Journal of Heredity Advance Access originally published online on January 13, 2005
Journal of Heredity 2005 96(2):89-96; doi:10.1093/jhered/esi021
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European Mink–Polecat Hybridization Events: Hazards From Natural Process?
From the Laboratoire d'écologie animale, UMR Paysages & Biodiversité, Université d'Angers, Faculté des Sciences, Belle Beille, 49045 Angers cedex, France (Lodé); Communauté de Communes de Haute-Saintonge, 17 Jonzac, France Guiral); and Laboratoire de génétique, Université d'Angers, Faculté des Sciences, Belle Beille, 49045 Angers cedex, France (Peltier).
Address correspondence to T. Lodé at the address above, or e-mail: thierry.lode{at}univ-angers.fr.
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Abstract |
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Determining the significance of hybridization events raises essential issues both in conservation and in evolutionary biology. Here, we report a genetic investigation of sympatric polecat and endangered European mink populations. Although the two species were morphologically very similar, the European mink and the polecat were easily discriminated from allozymes and microsatellites and showed a high level of private alleles (effective number of alleles: mink=1.45 and polecat=3.09). Nevertheless, the allozymic polymorphism remained lower in the European mink (4 loci, 10.5%) than in polecat (9 loci, 23.7%). Similarly, from microsatellite data, the polymorphism only reached 36% at 0.99 in the European mink; whereas in the polecat, the polymorphism reached 82% at 0.99. Natural hybridization events between two native species were detected. Because of the low fertility of hybrids, interbreeding could be regarded as producing "hybrid sink" that leads to a progressive assimilation of mink by polecat. Nonetheless, pure mink populations inhabited streams in western France, and hybridization events were only detected in areas where mink were rare and now presumed disappeared. Rather than revealing the poor efficiency of the specific recognition system, our results suggest that hybridization is associated with the scarcity of mating partners.
Documenting patterns of gene exchange between species has received growing interest as evolutionary biologists recognized that hybridization provides an exceptional set of problems to investigate reproductive isolation (Arnold et al. 1999). Hybridization may demonstrate the low efficiency of the specific mating recognition system (SMRS) (Paterson 1993; Randler 2002), illustrating incomplete sexual isolation, and may lead to considerable evolutionary changes (Grant and Grant 1994; Arnold et al. 1999). Mixing genes from different species may alter evolutionary processes and change the speed of speciation between two taxa (Arnold 1997; Grant and Grant 1994; Dowling and Secor 1997; Stone 2000). Moreover, hybridization may have dramatic effects for rare species living in sympatry with common species, especially after human-induced introductions (O'Brien and Mayr 1991; Rhymer and Simberloff 1996; Allendorf et al. 2001). When native and introduced species hybridize, the conservation of native species implies developing a plan for preventing such hybridization (Crozier 1997). Hybridization events may result in sterile offspring because of the incompatibility of genes or enzyme systems inherited from two dissimilar species. With or without introgression, such hybridization, especially after human-induced introductions, has produced the decline or the extinction of numerous native species (Rhymer and Simberloff 1996; Allendorf et al. 2001). When mating occurs with individuals from closely related species, hybridization may not result in the entire sterility of hybrids. Usually, the mechanism leads to low hybrid fitness, but such fertile crosses between genetically distinct animals present two main concerns. First, when native and introduced species hybridize, the rare species may be particularly affected by alien genes jeopardizing the genetic pool (Sillero-Zubiri et al. 1996; Vila and Wayne 1999); and, secondly, hybridization may entail outbreeding depression (Frankham et al. 2002). Hybridization may not allocate the particular set of genes allowing the survival in a specific environment, a process known as outbreeding depression (Templeton 1989; Thornhill 1993; Storfer 1999; Frankham et al. 2002). Furthermore, populations with a small effective size are highly vulnerable to genetic depletion (Frankham et al. 2002).
