypes. Compared with previous data from ancient DNAs, modern pig breeds and wild boars, the two Qinglongquan samples shared one haplotype with one sample from the Jiahu site, and the Lajia samples shared a haplotype with four samples from the Gaohong archaeological site and with three samples from the Taosi archaeological site, which are both located in Shanxi Province. The two haplotypes were consistent with the four main types of modern Chinese pigs. The results indicate that pigs in the upper reaches of the Yellow River originated from the same domestic center as the pigs in the middle and lower reaches of the Yellow River did. These findings further our understanding of the origin of pig domestication in China.

Free Dietary Choice and Free-Range Rearing Improve the Product Quality, Gait Score, and Microbial Richness of Chickens

Simple Summary The worldwide demand for productivity and quality meat, eggs, and other animal products is increasing. More and more people are expressing concerns relating to product quality and animal welfare. Our study aimed to provide scientific knowledge regarding how welfare factors contribute to quantity and quality of chicken. We used 400 Beijing You chickens to compare welfare factors by providing free dietary choice under cage rearing, and further comparing cage rearing with the free-range rearing system. Results showed that under cage rearing, free dietary choice of mealworms and fresh grass contributed to better meat quality, gait score and foot pad dermatitis than the conventional cage feeding and rearing system. This also gave rise to higher values of blood platelets and a richer gut microbial composition. As compared to caged chickens, free-range chickens developed better meat quality, gait score, and feather conditions, as well as a richer microbial composition. Our work provides a comprehensive understanding of welfare factors under both cage and free-range systems, and also broadens knowledge of health-related gut microbial composition in chickens. Abstract Poultry welfare has been extensively studied; however, there is a lack of rigorous scientific knowledge relating to the different aspects of welfare factors and how this may contribute to the production quantity and product quality as well as the welfare of chickens. Therefore, we conducted an integrated study to compare welfare factors in chickens by providing free dietary choice under cage rearing, and further comparing cage rearing with free-range rearing. One hundred chickens each were allocated to a cage rearing group with conventional feeding (CC), a cage rearing group with free dietary choice of mealworms (FDM), a cage rearing group with free dietary choice of mealworms and fresh grass (FDMG), and a free-range rearing system group with free dietary choice of mealworms and fresh grass (FRMG). Results showed that under cage rearing, free dietary choice contributed to better meat quality and gait score, higher values of blood platelets, and a richer gut microbial composition, but poorer egg production than CC chickens. As compared to FDMG, FRMG chickens showed better meat quality, gait score, and feather conditions, as well as a richer gut microbial composition; however, they had poorer egg production and a poorer foot pad and foot feather condition. We conclude that free dietary choice and free-range rearing systems improve the product quality, gait score, and microbial richness of chickens.

Mitochondrial haplotypes influence metabolic traits across bovine inter- and intra-species cybrids

In bovine species, mitochondrial DNA polymorphisms and their correlation to productive or reproductive performances have been widely reported across breeds and individuals. However, experimental evidence of this correlation has never been provided. In order to identify differences among bovine mtDNA haplotypes, transmitochondrial cybrids were generated, with the nucleus from MAC-T cell line, derived from a Holstein dairy cow (Bos taurus) and mitochondria from either primary cell line derived from a domestic Chinese native beef Luxi cattle breed or central Asian domestic yak (Bos grunniens). Yak primary cells illustrated a stronger metabolic capacity than that of Luxi. However, all yak cybrid parameters illustrated a drop in relative yak mtDNA compared to Luxi mtDNA, in line with a mitonuclear imbalance in yak interspecies cybrid. Luxi has 250 divergent variations relative to the mitogenome of Holsteins. In cybrids there were generally higher rates of oxygen consumption (OCR) and extracellular acidification (ECAR), and lower mRNA expression levels of nuclear-encoded mitochondrial genes, potentially reflecting active energy metabolism and cellular stress resistance. The results demonstrate that functional differences exist between bovine cybrid cells. While cybrid viability was similar between Holstein and Luxi breeds, the mitonuclear mismatch caused a marked metabolic dysfunction in cattle:yak cybrid species.

