On the origin and spread of horse domestication

For several decades, the origin of domestic horses has been the focus of research across multiple disciplines, yet many aspects of the horse domestication process remain poorly understood. One of the reasons for the difficulty in establishing a coherent scenario of horse domestication is that archaeological, mtDNA, and Y chromosome data have yielded ambiguous results, possibly because each class of markers reflects different aspects of the domestication process. In this thesis, I use large autosomal genetic datasets from horses sampled across Eurasia to investigate the origin and spread of horse domestication. I begin by characterising genetic diversity of horses from the Eurasian steppes and neighbouring regions, thus laying the groundwork for a more thorough analysis into the demographic history of horses. I then investigate the origin and mode of spread of horse domestication in the Eurasian steppe region using a spatially explicit genetic model. I show that horse domestication was initiated in the western part of the steppes, and that the spread of horse domestication involved both movement of domestic herds and extensive recruitment of wild horses from across this vast region, a scenario which integrates both archaeological and molecular evidence. Having established the route of spread of early domestic horses out of their domestication origin in the western steppe, I go on to investigate the routes and levels of gene flow among Eastern Eurasian horse populations post-domestication. I show that the ancient Silk Roads have played an important role in shaping the genetic structure of Eastern Eurasian horses, facilitating gene flow across deserts and high mountain chains. Finally, I provide further compelling evidence for the persistence of wild horses in the Iberian Peninsula throughout the Holocene period, and the substantial contribution of these local populations to the gene pool of Iberian domestic horses. Together, my results provide a coherent picture of the origin and spread of horse domestication, integrating for the first time previous evidence from archaeology, mtDNA and Y chromosome sequence data

RUNX2 tandem repeats and the evolution of facial length in placental mammals

Background When simple sequence repeats are integrated into functional genes, they can potentially act as evolutionary ‘tuning knobs’, supplying abundant genetic variation with minimal risk of pleiotropic deleterious effects. The genetic basis of variation in facial shape and length represents a possible example of this phenomenon. Runt-related transcription factor 2 (RUNX2), which is involved in osteoblast differentiation, contains a functionally-important tandem repeat of glutamine and alanine amino acids. The ratio of glutamines to alanines (the QA ratio) in this protein seemingly influences the regulation of bone development. Notably, in domestic breeds of dog, and in carnivorans in general, the ratio of glutamines to alanines is strongly correlated with facial length. Results In this study we examine whether this correlation holds true across placental mammals, particularly those mammals for which facial length is highly variable and related to adaptive behavior and lifestyle (e.g., primates, afrotherians, xenarthrans). We obtained relative facial length measurements and RUNX2 sequences for 41 mammalian species representing 12 orders. Using both a phylogenetic generalized least squares model and a recently-developed Bayesian comparative method, we tested for a correlation between genetic and morphometric data while controlling for phylogeny, evolutionary rates, and divergence times. Non-carnivoran taxa generally had substantially lower glutamine-alanine ratios than carnivorans (primates and xenarthrans with means of 1.34 and 1.25, respectively, compared to a mean of 3.1 for carnivorans), and we found no correlation between RUNX2 sequence and face length across placental mammals. Conclusions Results of our diverse comparative phylogenetic analyses indicate that QA ratio does not consistently correlate with face length across the 41 mammalian taxa considered. Thus, although RUNX2 might function as a ‘tuning knob’ modifying face length in carnivorans, this relationship is not conserved across mammals in general

Major population splits coincide with episodes of rapid climate change in a forest-dependent bird

Climate change influences population demography by altering patterns of gene flow and reproductive isolation. Direct mutation rates offer the possibility for accurate dating on the within-species level but are currently only available for a handful of vertebrate species. Here, we use the first directly estimated mutation rate in birds to study the evolutionary history of pied flycatchers (Ficedula hypoleuca). Using a combination of demographic inference and species distribution modelling, we show that all major population splits in this forest-dependent system occurred during periods of increased climate instability and rapid global temperature change. We show that the divergent Spanish subspecies originated during the Eemian-Weichselian transition 115-104 thousand years ago (kya), and not during the last glacial maximum (26.5-19 kya), as previously suggested. The magnitude and rates of climate change during the glacial-interglacial transitions that preceded population splits in pied flycatchers were similar to, or exceeded, those predicted to occur in the course of the current, human-induced climate crisis. As such, our results provide a timely reminder of the strong impact that episodes of climate instability and rapid temperature changes can have on species' evolutionary trajectories, with important implications for the natural world in the Anthropocene

