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Concept: Domestication of the horse

15

The Y chromosome directly reflects male genealogies, but the extremely low Y chromosome sequence diversity in horses has prevented the reconstruction of stallion genealogies [1, 2]. Here, we resolve the first Y chromosome genealogy of modern horses by screening 1.46 Mb of the male-specific region of the Y chromosome (MSY) in 52 horses from 21 breeds. Based on highly accurate pedigree data, we estimated the de novo mutation rate of the horse MSY and showed that various modern horse Y chromosome lineages split much later than the domestication of the species. Apart from few private northern European haplotypes, all modern horse breeds clustered together in a roughly 700-year-old haplogroup that was transmitted to Europe by the import of Oriental stallions. The Oriental horse group consisted of two major subclades: the Original Arabian lineage and the Turkoman horse lineage. We show that the English Thoroughbred MSY was derived from the Turkoman lineage and that English Thoroughbred sires are largely responsible for the predominance of this haplotype in modern horses.

Concepts: Genetic genealogy, Horse, Genealogical DNA test, Purebred, Domestication of the horse, Haplogroup, Arabian horse, Akhal-Teke

12

Some domestic animals are thought to be skilled at social communication with humans due to the process of domestication. Horses, being in close relationship with humans, similar to dogs, might be skilled at communication with humans. Previous studies have indicated that they are sensitive to bodily signals and the attentional state of humans; however, there are few studies that investigate communication with humans and responses to the knowledge state of humans. Our first question was whether and how horses send signals to their potentially helpful but ignorant caretakers in a problem-solving situation where a food item was hidden in a bucket that was accessible only to the caretakers. We then examined whether horses alter their behaviours on the basis of the caretakers' knowledge of where the food was hidden. We found that horses communicated to their caretakers using visual and tactile signals. The signalling behaviour of the horses significantly increased in conditions where the caretakers had not seen the hiding of the food. These results suggest that horses alter their communicative behaviour towards humans in accordance with humans' knowledge state.

Concepts: Psychology, Horse, Behavior, Maize, Communication, Behaviorism, Domestication, Domestication of the horse

7

The mammal gut microbiome, which includes host microbes and their respective genes, is now recognized as an essential second genome that provides critical functions to the host. In humans, studies have revealed that lifestyle strongly influences the composition and diversity of the gastrointestinal microbiome. We hypothesized that these trends in humans may be paralleled in mammals subjected to anthropogenic forces such as domestication and captivity, in which diets and natural life histories are often greatly modified. We investigated fecal microbiomes of Przewalski’s horse (PH; Equus ferus przewalskii), the only horses alive today not successfully domesticated by humans, and herded, domestic horse (E. f. caballus) living in adjacent natural grasslands. We discovered PH fecal microbiomes hosted a distinct and more diverse community of bacteria compared to domestic horses, which is likely partly explained by different plant diets as revealed by trnL maker data. Within the PH population, four individuals were born in captivity in European zoos and hosted a strikingly low diversity of fecal microbiota compared to individuals born in natural reserves in France and Mongolia. These results suggest that anthropogenic forces can dramatically reshape equid gastrointestinal microbiomes, which has broader implications for the conservation management of endangered mammals.

Concepts: Mammal, Horse, Wild horse, Equus, Donkey, Domestication of the horse, Przewalski's Horse, Tarpan

7

Przewalski’s horses (PHs, Equus ferus ssp. przewalskii) were discovered in the Asian steppes in the 1870s and represent the last remaining true wild horses. PHs became extinct in the wild in the 1960s but survived in captivity, thanks to major conservation efforts. The current population is still endangered, with just 2,109 individuals, one-quarter of which are in Chinese and Mongolian reintroduction reserves [1]. These horses descend from a founding population of 12 wild-caught PHs and possibly up to four domesticated individuals [2-4]. With a stocky build, an erect mane, and stripped and short legs, they are phenotypically and behaviorally distinct from domesticated horses (DHs, Equus caballus). Here, we sequenced the complete genomes of 11 PHs, representing all founding lineages, and five historical specimens dated to 1878-1929 CE, including the Holotype. These were compared to the hitherto-most-extensive genome dataset characterized for horses, comprising 21 new genomes. We found that loci showing the most genetic differentiation with DHs were enriched in genes involved in metabolism, cardiac disorders, muscle contraction, reproduction, behavior, and signaling pathways. We also show that DH and PH populations split ∼45,000 years ago and have remained connected by gene-flow thereafter. Finally, we monitor the genomic impact of ∼110 years of captivity, revealing reduced heterozygosity, increased inbreeding, and variable introgression of domestic alleles, ranging from non-detectable to as much as 31.1%. This, together with the identification of ancestry informative markers and corrections to the International Studbook, establishes a framework for evaluating the persistence of genetic variation in future reintroduced populations.

