Stationary Distributions of Microsatellite Loci Between Divergent Population Groups of the European Rabbit (Oryctolagus cuniculus)

Previous analysis of mitochondrial DNA polymorphism in the nativerange of the European rabbit (Oryctolagus cuniculus) demonstratedthe occurrence of two highly divergent (2 Myr) maternal lineageswith a well-defined geographical distribution. Analysis of bothprotein and immunoglobulin polymorphisms are highly concordantwith this pattern of differentiation. However, the present analysisof nine polymorphic microsatellite loci (with a total of 169alleles) in 24 wild populations reveals severe allele-size homoplasywhich vastly underestimates divergence between the main groupsof populations in Iberia. Nonetheless, when applied to morerecent historical phenomena, this same data set not only confirmsthe occurrence of a strong bottleneck associated with the colonizationof Mediterranean France but also suggests a two-step dispersalscenario that began with gene flow from northern Spain throughthe Pyrenean barrier and subsequent range expansion into northernFrance. The strength and appropriateness of applying microsatellitesto more recent evolutionary questions is highlighted by thefact that both mtDNA and protein markers lacked the allelicdiversity necessary to properly evaluate the colonization ofFrance. The well-documented natural history of European rabbitpopulations provides an unusually comprehensive framework withinwhich one can appraise the advantages and limitations of microsatellitemarkers in revealing patterns of genetic differentiation thathave occurred across varying degrees of evolutionary time. Thedegree of size homoplasy presented in our data should serveas a warning to those drawing conclusions from microsatellitedata sets which lack a set of complementary comparative markers,or involve long periods of evolutionary history, even withina single species.     

Cryptosporidium cuniculus in the rabbit (Oryctolagus cuniculus)

Cryptosporidium cuniculus was identified by light and electron microscopy in two apparently healthy rabbits. Organisms were firmly attached at the brush borders of intestinal epithelial cells. Cellular alterations were minimal, consisting of elongation and shortening of microvilli adjacent to the attachment sites of organisms. Various developmental stages of cryptosporidium were identified by electron microscopy.     

Patterns of parasite aggregation in the wild European rabbit (Oryctolagus cuniculus)

Understanding the factors controlling the distribution of parasites within their host population is fundamental to the wider understanding of parasite epidemiology and ecology. To explore changes in parasite aggregation, Taylor's power law was used to examine the distributions of five gut helminths of the wild rabbit. Aggregation was found to be a dynamic process that varied with year, season, host sex, age class, and myxomatosis. Yearly and seasonal changes are thought, in the main, to be the result of variations in weather conditions acting upon infectious stages (or intermediate hosts). Evidence in support of this was the comparatively low degree of fluctuation in the aggregation of the pinworm, Passalurus ambiguus, as the infectious stage of this parasite is likely to be less susceptible to environmental variation. Host age had a marked effect on the level of aggregation of all parasites, but this effect varied between parasite species. P. ambiguus, Trichostrongylus retortaeformis and Cittotaenia denticulata aggregation were lower in adult than juvenile rabbits whilst Graphidium strigosum and Mosgovoyia pectinata aggregation tended to increase with age. Host immunity is thought to be responsible for these differences. Differences in aggregation for different parasites were also seen when the rabbit population was split into males and females. Myxomatosis had a marked effect on helminth distribution with substantially less aggregation in rabbits showing clinical signs of the disease.     

Rabbit Oryctolagus cuniculus populations in Scotland since the introduction of myxomatosis

A Rabbit survey of Scotland was carried out in 1991 following the methods used for previous surveys in 1969, 1970, 1973 and 1974. The survey was split into direct field and postal questionnaire sections, and the results from the two were compared. Rabbit infestations were categorized as slight and serious. Slight infestation proved to be an inconsistent indicator of Rabbits, but the percentage of serious infestations was highly correlated across sampling areas, and was also related to the average loss estimated by farmers. The pattern of recovery of Rabbit populations after myxomatosis varied between different parts of the country. In the East, Northeast and eastern Highlands the percentage of serious infestations was 26.5% in 1991, as compared to previous survey estimates of 55.9% before 1954 and 1.5% in 1969/70. In the Central, West, South and South-west serious Rabbit problems disappeared after 1954 and are now only at the level of 5 %. It is estimated that Rabbits caused £11,790,000 worth of damage to agriculture in Scotland during 1990/91.     

The burrow structure of the European rabbit (Oryctolagus cuniculus L.)

