Selection against domestication alleles in introduced rabbit populations.

Humans have moved domestic animals around the globe for thousands of years. These have occasionally established feral populations in nature, often with devastating ecological consequences. To understand how natural selection shapes re-adaptation into the wild, we investigated one of the most successful colonizers in history, the European rabbit. By sequencing the genomes of 297 rabbits across three continents, we show that introduced populations exhibit a mixed wild-domestic ancestry. We show that alleles that increased in frequency during domestication were preferentially selected against in novel natural environments. Interestingly, causative mutations for common domestication traits sometimes segregate at considerable frequencies if associated with less drastic phenotypes (for example, coat colour dilution), whereas mutations that are probably strongly maladaptive in nature are absent. Whereas natural selection largely targeted different genomic regions in each introduced population, some of the strongest signals of parallelism overlap genes associated with neuronal or brain function. This limited parallelism is probably explained by extensive standing genetic variation resulting from domestication together with the complex mixed ancestry of introduced populations. Our findings shed light on the selective and molecular mechanisms that enable domestic animals to re-adapt to the wild and provide important insights for the mitigation and management of invasive populations.

Species delineation and genetic structure of two Chaerephon species (C. pusillus and C. leucogaster) on Madagascar and the Comoro archipelago.

Cryptic species diversity is known to be common in bats but remains challenging to study in these mammals, whose natural history traits render their sampling and monitoring challenging. For these animals, indirect genetic approaches provide a powerful tool to gain insight into the evolutionary history and ecology of cryptic bat species. The speciation history of the polyphyletic Chaerephon pumilus species group (Molossidae) is poorly understood, including those found on western Indian Ocean islands. Two species in this complex have been identified in the Comoros: C. pusillus and C. leucogaster. Here, we aim to genetically characterize these two species and investigate their spatial population genetic structure. Analyzing five nuclear microsatellite markers from 200 individuals and one mitochondrial DNA gene (Cyt-b) from 161 (out of the 200) individuals sampled on Madagascar and the Comoros, our findings indicated that these species are genetically differentiated. We observed mitonuclear discordance in numerous individuals (33% of the 161 mtDNA-sequenced individuals). Based on ABC analyses, we found that this pattern could potentially be the result of asymmetric introgressive hybridization from C. leucogaster to C. pusillus and calls for further studies on the demographic history of these species. Moreover, at the intra-specific level, analyses of the microsatellite loci suggested the evidence of a more pronounced, although weak, geographically based genetic structure in C. pusillus than in C. leucogaster. Altogether, our findings provide preliminary insights into the eco-evolutionary aspects of this species complex and warrant further research to understand hybridization dynamics and mechanisms responsible for mitonuclear discordance.

Hybridization between Felis silvestris silvestris and Felis silvestris catus in two contrasted environments in France.

European wildcat (Felis silvestris silvestris) populations are fragmented throughout most of the whole range of the subspecies and may be threatened by hybridization with the domestic cat F.s. catus. The underlying ecological processes promoting hybridization remain largely unknown. In France, wildcats are mainly present in the northeast and signs of their presence in the Pyrenees have been recently provided. However, no studies have been carried out in the French Pyrenees to assess their exposure to hybridization. We compared two local populations of wildcats, one living in a continuous forest habitat in the French Pyrenees, the other living in a highly fragmented forest-agricultural landscape in northeastern France to get insights into the variability of hybridization rates. Strong evidence of hybridization was detected in northeastern France and not in the Pyrenees. Close kin in the Pyrenees were not found in the same geographic location contrary to what was previously reported for females in the northeastern wildcat population. The two wildcat populations were significantly differentiated (F ST = 0.072) to an extent close to what has been reported (F ST = 0.103) between the Iberian population, from which the Pyrenean population may originate, and the German population, which is connected to the northeastern population. The genetic diversity of the Pyrenean wildcats was lower than that of northeastern wildcat populations in France and in other parts of Europe. The lower hybridization in the Pyrenees may result from the continuity of natural forest habitats. Further investigations should focus on linking landscape features to hybridization rates working on local populations.

Parallel adaptation of rabbit populations to myxoma virus.

In the 1950s the myxoma virus was released into European rabbit populations in Australia and Europe, decimating populations and resulting in the rapid evolution of resistance. We investigated the genetic basis of resistance by comparing the exomes of rabbits collected before and after the pandemic. We found a strong pattern of parallel evolution, with selection on standing genetic variation favoring the same alleles in Australia, France, and the United Kingdom. Many of these changes occurred in immunity-related genes, supporting a polygenic basis of resistance. We experimentally validated the role of several genes in viral replication and showed that selection acting on an interferon protein has increased the protein's antiviral effect.

