Genetic lineages of feral populations of the Oryctolagus
cuniculus (Leporidae, Lagomorpha) in Argentina
Never A. Bonino1,* and Ramón C. Soriguer2
Estación Experimental Bariloche, Instituto Nacional
de Tecnologı́a Agropecuaria, Casilla de Correo 277,
8400 Bariloche, Rı´o Negro, Argentina,
e-mail: nbonino@bariloche.inta.gov.ar
2
Estación Biológica Doñana, Consejo Superior de
Investigaciones Cientı́ficas, Avda Marı´a Luisa s/n,
Pabellón Perú, 41013 Sevilla, España
1
* Corresponding author
Keywords: European rabbit; genetic; introduced
species; mitochondrial DNA; Patagonia.
Both wild and domestic European rabbit belong to the
single species Oryctolagus cuniculus, which is the sole
extant representative of the genus Oryctolagus (Chapman and Flux 1990, Wilson and Reeder 2005). Two subspecies are recognized, O.c. algirus and O.c. cuniculus;
they are well differentiated with respect to mtDNA (Branco et al. 2000), the Y chromosome (Geraldes et al. 2005)
and some allozyme loci (Ferrand and Branco 2006).
When judged only on their mitochondrial DNA, 22 different rabbit haplotypes are recognized and organized into
two very divergent maternal lineages named A (corresponding to O.c. algirus) and B (corresponding to O.c.
cuniculus). And within each lineage, there sublineages
that are geographically substructure. Lineage A is found
in the south-west of the Iberian Peninsula. Lineage B is
distributed throughout the rest of Europe (including
northern Spain), and in most populations introduced to
other regions of the world (Ennafaa et al. 1987, BijuDuval et al. 1991, Monnerot et al. 1994). A clear subdivision into two groups was also found when nuclear
genes were studied (Van der Loo et al. 1991, 1999) with
a geographical distribution that largely coincides with
that of the mitochondrial clades A and B. Rabbits of both
lineages are very similar in their external appearance,
although B lineage animals are somewhat larger (Rogers
et al. 1994). All domestic rabbits belong to this B lineage,
i.e., to subspecies O.c. cuniculus (Monnerot et al. 1996).
The European rabbit has been introduced in different
regions of the world including Asia, Australia, New Zealand, and North and South America (Flux 1994). In this
last continent, rabbits were first introduced into several
regions of Chile from which they invaded the southwestern region of Argentina (Howard and Amaya 1975, Zunino
1989). In Argentina, the rabbits are now present in three
regions (Figure 1): 1) Tierra del Fuego Province, 2) Santa
Cruz Province and 3) Mendoza-Neuquén Provinces.
1) Tierra del Fuego Province: according to Jaksic and
Yañ ez (1983), the first introduction was made about 1880
onto a number of islands in the Beagle Channel. The
original stock of these Channel animals came from the
Falkland Islands, onto which rabbits had been introduced
by the French prior to 1765. Some of these rabbits were
set free around 1936 on the Chilean side of Tierra del
Fuego, and around 1950 more were released on the
Argentinan side of this island (Arentsen 1954, Goodall
1979). 2) Santa Cruz Province: in 1985 the rabbits were
detected at the southwestern edge of this province
(Clarke and Amaya 1986). Presumably they come from
nearby Puerto Natales (Chile), where several animal
(apparently originating from Tierra del Fuego) were
released in 1970 (A. Iriarte Walton, personal communication). 3) Mendoza-Neuqué n Provinces: in 1945 the
rabbits were first reported in these provinces. They originated from animals that crossed through low passes in
the Andean Cordillera from adjacent parts of central
Chile. These central Chilean rabbits are of Spanish origin
and had been introduced at the beginning of the 20th
century (Greer 1965, Howard and Amaya 1975). Within
these two provinces, the rabbit is currently undergoing a
process of dispersion and invasion of new areas (Bonino
and Gader 1986, Bonino and Soriguer 2004).
Therefore, rabbits inhabiting the southernmost two
regions of Argentina are likely to be of French origin,
whereas rabbits of the third northern region are likely to
be of Spanish origin. Therefore, we studied the mitochondrial DNA of rabbits of these introduced populations
to identify the maternal lineages.
A total of 64 rabbits were shot in the three geographic
areas where there are wild populations of European rabbit in Patagonia. The geographic locations of the populations sampled are shown in Figure 1 and collecting
localities are given in Table 1. A portion of liver or muscle
tissue was taken from freshly killed animals and stored
in 70% ethanol. Total DNA was obtained following the
method described by Rico et al. (1992) and used directly
for amplification. Rapid discrimination between mtDNA
haplotypes was carried out using diagnostic sites in two
mtDNA fragments (565 bp from the cytochrome b gene
digested with AluI and 586 bp from the non-coding
region, digested with RsaI) according to Mougel (1997).
According to the mtDNA typing, all rabbit populations
inhabiting Argentina belonged to the B lineage: rabbits of
Tierra del Fuego and Santa Cruz Provinces had the B3
haplotype and those in Neuqué n Province had the B1
haplotype (Table 1).
Note that the rabbits of Tierra del Fuego and Santa
Cruz (of putative French origin) displayed the B3 haplotype. This haplotype is currently uncommon in France,
provinces (Amaya and Bonino 1981). Another possibility
is that the initial introductions of rabbits into the Falkland
Islands and central Chile were animals from the domestic
breeds in existence in France and Spain approximately
250 years ago. To test these two hypotheses about the
degree of domestic strain versus wild-European genes in
the Argentine populations of the rabbit, we are planning
to re-examine our samples using more variable and
informative markers at microsatellite loci (Queney et al.
2001).
Acknowledgements
This paper is dedicated in memoriam to Francisco Barrera
(nuestro amigo Paco) deceased in Sierra Nevada in a tragic accident during a rescue practice work. We are grateful to R. Clarke
and F. Barrera Sanchez (†) for their assistance in the field and
to R.D. Sage, E. Donadio, and anonymous reviewers that helped
us to improve the final manuscript. Fieldwork was funded by the
Programa de Cooperación Cientı́fica con Iberoamérica (AECI)
and the Consejo Nacional de Investigaciones Cientı́ficas y Té cnicas (CONICET PIP 937).
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Figure 1 Geographic distribution (shading area) of the European rabbit in Argentina. The number indicates the collection
sites and these are specified in Table 1. The insert shows (in
black) the southwestern part of Argentina under discussion in
the text and in the larger section of this Figure.
Table 1 Collection sites, sample sizes, and mitochondrial DNA
typing of rabbits collected in the different areas of the European
rabbit distribution in Argentina.
Collection sites
Sample
sizes
Haplotype
1. Estancia Túnel
(548579390 S, 688299250 W)
2. Rı́ o Turbio
(518359360 S, 728219380 W)
3. Andacollo
(378109550 S, 708409310 W)
4. Junı́n de los Andes
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5. Lago Ñorquinco
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6. Paso de los Indios
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7. Sauzal Bonito
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15
B3
15
B3
6
B1
3
B1
15
B1
3
B1
7
B1
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