Samples of rabbit burrows were excavated and measured at four areas around Edinburgh. Of these, 31 burrows over 2 m long were analysed for internal structural relationships and the effect of soil composition and slope of the ground on their form. Seven variables were measured for each burrow—total length, number of entrance holes, number of junctions, number of ends, average length of sections between holes, junctions and ends, average depth and maximum depth. There are three main trends in burrow variation—size, an inverse relationship between relative number of holes and average depth, and an inverse relationship between average section length and relative number of junctions. Burrows in sand have relatively fewer holes and junctions, longer element lengths, a higher average depth and three times the enclosed volume per hole. Burrows dug into slopes have a higher average depth. Areas differed significantly in the relative number of holes and junctions, and average depth. It was concluded that an apparently complex structure could be summarized in terms of relatively few components. The chief of these, size, was largely independent of the soil and site characteristics, whereas the remaining two were dependent on the soil in which the burrow was dug. This may have implications for the ecology and behaviour of rabbits in different areas, and is relevant to the success of some rabbit control procedures such as burrow fumigation and warren ripping.     

High levels of nucleotide diversity in the European rabbit (Oryctolagus cuniculus) SRY gene

We have sequenced 2,388 bp of the European rabbit sex determining region Y (SRY) gene. These data provide a 10-fold increase in the coverage of the Y chromosome in this species, including the entire open reading frame of the SRY, the polyadenylation signal, and two repetitive sequences in the 5' -region. A survey of 2021 bp of this gene in eight domestic breeds and four wild individuals revealed a total of nine single nucleotide polymorphisms and one indel, defining two deeply divergent lineages. The resulting estimation of nucleotide diversity (pi=1.34 x10(-3)) is very high when compared with other species, but no variability was detected among the domestic breeds. This study represents a first step in the characterization of the European rabbit Y chromosome and its variability. These sequences can be used in additional phylogeographical analyses of the European rabbit and other Leporid species, as well as in evolutionary studies of sex determination and the Y chromosome in wild species.     

Recombination and Speciation: Loci Near Centromeres Are More Differentiated Than Loci Near Telomeres Between Subspecies of the European Rabbit (Oryctolagus cuniculus)

Recent empirical and theoretical studies suggest that regions of restricted recombination play an important role in the formation of new species. To test this idea, we studied nucleotide variation in two parapatric subspecies of the European rabbit (Oryctolagus cuniculus). We surveyed five loci near centromeres, where recombination is expected to be suppressed, and five loci near telomeres, where recombination is expected to be higher. We analyzed this multilocus data set using a divergence-with-gene flow framework and we report three main findings. First, we estimated that these subspecies diverged ~1.8 MYA and maintained large effective population sizes (O. c. algirus N_e ≈ 1,600,000 and O. c. cuniculus N_e ≈ 780,000). Second, we rejected a strict allopatric model of divergence without gene flow; instead, high rates of gene flow were inferred in both directions. Third, we found different patterns between loci near centromeres and loci near telomeres. Loci near centromeres exhibited higher levels of linkage disequilibrium than loci near telomeres. In addition, while all loci near telomeres showed little differentiation between subspecies, three of five loci near centromeres showed strong differentiation. These results support a view of speciation in which regions of low recombination can facilitate species divergence in the presence of gene flow.     

Fine-scale genetic structuring in a natural population of European wild rabbits (Oryctolagus cuniculus)

The genetic structure of a free-living tagged population of European wild rabbits (Oryctolagus cuniculus) was investigated for two consecutive years (1990 and 1991) using 10 polymorphic microsatellite loci. A specific social behaviour, the formation of stable breeding groups, influenced the genetic structure of the population. These breeding groups were shown to constitute genetically differentiated units with low levels of gene flow between them. The average relatedness among members of a social group was higher than within the population as a whole. As a result of female philopatry coupled with male-biased natal dispersal, the relatedness of females was higher than that of males, both within social groups and in the whole population. Furthermore, the average relatedness of females within groups was twice the relatedness of females between groups. This study reveals marked fine-scale, intrapopulation genetic structure, which is attributable to the social behaviour of the European wild rabbit.     

The effect of oral l-carnitine on lipoprotein composition in the Watanabe Heritable Hyperlipidemic Rabbit (Oryctolagus cuniculus)

1. We have recently reported the ability of orally administered l-carnitine to lower plasma triglyceride in the Watanabe Heritable Hyperlipidemic Rabbit (WHHL), an animal model of familial hyperlipoproteinemia. 2. In the present studies we examined the effect of l-carnitine administration upon individual lipoprotein subfractions in this animal model. 3. Carnitine feeding resulted in a reduction in very low density lipoproteins (VLDL) and high density lipoprotein (HDL). 4. Compositional analysis revealed a reduction in core triglyceride content with a concomitant increase in protein and phospholipid in VLDL and low density lipoproteins (LDL). 5. Conversely, electrophoretic mobility and apolipoprotein composition were unchanged with l-carnitine. 6. These results further demonstrate the ability of l-carnitine to modulate lipoprotein lipid composition in this animal model of familial hyperlipoproteinemia.     