Coexistence of two sympatric cryptic bat species in French Guiana: insights from genetic, acoustic and ecological data.

BACKGROUND: The distinction between lineages of neotropical bats from the Pteronotus parnellii species complex has been previously made according to mitochondrial DNA, and especially morphology and acoustics, in order to separate them into two species. In these studies, either sample sizes were too low when genetic and acoustic or morphological data were gathered on the same individuals, or genetic and other data were collected on different individuals. In this study, we intensively sampled bats in 4 caves and combined all approaches in order to analyse genetic, morphologic, and acoustic divergence between these lineages that live in the same caves in French Guiana. RESULTS: A multiplex of 20 polymorphic microsatellite markers was developed using the 454-pyrosequencing technique to investigate for the first time the extent of reproductive isolation between the two lineages and the population genetic structure within lineages. We genotyped 748 individuals sampled between 2010 and 2015 at the 20 nuclear microsatellite loci and sequenced a portion of the cytochrome c oxydase I gene in a subset of these. Two distinct, non-overlapping haplogroups corresponding to cryptic species P. alitonus and P. rubiginosus were revealed, in accordance with previous findings. No spatial genetic structure between caves was detected for both species. Hybridization appeared to be quite limited (0.1-4%) using microsatellite markers whereas introgression was more common (7.5%) and asymmetric for mitochondrial DNA (mtDNA). CONCLUSIONS: The extremely low rate of hybridization could be explained by differences in life cycle phenology between species as well as morphological and acoustical distinction between sexes in one or the other species. Taken together, these results add to our growing understanding of the nature of species boundaries in Pteronotus parnelli, but deserve more in-depth studies to understand the evolutionary processes underlying asymmetric mtDNA introgression in this group of cryptic species.

Levels and Patterns of Genetic Diversity and Population Structure in Domestic Rabbits.

Over thousands of years humans changed the genetic and phenotypic composition of several organisms and in the process transformed wild species into domesticated forms. From this close association, domestic animals emerged as important models in biomedical and fundamental research, in addition to their intrinsic economical and cultural value. The domestic rabbit is no exception but few studies have investigated the impact of domestication on its genetic variability. In order to study patterns of genetic structure in domestic rabbits and to quantify the genetic diversity lost with the domestication process, we genotyped 45 microsatellites for 471 individuals belonging to 16 breeds and 13 wild localities. We found that both the initial domestication and the subsequent process of breed formation, when averaged across breeds, culminated in losses of ~20% of genetic diversity present in the ancestral wild population and domestic rabbits as a whole, respectively. Despite the short time elapsed since breed diversification we uncovered a well-defined structure in domestic rabbits where the FST between breeds was 22%. However, we failed to detect deeper levels of structure, probably consequence of a recent and single geographic origin of domestication together with a non-bifurcating process of breed formation, which were often derived from crosses between two or more breeds. Finally, we found evidence for intrabreed stratification that is associated with demographic and selective causes such as formation of strains, colour morphs within the same breed, or country/breeder of origin. These additional layers of population structure within breeds should be taken into account in future mapping studies.

Rabbit genome analysis reveals a polygenic basis for phenotypic change during domestication.

The genetic changes underlying the initial steps of animal domestication are still poorly understood. We generated a high-quality reference genome for the rabbit and compared it to resequencing data from populations of wild and domestic rabbits. We identified more than 100 selective sweeps specific to domestic rabbits but only a relatively small number of fixed (or nearly fixed) single-nucleotide polymorphisms (SNPs) for derived alleles. SNPs with marked allele frequency differences between wild and domestic rabbits were enriched for conserved noncoding sites. Enrichment analyses suggest that genes affecting brain and neuronal development have often been targeted during domestication. We propose that because of a truly complex genetic background, tame behavior in rabbits and other domestic animals evolved by shifts in allele frequencies at many loci, rather than by critical changes at only a few domestication loci.

The genetic structure of domestic rabbits.

Understanding the genetic structure of domestic species provides a window into the process of domestication and motivates the design of studies aimed at making links between genotype and phenotype. Rabbits exhibit exceptional phenotypic diversity, are of great commercial value, and serve as important animal models in biomedical research. Here, we provide the first comprehensive survey of nucleotide polymorphism and linkage disequilibrium (LD) within and among rabbit breeds. We resequenced 16 genomic regions in population samples of both wild and domestic rabbits and additional 35 fragments in 150 rabbits representing six commonly used breeds. Patterns of genetic variation suggest a single origin of domestication in wild populations from France, supporting historical records that place rabbit domestication in French monasteries. Levels of nucleotide diversity both within and among breeds were ~0.2%, but only 60% of the diversity present in wild populations from France was captured by domestic rabbits. Despite the recent origin of most breeds, levels of population differentiation were high (F(ST) = 17.9%), but the majority of polymorphisms were shared and thus transferable among breeds. Coalescent simulations suggest that domestication began with a small founding population of less than 1,200 individuals. Taking into account the complex demographic history of domestication with two successive bottlenecks, two loci showed deviations that were consistent with artificial selection, including GPC4, which is known to be associated with growth rates in humans. Levels of diversity were not significantly different between autosomal and X-linked loci, providing no evidence for differential contributions of males and females to the domesticated gene pool. The structure of LD differed substantially within and among breeds. Within breeds, LD extends over large genomic distances. Markers separated by 400 kb typically showed r(2) higher than 0.2, and some LD extended up to 3,200 kb. Much less LD was found among breeds. This advantageous LD structure holds great promise for reducing the interval of association in future mapping studies.

