Adam H. Freedman

Genome Sequencing Highlights the Dynamic Early History of Dogs

To identify genetic changes underlying dog domestication and reconstruct their early evolutionary history, we generated high-quality genome sequences from three gray wolves, one from each of the three putative centers of dog domestication, two basal dog lineages (Basenji and Dingo) and a golden jackal as an outgroup. Analysis of these sequences supports a demographic model in which dogs and wolves diverged through a dynamic process involving population bottlenecks in both lineages and post-divergence gene flow. In dogs, the domestication bottleneck involved at least a 16-fold reduction in population size, a much more severe bottleneck than estimated previously. A sharp bottleneck in wolves occurred soon after their divergence from dogs, implying that the pool of diversity from which dogs arose was substantially larger than represented by modern wolf populations. We narrow the plausible range for the date of initial dog domestication to an interval spanning 11–16 thousand years ago, predating the rise of agriculture. In light of this finding, we expand upon previous work regarding the increase in copy number of the amylase gene (AMY2B) in dogs, which is believed to have aided digestion of starch in agricultural refuse. We find standing variation for amylase copy number variation in wolves and little or no copy number increase in the Dingo and Husky lineages. In conjunction with the estimated timing of dog origins, these results provide additional support to archaeological finds, suggesting the earliest dogs arose alongside hunter-gathers rather than agriculturists. Regarding the geographic origin of dogs, we find that, surprisingly, none of the extant wolf lineages from putative domestication centers is more closely related to dogs, and, instead, the sampled wolves form a sister monophyletic clade. This result, in combination with dog-wolf admixture during the process of domestication, suggests that a re-evaluation of past hypotheses regarding dog origins is necessary.

Complete mitochondrial genomes of ancient canids suggest a European origin of domestic dogs

Dog Domestication The precise details of the domestication and origins of domestic dogs are unclear. Thalmann et al. (p. 871; see the cover) analyzed complete mitochondrial genomes from present-day dogs and wolves, as well as 18 fossil canids dating from 1000 to 36,000 years ago from the Old and New Worlds. The data suggest that an ancient, now extinct, central European population of wolves was directly ancestral to domestic dogs. Furthermore, several ancient dogs may represent failed domestication events. Ancient DNA suggests that dog domestication was complex and likely originated in Europe. The geographic and temporal origins of the domestic dog remain controversial, as genetic data suggest a domestication process in East Asia beginning 15,000 years ago, whereas the oldest doglike fossils are found in Europe and Siberia and date to >30,000 years ago. We analyzed the mitochondrial genomes of 18 prehistoric canids from Eurasia and the New World, along with a comprehensive panel of modern dogs and wolves. The mitochondrial genomes of all modern dogs are phylogenetically most closely related to either ancient or modern canids of Europe. Molecular dating suggests an onset of domestication there 18,800 to 32,100 years ago. These findings imply that domestic dogs are the culmination of a process that initiated with European hunter-gatherers and the canids with whom they interacted.

Genomic signals of diversification along ecological gradients in a tropical lizard

Studies of rainforest diversification that simultaneously consider the effects of genetic drift and natural selection are rare. We use Amplified Fragment Length Polymorphism genome scans of the African rainforest lizard Trachylepis affinis from Cameroon to examine the spatial patterns and environmental associations of both neutrally evolving loci and those thought to be under selection. Bayesian selection scans revealed that approximately 7% of the genome may be under divergent selection. Using non‐linear environmental modelling techniques, we fit patterns of genetic differentiation recovered from the pooled neutral data and from individual loci showing a signature of natural selection. Neutral differentiation occurred along a cline from coastal lowland rainforest inland toward the gallery forests‐savanna mosaic (ecotone), and was associated with both geographic distance and changing precipitation patterns. Loci under selection were differentiated predominantly along the forest–ecotone gradient—in concordance with morphological divergence in traits related to fitness. A second set of these loci was differentiated between lowland and montane habitats. A third set of loci was indicative of divergent selection between rainforest refugia. Niche models and demographic signals in mitochondrial sequence data support a population expansion out of a core rainforest area into savanna since the last glacial maximum. Our findings indicate adaptive diversification in T. affinis may be taking place along the forest–ecotone gradient during range expansions or contractions, and that refugial isolation augmented by divergent adaptation to different rainforest environments appears to play a less significant role.

