Esther Ramírez

Translocations as a risk for the conservation of European wild rabbit Oryctolagus cuniculus lineages

Population units that merit separate management and are of conservation concern have been called evolutionary significant units. Two divergent lineages of the European rabbit Oryctolagus cuniculus occur naturally in Spain, with a well-marked geographical distribution. We analysed the frequency and importance of rabbit translocations in central-southern Spain and whether this practice, carried out by hunters and conservationists, could cause the mixture of two clearly different evolutionary significant units. We carried out interviews in 1993 and 2002 at 60 locations to determine the presence and intensity of translocations during both decades. The distribution of the lineages was obtained using mtDNA analysis of hunted rabbits in 2003-2005. We demonstrate that rabbit translocation was used frequently in the 1980s and increased in the 1990s. Up to 43% of the studied areas translocated rabbits in the latter decade, whereas only 25% did so in the 1980s. Our results show that neither the origin of the introduced rabbits nor their genetic lineage were taken into account in most of the translocations. We found rabbits of lineage A in several localities within the distribution area of lineage B, and vice versa, probably as a consequence of translocations. The distribution of both lineages is likely to have been altered by human activity and this could represent the loss of the results of 2 million years of genetic differentiation with possible attendent ecological consequences. Consequently, authorities should more closely regulate rabbit translocations and convey to both hunters and conservationists the importance of not mixing the lineages by translocations.

Steep clines within a highly permeable genome across a hybrid zone between two subspecies of the European rabbit

Maintenance of genetic distinction in the face of gene flow is an important aspect of the speciation process. Here, we provide a detailed spatial and genetic characterization of a hybrid zone between two subspecies of the European rabbit. We examined patterns of allele frequency change for 22 markers located on the autosomes, X‐chromosome, Y‐chromosome and mtDNA in 1078 individuals sampled across the hybrid zone. While some loci revealed extremely wide clines (w ≥ 300 km) relative to an estimated dispersal of 1.95–4.22 km/generation, others showed abrupt transitions (w ≈ 10 km), indicating localized genomic regions of strong selection against introgression. The subset of loci showing steep clines had largely coincident centers and stepped changes in allele frequency that did not co‐localize with any physical barrier or ecotone, suggesting that the rabbit hybrid zone is a tension zone. The steepest clines were for X‐ and Y‐chromosome markers. Our results are consistent with previous inference based on DNA sequence variation of individuals sampled in allopatry in suggesting that a large proportion of each genome has escaped the overall barrier to gene flow in the middle of the hybrid zone. These results imply an old history of hybridization and high effective gene flow and anticipate that isolation factors should often localize to small genomic regions.

Field experimental vaccination campaigns against myxomatosis and their effectiveness in the wild.

We conducted a field experiment in SW Spain to test the efficacy of a myxomatosis vaccine, a viral disease strongly affecting wild rabbit populations, by assessing individual survival and antibody seroprevalence of monthly live-trapped, vaccinated (N=466) and unvaccinated (N=558) juvenile wild rabbits, between April and October 2007. Eight percent of all juveniles caught from April to June showed maternal antibodies against myxomatosis, whereas all animals were seropositive to the disease after the outbreak. Juveniles vaccinated before the outbreak showed 17% higher survival (31% vs. 14%) and an increased mortality probability of 8% after the outbreak. Results suggest that only a costly and systematic vaccination performed before the annual myxomatosis outbreak, would improve the survival of juvenile rabbits, a premise not always accomplished that compromises its efficacy in the field.

Establishing a serological surveillance protocol for rabbit hemorrhagic disease by combining mathematical models and field data: implication for rabbit conservation

Rabbit hemorrhagic disease (RHD) became endemic in wild rabbit (Oryctolagus cuniculus) populations in the Iberian Peninsula after its first arrival in 1988. This had significant implications for both the economy and environmental conservation because rabbits are one of the main game species in the Iberian Peninsula and a keystone species in the Mediterranean ecosystems. As a consequence, it is planned to include RHD surveillance in the Spanish Wildlife Disease Surveillance Strategy. Nevertheless, there is no practical methodology included in this program to help conservationists and gamekeepers understand the impact of disease on wild rabbit populations. Results from sera collected during the hunting season from 11 rabbit populations of Central and South Spain, which differed in their population abundance and trends, allowed us to use mathematical models to interpret the serological results gathered and determine the best strategy for finalizing a plan of RHD surveillance. Put simply, we focused our field surveys within the hunting season (October-January), and those times when the rabbit populations are at their highest (June or July). Field results showed that both rabbit abundance and population trend are closely related to the prevalence of RHD antibodies when rabbit abundance was at its annual low point (usually October-November). Rabbit population trends were positive only if antibody prevalence was high (>40%), and always negative if prevalence was low. Moreover, rabbit populations where abundance was low always showed low antibody prevalence. Since our models predicted a low variability in the prevalence obtained during the hunting season, it is suggested that future serological surveys should be carried out within this period to avoid problems related to the low sample size in low density rabbit populations.

Large-scale assessment of myxomatosis prevalence in European wild rabbits (Oryctolagus cuniculus) 60 years after first outbreak in Spain

Myxomatosis is a viral disease that affects European rabbits (Oryctolagus cuniculus) worldwide. In Spain, populations of wild rabbits drastically decreased in the 1950s after the first outbreak of myxomatosis. Since that first appearance, it seems to be an annual epizootic in Spain with periodic outbreaks, predominantly in summer and autumn. Taking into account rabbit population structure, abundance, and genetic lineage, this paper attempts to make a large-scale characterization of myxomatosis seroprevalence based on the immune status of 29 rabbit populations distributed throughout Spain, where O. cuniculus cuniculus and O. c. algirus, the two known rabbit subspecies, naturally inhabit. A total of 654 samples were collected between 2003 and 2009, and seroprevalence of antibodies against Myxoma virus (MYXV) was determined. Overall, our results revealed that 53% of the rabbit samples were positive to antibodies against MYXV. Newborn and juvenile rabbits were the most susceptible animals to the virus, with 19% and 16% seropositivity for newborn and juveniles, respectively, while adult rabbits were the most protected, with 65% of seropositive samples. This suggests that prevalence is negatively related to the proportion of newborn and juvenile rabbits in a population. Our results also showed that seroprevalence against MYXV tended to be higher in high-abundance populations. In contrast, no differences were detected in seroprevalence between rabbit subspecies. This study confirms that >60years since first outbreak, myxomatosis is an endemic disease in Spain. Based on the results, the establishment of a myxomatosis surveillance protocol is proposed.