While a large consideration for biological conservation has been devoted to anthropogenic incidental hybridization (Allendorf et al. 2001; Frankham et al. 2002), natural hybridization raises controversial concerns. Natural hybridization may be regarded as a natural component of the evolutionary process of related species (Arnold 1992; DeMarais et al. 1992; Arnold et al. 1999). Nevertheless, the conservation of native pure populations should be addressed when a relatively widespread species can hybridize with a rare threatened species such as the endemic European mink Mustela lutreola, which had a recent history of population bottleneck (Maran and Henttonen 1995; Maran et al. 1998; Lodé 1999). The European polecat M. putorius remained a widespread species in western Europe, although showing declining populations this species is now regarded as vulnerable. The European mink is considered as one of the most endangered species, and the western population of European mink showed a severe demographic decline (Lodé et al. 2001), with the current distribution being affected by watercourse quality and riparian habitat (Lodé 2002, Zabala et al. 2003). Allendorf et al. (2001) mentioned that potential hybridization with the introduced American mink M. vison has accelerated the decline of the European mink. But in western France, European mink had been declining several years before the feral American mink colonized watercourses (Lodé et al. 2001). European mink and polecats are closely related mustelids, which may be regarded as sympatric sister species (Sato et al. 2003). The dark phenotype of polecat shows a morphological convergence with the European mink (Lodé 2001a). Both species, called "water-polecats" by hunters, are often misidentified in the wild. European mink-polecat hybridization events could be regarded as a natural process concerning two sympatric native uncommon species questioning the significance of hybridization in the local extinction process. The evolutionary consequences of such natural events raise considerable issues regarding both outbreeding, the adaptive value of hybridization, and specific reproductive isolation.
We examined genetic variations between individuals morphologically identified as polecat or mink, both within a sympatric area and outside this area. Investigating natural hybridization events in two native species, our goal is: (1) to identify which alleles could be diagnostic between the two species and (2) to estimate the level of effective hybridization in sympatric populations.
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Materials and Methods |
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Frequency of Hybridization Events
We performed a capture design, carried out on the Seugne River and adjacent watercourses (Haute-Saintonge), between 1999 and 2002 to assess the hybridization rate between the European mink and the polecat, which breed sympatrically in this area (Figure 1). This area may be regarded as the current north range of the European mink's western population after the mink decline from northwestern France (Lodé et al. 2001); only polecats are widespread outside this area. Although, as top predators, carnivores are generally found in low densities even in optimal conditions, both polecats and European mink were commonly found on the Seugne River, and the Haute-Saintonge may be one of the main mink subpopulations in the world (Lodé and Peltier 2004). Furthermore, this area should be considered as a contact zone. A total of 70 wire-mesh traps were placed every 75–100 m in two lines along a 5–6 km stretch of river for 20 consecutive nights. Live-trapping sessions were carried out 17 times (every three months) in the same study zones, totaling 75 km of riverbank-side. Field data included sex, age, weight, date, and location of capture. A total of 35 European mink were live-trapped, and the animals were released. For genetic studies, a sample of hair was removed from 19 mink. Although dark polecats and mink can be discriminated by the length of the guard hair (<23 mm in European mink, >35mm in polecat), genetic analysis is often required in numerous cases. Both European mink and polecat start breeding at one year old, in the spring following their birth.
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Genetic Determination
We investigated genetic variations in 51 European mink and 126 polecats. Crude proteins and DNA extracts were obtained from tissue samples of 32 road-killed mink and 114 polecats opportunistically sampled from the Vendée to the Pyrenees, France. In addition, we analyzed DNA from hair of 19 live-trapped individuals regarded as mink and 12 polecats in the study area. Allozymic variation was measured from 38 presumptive structural gene loci by starch gel electrophoresis, using three continuous buffer systems (TC6, TC8, TEB8), (Lodé 2001a). Slices were stained following Pasteur et al. (1987), Murphy et al. (1990), and Rothe (1994). Loci successfully resolved were: AAT-1 and AAT-2 (E.C. 2.6.1.1); ACO-1 and ACO-2 (4.2.1.3); ADA (3.5.4.4); AK (2.7.4.3); CK-1 and CK-2 (2.7.3.2); DDH-1 and DDH-2 (1.8.1.4); EST-1 and EST-2 (3.1.1.1); FUMH (4.2.1.2); Gly2DH (1.1.1.29); G6PDH (1.1.1.49); GPI (5.3.1.9); HK-1, HK-2, and HK-3 (2.7.1.1); IDH-1 and IDH-2 (1.1.1.42); LDH-1 and LDH-2 (1.1.1.27); MDH-1 and MDH-2 (1.1.1.37); ME-1 and ME-2 (1.1.1.40); MPI (5.3.1.8); PEP-1 and PEP-2 (3.4.11.1); PGDH (1.1.1.44); PGM-2 (2.7.5.1); PNP (2.4.2.1); SDH (1.1.1.14); SOD (1.15.1.1); TPI (5.3.1.1); and two nonspecific proteins. Electromorphs were presumed to have a simple genetic basis. The number 100 was assigned to the most common alleles, and other alleles were designated in increasing order of mobility.