Prevalence of the MYBPC3-A31P mutation in a large European feline population and association with hypertrophic cardiomyopathy in the Maine Coon breed.

OBJECTIVES: The MYBPC3-A31P mutation has been identified in the USA in a colony of Maine Coon cats with an autosomal dominant hypertrophic cardiomyopathy (HCM). The objectives of this prospective study were: 1) to evaluate the prevalence of this mutation in a large feline population from Europe; 2) to compare these data with the prevalence of HCM in the Maine Coon breed. ANIMALS AND METHODS: 1) 3757 cats from different breeds including 2744 Maine Coon cats were screened for the mutation. 2) 164/2744 Maine Coon cats were subjected to echocardiography (Echo-Group, mean age = 2.6 years [0.3-11.5]). RESULTS: 1) In the whole study population, the mutation was only found in Maine Coon cats (prevalence = 41.5%), except for one British Longhair cat. 2) 55/164 (34%) cats from the Echo-Group carried the mutation while only 12/164 (7%; 5/48 heterozygous, 5/7 homozygous mutated, 2/109 homozygous wild-type cats) showed HCM. MYBPC3-A31P was associated with a significant increased risk of HCM (relative risk = 9.91). CONCLUSION: The MYBPC3-A31P mutation is highly prevalent in Maine Coon cats in Europe and appears to be breed specific with potential marginal events. Young unaffected mutated cats and affected homozygous wild-type cats illustrate the phenotypic and etiological heterogeneity of feline HCM, as demonstrated in humans.

Progressive retinal atrophy in the Border Collie: a new XLPRA.

BACKGROUND: Several forms of progressive retinal atrophy (PRA) segregate in more than 100 breeds of dog with each PRA segregating in one or a few breeds. This breed specificity may be accounted for by founder effects and genetic drift, which have reduced the genetic heterogeneity of each breed, thereby facilitating the identification of causal mutations. We report here a new form of PRA segregating in the Border Collie breed. The clinical signs, including the loss of night vision and a progressive loss of day vision, resulting in complete blindness, occur at the age of three to four years and may be detected earlier through systematic ocular fundus examination and electroretinography (ERG). RESULTS: Ophthalmic examinations performed on 487 dogs showed that affected dogs present a classical form of PRA. Of those, 274 have been sampled for DNA extraction and 87 could be connected through a large pedigree. Segregation analysis suggested an X-linked mode of transmission; therefore both XLPRA1 and XLPRA2 mutations were excluded through the genetic tests. CONCLUSION: Having excluded these mutations, we suggest that this PRA segregating in Border Collie is a new XLPRA (XLPRA3) and propose it as a potential model for the homologous human disease, X-Linked Retinitis Pigmentosa.

Taurine-deficient dilated cardiomyopathy in a family of golden retrievers.

A reversible taurine-deficient dilated cardiomyopathy occurred in five related golden retrievers. An apical systolic heart murmur was the most common physical abnormality. According to fractional shortening and end-systolic diameter on echocardiography, significant improvements (P<0.005) were recorded within 3 to 6 months of starting taurine supplementation. The dogs regained substantial systolic function, and four were weaned off all cardiac medications except taurine. This response to therapy was unusual, because canine dilated cardiomyopathy is generally progressive and fatal.

Integrative biology and genetic resources management.

Integrative Biology is exemplified by a diversity of recently established collaborations to study the genetic diversity of the European rabbit, Oryctolagus cuniculus. Molecular markers were developed and used to investigate the link between wild population decreases or domestication procedures and possible losses of genetic diversity. Simultaneously, a European programme was launched for the management of genetic resources. The Integrative Biology approach shows that changes in genetic diversity are often buffered by the flexibility of rabbit reproductive systems. It appears, also, that all domestic animals belong to a subset of the wild genetic pool of their species without major loss of diversity despite exposure to severe viral infections. Consequently, management of genetic resources for production purposes and conservation or protection of declining Iberian wild populations require different approaches and measures.