Rafael Villafuerte

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

Rabbits softly swept to domestication When people domesticate animals, they select for tameness and tolerance of humans. What else do they look for? To identify the selective pressures that led to rabbit domestication, Carneiro et al. sequenced a domestic rabbit genome and compared it to that of its wild brethren (see the Perspective by Lohmueller). Domestication did not involve a single gene changing, but rather many gene alleles changing in frequency between tame and domestic rabbits, known as a soft selective sweep. Many of these alleles have changes that may affect brain development, supporting the idea that tameness involves changes at multiple loci. Science, this issue p. 1074; see also p. 1000 The domestication of rabbits primarily shifted the frequencies of alleles represented, rather than creating new genes. [Also see Perspective by Lohmueller] 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.

Traditional management of scrubland for the conservation of rabbits Oryctolagus cuniculus and their predators in Doñana National Park, Spain

Several endangered carnivores and raptors in Mediterranean Spain are very dependent on rabbits Oryctolagus cuniculus, which have shown a progressive decline in abundance for several decades. Land use neglect, and the consequent abandonment of traditional land use methods such as burning, is considered one of the factors responsible for this decrease. To examine this hypothesis we have compared rabbit use of experimentally burned and unburned scrubland areas. Rabbit activity was found to be significantly higher in burned areas, with the greatest use in less productive habitats in close proximity to scrub cover. The promotion of traditional land practices for nature conservation in the natural ecosystems of the Mediterranean Basin is discussed.

First epizootic of rabbit hemorrhagic disease in free living populations of Oryctolagus cuniculus at Doñana National Park, Spain

The first known epizootic of rabbit hemorrhagic disease (RHD) occurred in two free-living wild rabbit (Oryctolagus cuniculus) populations at Doñana National Park, Spain. Rabbit population density was not correlated to RHD mortality. Only adult animals were affected; males and females had similar mortality rates.

HABITAT-RELATED DIFFERENCES IN RABBIT (ORYCTOLAGUS CUNICULUS) ABUNDANCE, DISTRIBUTION, AND ACTIVITY

Abstract The European rabbit (Oryctolagus cuniculus) is a key prey species in Mediterranean ecosystems and is ecologically plastic. However, ecological responses of rabbits to different habitats are poorly understood. We present data on abundance, distribution, activity, and survival in 3 neighboring habitats in southwestern Spain differing in refuge and forage availability. Scrubland presents dense cover but low forage abundance; grassland offers little protective vegetation but high food availability; the ecotone provides intermediate levels of both resources. Rabbits reached the highest abundance in ecotone, whereas low food and refuge availability seemed to limit their abundance in scrubland and grassland, respectively. In scrubland, rabbits were dispersed among the cover. In grassland, rabbits were linked to aggregated burrows. In ecotone, rabbits dug burrows in the bordering bushes that abutted grassy feeding pasture. Predation by raptors was low in scrubland, and mortality due to mammalian carnivores was higher in spite of more diurnal rabbit activity. Carnivore predation also caused higher mortality in grassland, where rabbits were more nocturnal. In ecotone, the effect of both mammalian carnivores and raptors on rabbits was similar. Mortality by disease seemed to be linked to level of rabbit aggregation.

Rabbit populations and game management: the situation after 15 years of rabbit haemorrhagic disease in central-southern Spain

Over recent decades wild rabbit populations have undergone a sharp decline in Spain with consequent negative impact both on a game-based economy, and on the conservation of threatened species that depend on rabbits. We investigated the relationships between rabbit population change and habitat and game management in central-southern Spain. To determine recent rabbit population changes we revisited 60 localities during summer 2002 to repeat surveys previously carried out in 1993. Each survey consisted of 4-km walked transects to record indices of rabbit abundance. The percentage of vegetation cover and of different soil types were also estimated during these transects. In the same areas, the type and intensity of game management practices were obtained by interviewing hunting managers, hunters or gamekeepers. Rabbit populations were stable or increasing only in 26.6% of the studied populations, more commonly in areas with soft soils where warren building is easier for rabbits and where rabbits were an important game species and managed to increase their numbers. Although we could not establish causality, habitat management and predator removal were the main management practices related to rabbit population change. Rabbit scarcity in Spain constitutes a serious problem for conservation, so hunters, researchers and policy makers need to reach a consensus to establish a long-term program to monitor rabbit population trends and share results obtained, especially when intense manage programs are being carried out to improve rabbit abundance.

Habitat related differences in helminth parasites of red foxes in the Ebro valley.

The prevalences of helminth parasites found on red foxes collected in two different habitats of the Ebro Valley, in north-eastern Spain were compared. Twenty helminth species, including one trematode, six cestodes, 12 nematodes and one acanthocephalan were found. Metorchis albidus, Uncinaria stenocephala and Dirofilaria immitis were more prevalent in the irrigated lands close to the main rivers of the study area, whereas Trichuris vulpis and Pterygodermatites affinis showed higher prevalences in the semiarid stepparian habitat. Habitat characteristics need to be considered when surveying helminths over large geographical areas. The study shows that in the Ebro Valley the fox constitutes a reservoir host for several helminth species that are parasites of the domestic dog or the wolf, or may have importance as zoonoses.