Concepts: Gene, Genetics, Horse, Extinction, Wild horse, Domestication of the horse, Przewalski's Horse, Tarpan

7

Despite decades of research across multiple disciplines, the early history of horse domestication remains poorly understood. On the basis of current evidence from archaeology, mitochondrial DNA, and Y-chromosomal sequencing, a number of different domestication scenarios have been proposed, ranging from the spread of domestic horses out of a restricted primary area of domestication to the domestication of numerous distinct wild horse populations. In this paper, we reconstruct both the population genetic structure of the extinct wild progenitor of domestic horses, Equus ferus, and the origin and spread of horse domestication in the Eurasian steppes by fitting a spatially explicit stepping-stone model to genotype data from >300 horses sampled across northern Eurasia. We find strong evidence for an expansion of E. ferus out of eastern Eurasia about 160 kya, likely reflecting the colonization of Eurasia by this species. Our best-fitting scenario further suggests that horse domestication originated in the western part of the Eurasian steppe and that domestic herds were repeatedly restocked with local wild horses as they spread out of this area. By showing that horse domestication was initiated in the western Eurasian steppe and that the spread of domestic herds across Eurasia involved extensive introgression from the wild, the scenario of horse domestication proposed here unites evidence from archaeology, mitochondrial DNA, and Y-chromosomal DNA.

Concepts: Horse, Steppe, Wild horse, Domestication of the horse, Central Asia, Kazakhstan, Eurasian, Eurasian Steppe

3

Nosebands are used by riders to prevent the horse from opening its mouth, to increase control and, in some cases, to comply with the competition rules. While equestrian texts traditionally recommend that two adult human fingers should be able to fit under a fastened noseband, noseband tightness levels are not, in general, regulated in competition. Possible detrimental consequences for the horse, of excessively tight nosebands, include discomfort, pain or tissue damage. The current study investigated noseband usage in equestrian competition. Data regarding noseband type, position, width and tightness were collected from 750 horses in eventing (n = 354), dressage (n = 334) and performance hunter (n = 62) competitions in Ireland, England and Belgium. Data were collected immediately before or after the performance. Using the ISES taper gauge as a guide, results were classified according to the number of ‘fingers’ that could fit under the noseband at the nasal planum, and assigned to six groups: greater than 2 fingers; 2 fingers; 1.5 fingers; 1 finger; 0.5 fingers; zero fingers. A calliper was used to measure noseband width and position relative to the facial crest. The data were not normally distributed so Kruskall-Wallis and Mann-Whitney tests were used. In all, 44% of horses fell into the zero fingers classification while only 7% were in the two fingers classification. Significant differences emerged between disciplines (p<0.001), with the highest levels of noseband tightness measured among eventers followed by dressage horses with lowest levels among performance hunters. Noseband tightness did not differ significantly with horse age (p>0.05), which ranged from 4 to 19 years. The flash noseband was the most commonly used noseband (n = 326) and was significantly tighter than the cavesson (p < 0.001), drop noseband (p < 0.001) and the Micklem (p < 0.005). Noseband width ranged from 10 to 50 mm. Noseband position varied widely with the distance between the facial crest and upper noseband margin ranging from 0 to 70 mm. The high proportion of very tight nosebands found in this study raises concerns regarding the short and long term behavioural and physiological consequences of such tight nosebands are for the horse. Although these data are currently lacking, the findings are of concern.