European domestic horses originated in two holocene refugia

The role of European wild horses in horse domestication is poorly understood. While the fossil record for wild horses in Europe prior to horse domestication is scarce, there have been suggestions that wild populations from various European regions might have contributed to the gene pool of domestic horses. To distinguish between regions where domestic populations are mainly descended from local wild stock and those where horses were largely imported, we investigated patterns of genetic diversity in 24 European horse breeds typed at 12 microsatellite loci. The distribution of high levels of genetic diversity in Europe coincides with the distribution of predominantly open landscapes prior to domestication, as suggested by simulation-based vegetation reconstructions, with breeds from Iberia and the Caspian Sea region having significantly higher genetic diversity than breeds from central Europe and the UK, which were largely forested at the time the first domestic horses appear there. Our results suggest that not only the Eastern steppes, but also the Iberian Peninsula provided refugia for wild horses in the Holocene, and that the genetic contribution of these wild populations to local domestic stock may have been considerable. In contrast, the consistently low levels of diversity in central Europe and the UK suggest that domestic horses in these regions largely derive from horses that were imported from the Eastern refugium, the Iberian refugium, or both.This work was partially supported by a research studentship from the Biotechnology and Biological Sciences Research Council (BB/E527604/1) and a PhD studentship from the German Academic Exchange Service (D/07/44562) to VW, and a Leverhulme Trust project grant (F/09 757/B) to MAB. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript

Data from: Genotype-free estimation of allele frequencies reduces bias and improves demographic inference from RADSeq data

Restriction-site associated sequencing (RADSeq) facilitates rapid generation of thousands of genetic markers at relatively low cost; however, several sources of error specific to RADSeq methods often lead to biased estimates of allele frequencies and thereby to erroneous population genetic inference. Estimating the distribution of sample allele frequencies without calling genotypes was shown to improve population inference from whole genome sequencing data, but the ability of this approach to account for RADSeq-specific biases remains unexplored. Here we assess in how far genotype-free methods of allele frequency estimation affect demographic inference from empirical RADSeq data. Using the well-studied pied flycatcher (Ficedula hypoleuca) as a study system, we compare allele frequency estimation and demographic inference from whole genome sequencing data with that from RADSeq data matched for samples using both genotype-based and genotype free methods. The demographic history of pied flycatchers as inferred from RADSeq data was highly congruent with that inferred from WGS data when allele frequencies were estimated directly from the read data. In contrast, when allele frequencies were derived from called genotypes, RADSeq-based estimates of most model parameters fell outside the 95% confidence interval (CI) of estimates derived from WGS data. Notably, more stringent filtering of genotypes tended to increase the discrepancy between parameter estimates from WGS and RADSeq data, respectively. The results from this study demonstrate the ability of genotype-free methods to improve AFS-based demographic inference from RADSeq data and highlight the need to account for uncertainty in NGS data regardless of sequencing method

Major population splits coincide with episodes of rapid climate change in a forest-dependent bird

Climate change influences population demography by altering patterns of gene flow and reproductive isolation. Direct mutation rates offer the possibility for accurate dating on the within-species level but are currently only available for a handful of vertebrate species. Here, we use the first directly estimated mutation rate in birds to study the evolutionary history of pied flycatchers (Ficedula hypoleuca). Using a combination of demographic inference and species distribution modelling, we show that all major population splits in this forest-dependent system occurred during periods of increased climate instability and rapid global temperature change. We show that the divergent Spanish subspecies originated during the Eemian-Weichselian transition 115-104 thousand years ago (kya), and not during the last glacial maximum (26.5-19 kya), as previously suggested. The magnitude and rates of climate change during the glacial-interglacial transitions that preceded population splits in pied flycatchers were similar to, or exceeded, those predicted to occur in the course of the current, human-induced climate crisis. As such, our results provide a timely reminder of the strong impact that episodes of climate instability and rapid temperature changes can have on species' evolutionary trajectories, with important implications for the natural world in the Anthropocene.Peer reviewe

Data from: Ancient trade routes shaped the genetic structure of horses in eastern Eurasia