Origin and dispersal of early domestic pigs in northern China

It is widely accepted that modern pigs were domesticated independently at least twice, and Chinese native pigs are deemed as direct descendants of the first domesticated pigs in the corresponding domestication centers. By analyzing mitochondrial DNA sequences of an extensive sample set spanning 10,000 years, we find that the earliest pigs from the middle Yellow River region already carried the maternal lineages that are dominant in both younger archaeological populations and modern Chinese pigs. Our data set also supports early Neolithic pig utilization and a long-term in situ origin for northeastern Chinese pigs during 8,000–3,500 BP, suggesting a possibly independent domestication in northeast China. Additionally, we observe a genetic replacement in ancient northeast Chinese pigs since 3,500 BP. The results not only provide increasing evidence for pig origin in the middle Yellow River region but also depict an outline for the process of early pig domestication in northeast China.

Mitochondrial DNA T7719G in tRNA-Lys gene affects litter size in Small-tailed Han sheep

BackgroundIn farm animals, mitochondrial DNA (mtDNA) effect on economic performance remains hot-topic for breeding and genetic selection. Here, 53 maternal lineages of Small-tailed Han sheep were used to investigate the association of mitochondrial DNA variations and the lambing litter size.ResultsSequence sweeping of the mitochondrial coding regions discovered 31 non-synonymous mutations, and the association study revealed that T7719G in mtDNA tRNA-Lys gene was associated with litter size (P < 0.05), manifesting 0.29 lambs per litter between the G and T carriers. Furthermore, using the mixed linear model, we assayed the potential association of the ovine litter size and haplogroups and multiple-level mtDNA haplotypes, including general haplotypes, assembled haplotypes of electron transport chain contained sequences (H-ETC), mitochondrial respiratory complex contained sequences (H-MRC) and mitochondrial genes (H-gene, including polypeptide-coding genes, rRNA genes and tRNA genes). The strategy for assembled mitochondrial haplotypes was proposed for the first time in mtDNA association analyses on economic traits, although none of the significant relations could be concluded (P > 0.05). In addition, the nuclear major gene BMPR1B was significantly correlated with litter size in the flock (P < 0.05), however, did not interact with mtDNA T7719G mutation (P > 0.05).ConclusionsOur results highlight mutations of ovine mitochondrial coding genes, suggesting T7719G in tRNA-Lys gene be a potentially useful marker for selection of sheep litter size.

Transcriptome changes provide genetic insights into the effects of rearing systems on chicken welfare and product quality

Farm animals raised under free-range (FR) systems are assumed to have improved welfare and higher-quality products that are better to eat than intensively reared animals. However, the modulations are limited in scientific investigations. In this study, we compared 2 rearing systems (FR and cage) and their effects on chickens, including production performance, product quality, body condition, physiological indicators, and gene expression. By using a match-mismatch design in which each treatment was transferred to the other treatment during the last period of the experiment, we aimed to understand the influence of current and former rearing conditions and the ability of individuals to adapt to the current environment. The results indicated that the FR system led to better chicken welfare (e.g., gait score, feather condition, and physiological indicators, P < 0.05) and contributed to higher product quality (P < 0.05), although it resulted in poorer production performance (P < 0.05) and foot pad condition (P < 0.05) than that of the cage rearing system. Additionally, the FR system triggered a series of inner changes and genetic responses in chickens, such as the upregulation of calcium and GnRH signaling, actin and cytoskeleton regulations, immune functions, and developmental processes, and the downregulation of pathological regulations (q-value < 0.05 for all gene ontology terms and P < 0.05 for all Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways). In conclusion, rearing systems alter chicken gene expression patterns, which provide a genetic basis for the adaptability to rearing environments and ultimately affects chicken welfare and products.