Concepts: Horse, Domestication of the horse, Eventing, Dressage, Bridle, Horse tack, Show jumping, Noseband

3

For centuries, domestic horses have represented an important means of transport and served as working and companion animals. Although their role in transportation is less important today, many horse breeds are still subject to intense selection based on their pattern of locomotion. A striking example of such a selected trait is the ability of a horse to perform additional gaits other than the common walk, trot and gallop. Those could be four-beat ambling gaits, which are particularly smooth and comfortable for the rider, or pace, used mainly in racing. Gaited horse breeds occur around the globe, suggesting that gaitedness is an old trait, selected for in many breeds. A recent study discovered that a nonsense mutation in DMRT3 has a major impact on gaitedness in horses and is present at a high frequency in gaited breeds and in horses bred for harness racing. Here, we report a study of the worldwide distribution of this mutation. We genotyped 4396 horses representing 141 horse breeds for the DMRT3 stop mutation. More than half (2749) of these horses also were genotyped for a SNP situated 32 kb upstream of the DMRT3 nonsense mutation because these two SNPs are in very strong linkage disequilibrium. We show that the DMRT3 mutation is present in 68 of the 141 genotyped horse breeds at a frequency ranging from 1% to 100%. We also show that the mutation is not limited to a geographical area, but is found worldwide. The breeds with a high frequency of the stop mutation (>50%) are either classified as gaited or bred for harness racing.

Concepts: Horse, Nonsense mutation, Purebred, Domestication of the horse, Ambling, Trot, Horse gait, Peruvian Paso

2

The horse was domesticated only 5.5 KYA, thousands of years after dogs, cattle, pigs, sheep, and goats. The horse nonetheless represents the domestic animal that most impacted human history; providing us with rapid transportation, which has considerably changed the speed and magnitude of the circulation of goods and people, as well as their cultures and diseases. By revolutionizing warfare and agriculture, horses also deeply influenced the politico-economic trajectory of human societies. Reciprocally, human activities have circled back on the recent evolution of the horse, by creating hundreds of domestic breeds through selective programs, while leading all wild populations to near extinction. Despite being tightly associated with humans, several aspects in the evolution of the domestic horse remain controversial. Here, we review recent advances in comparative genomics and paleogenomics that helped advance our understanding of the genetic foundation of domestic horses.

Concepts: Gene, Evolution, Mammal, Horse, Extinction, Domestication, Livestock, Domestication of the horse

2

For the last 150 y scholars have focused upon the roles of intentional breeding and genetic isolation as fundamental to understanding the process of animal domestication. This analysis of ethnoarchaeological, archaeological, and genetic data suggests that long-term gene flow between wild and domestic stocks was much more common than previously assumed, and that selective breeding of females was largely absent during the early phases of animal domestication. These findings challenge assumptions about severe genetic bottlenecks during domestication, expectations regarding monophyletic origins, and interpretations of multiple domestications. The findings also raise new questions regarding ways in which behavioral and phenotypic domestication traits were developed and maintained.

Concepts: Gene, Genetics, Organism, Selective breeding, Genetic pollution, Domestication, Domestication of the horse, Wildness

2

Archaeological and genetic evidence concerning the time and mode of wild horse (Equus ferus) domestication is still debated. High levels of genetic diversity in horse mtDNA have been detected when analyzing the control region; recurrent mutations, however, tend to blur the structure of the phylogenetic tree. Here, we brought the horse mtDNA phylogeny to the highest level of molecular resolution by analyzing 83 mitochondrial genomes from modern horses across Asia, Europe, the Middle East, and the Americas. Our data reveal 18 major haplogroups (A-R) with radiation times that are mostly confined to the Neolithic and later periods and place the root of the phylogeny corresponding to the Ancestral Mare Mitogenome at ~130-160 thousand years ago. All haplogroups were detected in modern horses from Asia, but F was only found in E. przewalskii–the only remaining wild horse. Therefore, a wide range of matrilineal lineages from the extinct E. ferus underwent domestication in the Eurasian steppes during the Eneolithic period and were transmitted to modern E. caballus breeds. Importantly, now that the major horse haplogroups have been defined, each with diagnostic mutational motifs (in both the coding and control regions), these haplotypes could be easily used to (i) classify well-preserved ancient remains, (ii) (re)assess the haplogroup variation of modern breeds, including Thoroughbreds, and (iii) evaluate the possible role of mtDNA backgrounds in racehorse performance.

Concepts: DNA, Phylogenetics, Horse, Population genetics, Asia, Wild horse, Feral, Domestication of the horse