Extensive Genetic Polymorphism of Peptidases A, B, C, and D, in Wild Rabbit (Oryctolagus cuniculus) Populations from the Iberian Peninsula

Genetic polymorphism of peptidases A, B, C, andD in the wild rabbit (Oryctolagus cuniculus)was assessed by horizontal starch gel electrophoresis,in a total of 1003 individuals comprising 16 Iberian and 2 French populations and 1 domestic stock.Twenty-five different alleles were detected: 6 in PEPA,4 in PEPB, 8 in PEPC, and 7 in PEPD. The highest valuesof observed heterozygosity averaged over the four loci were obtained for the southwestern Iberianpopulations and a clinal loss of variability in anortheastern direction was detected. A clear separationbetween the two putative subspecies O. c.cuniculus and O. c. algirus was notobtained.     

Coccidiosis of the wild rabbit (Oryctolagus cuniculus) in France

In 1998-1999 a survey of coccidiosis in wild rabbits was carried out in six different localities in France. About five individuals were caught monthly in each locality and a total of 254 wild rabbits was examined. Ten species of Coccidio were identified: Eimeria perforans, E. flavescens, E. piriformis, E. exigua, E. media, E. magna, E. coecicola, E. stiedai, E. roobroucki, E. intestinalis. Intensity of infection in young individuals was higher than in adults. Intensity was highest in winter but, as there are no young rabbits in winter, in young individuals it was higher in spring and autumn than in summer. Intensities were higher in the northern rather than in southern localities. Ranking of prevalence was remarkably stable, in contrast to the variability of the parasitic load. The equilibrium between congeneric species of rabbit coccidia (stable prevalence rank, variable parasitic load) is thought to be probably the consequence of the opportunistic feeding habits of rabbits.     

Natal dispersal and genetic structure in a population of the European wild rabbit (Oryctolagus cuniculus)

A combination of behavioural observation, DNA fingerprinting, and allozyme analysis were used to examine natal dispersal in a wild rabbit population. Rabbits lived in territorial, warren based social groups. Over a 6-year period, significantly more male than female rabbits moved to a new social group before the start of their first breeding season. This pattern of female philopatry and male dispersal was reflected in the genetic structure of the population. DNA fingerprint band-sharing coefficients were significantly higher for females within the same group than for females between groups, while this was not the case for males. Wrighfs inbreeding coefficients were calculated from fingerprint band-sharing values and compared to those obtained from allozyme data. There was little correlation between the relative magnitudes of the F-statistics calculated using the two techniques for comparisons between different social groups. In contrast, two alternative methods for calculating F_ST from DNA fingerprints gave reasonably concordant values although those based on band-sharing were consistently lower than those calculated by an ‘allele’ frequency approach. A negative F_IS value was obtained from allozyme data. Such excess heterozygosity within social groups is expected even under random mating given the social structure and sex-biased dispersal but it is argued that the possibility of behavioural avoidance of inbreeding should not be discounted in this species. Estimates of genetic differentiation obtained from allozyme and DNA fingerprint data agreed closely with reported estimates for the yellow-bellied marmot, a species with a very similar social structure to the European rabbit.     

Helminths of the wild rabbit (Oryctolagus cuniculus) in Macaronesia

Two hundred and four rabbits from 8 Macaronesian islands (Pico, San Jorge, San Miguel, Terceira, and Flores from Azores Archipelago; Tenerife and Alegranza from Canary Islands; and Madeira from Madeira Archipelago) were examined for helminth parasites between 1995 and 2000. Three species of cestodes, Taenia pisiformis (larvae), Andrya cuniculi, and Mosgovoyia ctenoides, and 5 species of nematodes, Trichuris leporis, Graphidium strigosum, Trichostrongylus retortaeformis, Passalurus ambiguus, and Dermatoxys hispaniensis, were identified. Only 3 species (M. ctenoides, T. retortaeformis, and P. ambiguus) were regularly distributed over the 3 archipelagos. Taenia pisiformis was not collected in Madeira, nor was A. cuniculi in the Azores and G. strigosum in the Canary Islands. Trichuris leporis and D. hispaniensis were only found in Madeira. Significant differences in the general prevalence of the nematodes G. strigosum and T. retortaeformis were detected between Azores and Madeira. The prevalence of T. retortaeformis differs significantly between the Azores and the Canaries and that of P. ambiguus was higher in Madeira than in Azores and Canaries. The helminth richness found in the wild rabbit in these Macaronesian archipelagos was very low compared with the Palearctic helminth fauna of this host. The wild rabbit was introduced from the Iberian Peninsula into different Macaronesian islands. Helminths introduced with Oryctolagus cuniculus into these islands also are commonly found in Iberian wild rabbits, which are excellent colonizers, as demonstrated in this study.