Landscape genetics of California mule deer (Odocoileus hemionus): the roles of ecological and historical factors in generating differentiation

Landscape genetics is an emerging discipline that utilizes environmental and historical data to understand geographic patterns of genetic diversity. Niche modelling has added a new dimension to such efforts by allowing species–environmental associations to be projected into the past so that hypotheses about historical vicariance can be generated and tested independently with genetic data. However, previous approaches have primarily utilized DNA sequence data to test inferences about historical isolation and may have missed very recent episodes of environmentally mediated divergence. We type 15 microsatellite loci in California mule deer and identify five genetic groupings through a Structure analysis that are also well predicted by environmental data. We project the niches of these five deer ecotypes to the last glacial maximum (LGM) and show they overlap to a much greater extent than today, suggesting that vicariance associated with the LGM cannot explain the present‐day genetic patterns. Further, we analyse mitochondrial DNA (mtDNA) sequence trees to search for evidence of historical vicariance and find only two well‐supported clades. A coalescence‐based analysis of mtDNA data shows that the genetic divergence of the mule deer genetic clusters in California is recent and appears to be mediated by ecological factors. The importance of environmental factors in explaining the genetic diversity of California mule deer is unexpected given that they are highly mobile species and have a broad habitat distribution. Geographic differences in the timing of reproduction and peak vegetation as well as habitat choice reflecting natal origin may explain the persistence of genetic subdivision.

Spatial modelling and landscape-level approaches for visualizing intra-specific variation.

Spatial analytical methods have been used by biologists for decades, but with new modelling approaches and data availability their application is accelerating. While early approaches were purely spatial in nature, it is now possible to explore the underlying causes of spatial heterogeneity of biological variation using a wealth of environmental data, especially from satellite remote sensing. Recent methods can not only make inferences regarding spatial relationships and the causes of spatial heterogeneity, but also create predictive maps of patterns of biological variation under changing environmental conditions. Here, we review the methods involved in making continuous spatial predictions from biological variation using spatial and environmental predictor variables, provide examples of their use and critically evaluate the advantages and limitations. In the final section, we discuss some of the key challenges and opportunities for future work.

Demographically-Based Evaluation of Genomic Regions under Selection in Domestic Dogs.

Controlling for background demographic effects is important for accurately identifying loci that have recently undergone positive selection. To date, the effects of demography have not yet been explicitly considered when identifying loci under selection during dog domestication. To investigate positive selection on the dog lineage early in the domestication, we examined patterns of polymorphism in six canid genomes that were previously used to infer a demographic model of dog domestication. Using an inferred demographic model, we computed false discovery rates (FDR) and identified 349 outlier regions consistent with positive selection at a low FDR. The signals in the top 100 regions were frequently centered on candidate genes related to brain function and behavior, including LHFPL3, CADM2, GRIK3, SH3GL2, MBP, PDE7B, NTAN1, and GLRA1. These regions contained significant enrichments in behavioral ontology categories. The 3rd top hit, CCRN4L, plays a major role in lipid metabolism, that is supported by additional metabolism related candidates revealed in our scan, including SCP2D1 and PDXC1. Comparing our method to an empirical outlier approach that does not directly account for demography, we found only modest overlaps between the two methods, with 60% of empirical outliers having no overlap with our demography-based outlier detection approach. Demography-aware approaches have lower-rates of false discovery. Our top candidates for selection, in addition to expanding the set of neurobehavioral candidate genes, include genes related to lipid metabolism, suggesting a dietary target of selection that was important during the period when proto-dogs hunted and fed alongside hunter-gatherers.