Animal exchange networks have been shown to play an important role in determining gene flow among domestic animal populations. The Silk Road is one of the oldest continuous exchange networks in human history, yet its effectiveness in facilitating animal exchange across large geographic distances and topographically challenging landscapes has never been explicitly studied. Horses are known to have been traded along the Silk Roads; however, extensive movement of horses in connection with other human activities may have obscured the genetic signature of the Silk Roads. To investigate the role of the Silk Roads in shaping the genetic structure of horses in eastern Eurasia we analysed microsatellite genotyping data from 455 village horses sampled from 17 locations. Using least-cost path methods, we compared the performance of models containing the Silk Roads as corridors for gene flow with models containing single landscape features. We also determined whether the recent isolation of former Soviet Union countries from the rest of Eurasia has affected the genetic structure of our samples. The overall level of genetic differentiation was low, consistent with historically high levels of gene flow across the study region. The spatial genetic structure was characterised by a significant, albeit weak, pattern of isolation by distance across the continent with no evidence for the presence of distinct genetic clusters. Incorporating landscape features considerably improved the fit of the data; however, when we controlled for geographic distance, only the correlation between genetic differentiation and the Silk Roads remained significant, supporting the effectiveness of this ancient trade network in facilitating gene flow across large geographic distances in a topographically complex landscape

Parallel plumage colour evolution and introgressive hybridization in wheatears

Genetic and phenotypic mosaics, in which various phenotypes and different genomic regions show discordant patterns of species or population divergence, offer unique opportunities to study the role of ancestral and introgressed genetic variation in phenotypic evolution. Here, we investigated the evolution of discordant phenotypic and genetic divergence in a monophyletic clade of four songbird taxa—pied wheatear (O. pleschanka), Cyprus wheatear (Oenanthe cypriaca), and western and eastern subspecies of black-eared wheatear (O. h. hispanica and O. h. melanoleuca). Phenotypically, black back and neck sides distinguish pied and Cyprus wheatears from the white-backed/necked black-eared wheatears. Meanwhile, mitochondrial variation only distinguishes western black-eared wheatear. In the absence of nuclear genetic data, and given frequent hybridization among eastern black-eared and pied wheatear, it remains unclear whether introgression is responsible for discordance between mitochondrial divergence patterns and phenotypic similarities, or whether plumage coloration evolved in parallel. Multispecies coalescent analyses of about 20,000 SNPs obtained from RAD data mapped to a draft genome assembly resolve the species tree, provide evidence for the parallel evolution of colour phenotypes and establish western and eastern black-eared wheatears as independent taxa that should be recognized as full species. The presence of the entire admixture spectrum in the Iranian hybrid zone and the detection of footprints of introgression from pied into eastern black-eared wheatear beyond the hybrid zone despite strong geographic structure of ancestry proportions furthermore suggest a potential role for introgression in parallel plumage colour evolution. Our results support the importance of standing heterospecific and/or ancestral variation in phenotypic evolution

Data from: Parallel plumage color evolution and introgressive hybridization in wheatears

Genetic and phenotypic mosaics, in which various phenotypes and different genomic regions show discordant patterns of species or population divergence, offer unique opportunities to study the role of ancestral and introgressed genetic variation in phenotypic evolution. Here, we investigated the evolution of discordant phenotypic and genetic divergence in a monophyletic clade of four songbird taxa – pied wheatear (O. pleschanka), Cyprus wheatear (O. cypriaca), and western and eastern subspecies of black-eared wheatear (O. h. hispanica and O. h. melanoleuca). Phenotypically, black back and neck-sides distinguish pied and Cyprus wheatears from the white-backed/necked black-eared wheatears. Meanwhile, mitochondrial variation only distinguishes western black-eared wheatear. In the absence of nuclear genetic data, and given frequent hybridization among eastern black-eared and pied wheatear, it remains unclear whether introgression is responsible for discordance between mitochondrial divergence patterns and phenotypic similarities, or whether plumage coloration evolved in parallel. Multispecies coalescent analyses of about 20’000 SNPs obtained from RAD data mapped to a draft genome assembly resolve the species tree, provide evidence for the parallel evolution of color phenotypes, and establish western and eastern black-eared wheatears as independent taxa that should be recognized as full species. The presence of the entire admixture spectrum in the Iranian hybrid zone and the detection of footprints of introgression from pied into eastern black-eared wheatear beyond the hybrid zone despite strong geographic structure of ancestry proportions furthermore suggest a potential role for introgression in parallel plumage color evolution. Our results support the importance of standing heterospecific and/or ancestral variation in phenotypic evolution