A Comparison of Brain Gene Expression Levels in Domesticated and Wild Animals

Domestication has led to similar changes in morphology and behavior in several animal species, raising the question whether similarities between different domestication events also exist at the molecular level. We used mRNA sequencing to analyze genome-wide gene expression patterns in brain frontal cortex in three pairs of domesticated and wild species (dogs and wolves, pigs and wild boars, and domesticated and wild rabbits). We compared the expression differences with those between domesticated guinea pigs and a distant wild relative (Cavia aperea) as well as between two lines of rats selected for tameness or aggression towards humans. There were few gene expression differences between domesticated and wild dogs, pigs, and rabbits (30–75 genes (less than 1%) of expressed genes were differentially expressed), while guinea pigs and C. aperea differed more strongly. Almost no overlap was found between the genes with differential expression in the different domestication events. In addition, joint analyses of all domesticated and wild samples provided only suggestive evidence for the existence of a small group of genes that changed their expression in a similar fashion in different domesticated species. The most extreme of these shared expression changes include up-regulation in domesticates of SOX6 and PROM1, two modulators of brain development. There was almost no overlap between gene expression in domesticated animals and the tame and aggressive rats. However, two of the genes with the strongest expression differences between the rats (DLL3 and DHDH) were located in a genomic region associated with tameness and aggression, suggesting a role in influencing tameness. In summary, the majority of brain gene expression changes in domesticated animals are specific to the given domestication event, suggesting that the causative variants of behavioral domestication traits may likewise be different.

Epidemiology of viral haemorrhagic disease and myxomatosis in a free-living population of wild rabbits

From January 1993 to June 1996, the epidemiology of myxomatosis and viral haemorrhagic disease (VHD) was studied in a free-living population of wild rabbits (Oryctolagus cuniculus) in Spain by means of serological surveys and radiotracking. Myxomatosis was endemic and associated with the breeding period. Its serological pattern was characterised by a 100 per cent prevalence of antibodies in adult rabbits and a rapid increase in antibodies in young rabbits in their first year. No mortality from myxomatosis was detected in adults, and mortality in young rabbits could not be estimated because of interference by predators and scavengers and the deaths of many radiotagged rabbits inside their burrows. VHD was also an endemic disease associated with the breeding period. Adults had a higher prevalence of antibodies against VHD than young rabbits, teaching values of 80 to 90 per cent. During the study, there was an increase in rabbit numbers as a result of a decrease in mortality from predation which was associated with an increase in mortality due to VHD and in the prevalence of antibodies to VHD. Mortality from VHD was lower in rabbits with VHD antibodies than in seronegative rabbits, but some mortality from the disease was also detected in seropositive rabbits. The annual mean mortality rate due to VHD in adult rabbits was estimated to be 21.8 per cent

Modelling hunting strategies for the conservation of wild rabbit populations

Recently, European wild rabbit (Oryctolagus cuniculus) populations have undergone a sharp decline that may be exacerbated by hunting. We investigate the effects of the timing of hunting on the conservation of wild rabbit using a model for rabbit population dynamics. Scenarios with different hunting rates and age strategies were simulated for different population qualities. We interviewed hunters to ascertain the degree to which they would accept a change in the timing of hunting. We also investigated the hunting pressure applied by hunters and its relationship with rabbit abundance. Modelling results indicate that the current hunting season has the greatest impact on rabbit abundance. Hunting in late spring optimises hunting extraction while conserving rabbit populations. When the rabbit population quality is low the effects of age strategies and the timing of hunting are less important than the effect of the hunting rate applied. Almost half the hunters would agree to policy changes. More than 75% of hunters implemented self-imposed hunting restrictions to improve rabbit populations, that were more frequently applied in high rabbit abundance areas. Therefore, changing the timing of hunting and increasing the participation of hunters in low abundance areas could optimise both the exploitation and the conservation of wild rabbit populations in southwestern Europe.

The genomic architecture of population divergence between subspecies of the european rabbit

The analysis of introgression of genomic regions between divergent populations provides an excellent opportunity to determine the genetic basis of reproductive isolation during the early stages of speciation. However, hybridization and subsequent gene flow must be relatively common in order to localize individual loci that resist introgression. In this study, we used next-generation sequencing to study genome-wide patterns of genetic differentiation between two hybridizing subspecies of rabbits (Oryctolagus cuniculus algirus and O. c. cuniculus) that are known to undergo high rates of gene exchange. Our primary objective was to identify specific genes or genomic regions that have resisted introgression and are likely to confer reproductive barriers in natural conditions. On the basis of 326,000 polymorphisms, we found low to moderate overall levels of differentiation between subspecies, and fewer than 200 genomic regions dispersed throughout the genome showing high differentiation consistent with a signature of reduced gene flow. Most differentiated regions were smaller than 200 Kb and contained very few genes. Remarkably, 30 regions were each found to contain a single gene, facilitating the identification of candidate genes underlying reproductive isolation. This gene-level resolution yielded several insights into the genetic basis and architecture of reproductive isolation in rabbits. Regions of high differentiation were enriched on the X-chromosome and near centromeres. Genes lying within differentiated regions were often associated with transcription and epigenetic activities, including chromatin organization, regulation of transcription, and DNA binding. Overall, our results from a naturally hybridizing system share important commonalities with hybrid incompatibility genes identified using laboratory crosses in mice and flies, highlighting general mechanisms underlying the maintenance of reproductive barriers.