Human Impacts Flatten Rainforest-Savanna Gradient and Reduce Adaptive Diversity in a Rainforest Bird

Ecological gradients have long been recognized as important regions for diversification and speciation. However, little attention has been paid to the evolutionary consequences or conservation implications of human activities that fundamentally change the environmental features of such gradients. Here we show that recent deforestation in West Africa has homogenized the rainforest-savanna gradient, causing a loss of adaptive phenotypic diversity in a common rainforest bird, the little greenbul (Andropadus virens). Previously, this species was shown to exhibit morphological and song divergence along this gradient in Central Africa. Using satellite-based estimates of forest cover, recent morphological data, and historical data from museum specimens collected prior to widespread deforestation, we show that the gradient has become shallower in West Africa and that A. virens populations there have lost morphological variation in traits important to fitness. In contrast, we find no loss of morphological variation in Central Africa where there has been less deforestation and gradients have remained more intact. While rainforest deforestation is a leading cause of species extinction, the potential of deforestation to flatten gradients and inhibit rainforest diversification has not been previously recognized. More deforestation will likely lead to further flattening of the gradient and loss of diversity, and may limit the ability of species to persist under future environmental conditions.

Modeling the effects of anthropogenic habitat change on savanna snake invasions into African rainforest.

We used a species-distribution modeling approach, ground-based climate data sets, and newly available remote-sensing data on vegetation from the MODIS and Quick Scatterometer sensors to investigate the combined effects of human-caused habitat alterations and climate on potential invasions of rainforest by 3 savanna snake species in Cameroon, Central Africa: the night adder (Causus maculatus), olympic lined snake (Dromophis lineatus), and African house snake (Lamprophis fuliginosus). Models with contemporary climate variables and localities from native savanna habitats showed that the current climate in undisturbed rainforest was unsuitable for any of the snake species due to high precipitation. Limited availability of thermally suitable nest sites and mismatches between important life-history events and prey availability are a likely explanation for the predicted exclusion from undisturbed rainforest. Models with only MODIS-derived vegetation variables and savanna localities predicted invasion in disturbed areas within the rainforest zone, which suggests that human removal of forest cover creates suitable microhabitats that facilitate invasions into rainforest. Models with a combination of contemporary climate, MODIS- and Quick Scatterometer-derived vegetation variables, and forest and savanna localities predicted extensive invasion into rainforest caused by rainforest loss. In contrast, a projection of the present-day species-climate envelope on future climate suggested a reduction in invasion potential within the rainforest zone as a consequence of predicted increases in precipitation. These results emphasize that the combined responses of deforestation and climate change will likely be complex in tropical rainforest systems.

Demographic history, selection and functional diversity of the canine genome

The domestic dog represents one of the most dramatic long-term evolutionary experiments undertaken by humans. From a large wolf-like progenitor, unparalleled diversity in phenotype and behaviour has developed in dogs, providing a model for understanding the developmental and genomic mechanisms of diversification. We discuss pattern and process in domestication, beginning with general findings about early domestication and problems in documenting selection at the genomic level. Furthermore, we summarize genotype–phenotype studies based first on single nucleotide polymorphism (SNP) genotyping and then with whole-genome data and show how an understanding of evolution informs topics as different as human history, adaptive and deleterious variation, morphological development, ageing, cancer and behaviour.

Similar genomic proportions of copy number variation within gray wolves and modern dog breeds inferred from whole genome sequencing

BackgroundWhole genome re-sequencing data from dogs and wolves are now commonly used to study how natural and artificial selection have shaped the patterns of genetic diversity. Single nucleotide polymorphisms, microsatellites and variants in mitochondrial DNA have been interrogated for links to specific phenotypes or signals of domestication. However, copy number variation (CNV), despite its increasingly recognized importance as a contributor to phenotypic diversity, has not been extensively explored in canids.ResultsHere, we develop a new accurate probabilistic framework to create fine-scale genomic maps of segmental duplications (SDs), compare patterns of CNV across groups and investigate their role in the evolution of the domestic dog by using information from 34 canine genomes. Our analyses show that duplicated regions are enriched in genes and hence likely possess functional importance. We identify 86 loci with large CNV differences between dogs and wolves, enriched in genes responsible for sensory perception, immune response, metabolic processes, etc. In striking contrast to the observed loss of nucleotide diversity in domestic dogs following the population bottlenecks that occurred during domestication and breed creation, we find a similar proportion of CNV loci in dogs and wolves, suggesting that other dynamics are acting to particularly select for CNVs with potentially functional impacts.ConclusionsThis work is the first comparison of genome wide CNV patterns in domestic and wild canids using whole-genome sequencing data and our findings contribute to study the impact of novel kinds of genetic changes on the evolution of the domestic dog.