Individuals were genotyped with 11 nucleotide microsatellites (Mvis002, Mvis020, Mvis027, Mvis054, Mvis072, Mvis075, Mvis099, Mvis111, Mvis389, Mvis1843, PutFK1) using primer sequences that allowed amplification of simple sequence repeats published for related species (O'Connel et al. 1996; Brusgaard 1997; Fleming et al. 1999) and of simple sequence repeat evidenced in M. putorius furo (FK1) (GB : U06156.1). DNA was extracted from muscle tissue using standard chloroform-phenol protocol (Biase et al. 2002) and from hair follicles based in the method published by Wang et al. (2002). PCR amplifications were performed in 25 µl, and amplifications were run using a thermocycler biorad with 30 s at 94°C, 30 s at Tm and 30 s at 72°C. Products were denatured, resolved on polyacrylamide gels for detection by silver staining, and sized (Peltier and Lodé 2003). Sequencing reaction ladders were used. The effective number of alleles and assignment tests (maximum likelihood method) were performed using the Genetix (Belkhir, Genetix{at}crit.univ-montp2.fr) and WhichRun programs (Banks M and Eichert W, http://www-bml.ucdavis.edu/whichrun.htm). For each species, a value represents the likelihood of the individual's membership in that population. Each individual genotype is represented by its score for each allele at each locus.
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Results |
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Hybridization and Discrimination between European Mink and Polecat
Only four allozyme loci (10.5%) were found polymorphic in European mink (Est-2, Me-1 Mdh-1, Np), while allozyme polymorphism was found in nine loci (23.7%) for polecat (Ada, Est-2, G6pgdh, Me-1, Mdh-1, Np, Pep-2, Pgm-2, Sdh) (Table 1). From allozymic variations, European mink and polecats were easily discriminated from five loci (Table 2).
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Three animals had been erroneously determined. Two putative European mink were genetically identified as polecats, exhibiting the coat pattern of the "dark" phenotype. Both the length of guard hair and the genetic pattern made the determination certain. However, one heterozygous individual displayed both diagnostic alleles of European mink and polecat at five loci (Table 2). Because this animal displayed both allozymic characteristics of the two species, it should be regarded as an F1 hybrid between European mink and polecat.
From microsatellite data, polecats and European mink could be differentiated by five polymorphic and two monomorphic loci (Table 2). The loci Mvis002, Mvis020, Mvis075, and Mvis1843 clearly discriminated between European mink and polecat. The assignment test revealed these alleles to be diagnostic and confirmed one individual as a hybrid (Figure 2; probability 0.0001). The hybrid showed an intermediate pattern (Table 2). At locus Mvis054, a 118 pb allele was present in European mink, whereas a 114 pb allele was fixed in polecats. Interestingly, we also found the same 118 pb allele in three heterozygous polecats. At locus Mvis111, a small allele (89 pb) was fixed in European mink, but only two heterozygous polecats (one of which was among the previous individuals) showed the same allele. The clear-cut variation in allele size between the two species (five repeats; 10 base pairs) allowed us to exclude the possibility that the European mink allele could originate from a polecat allele by replication slippage. Similarly, the locus Mvis389 was monomorphic (103 pb) in the mink population; but two polecats (3%) fixed the same allele (103 pb), whereas every other polecat showed another allele (107 pb). Thus, for these three loci, the shared alleles were common in mink but rare and only found in heterozygous polecats. These indications were suggestive of six previous hybridization events between the two native carnivores. Most of these six heterozygous individuals—and the hybrid—were found in the north of the current range of European mink (Figure 1).
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Only four loci (36%) were found polymorphic at 0.99 in European mink (Table 3); whereas in the European polecat, the polymorphism reached 82% at 0.99 with nine loci over 11 scored (Table 4). Similarly, the mean number of alleles per locus was lower in the European mink than in the polecat.
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Frequency of Hybridization Events
Although the European mink was a rare and critically endangered species, a total of 35 European mink were live-trapped on 58 occasions, representing the highest number of European mink ever captured in the same area. We found no hybrid among these individuals, showing that pure European mink population currently inhabited the Seugne River. The sex-ratio of adults (number of males to number of females) only reached 0.69, emphasizing the predominance of mature females.
All live-trapped polecats (n=12) were pure polecats, thus revealing that the two native species can live sympatrically with no hybridization events being detected. Consequently, hybridization events should be considered as occurring very rarely (less than 3%, 1 vs 35 individuals), being beyond the level of detection by our design, or as happening elsewhere.
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Discussion |
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Hybridization events between the European mink and the polecat address an original evolutionary issue about the coexistence of sympatric native species and mechanisms promoting reproductive isolation. The main results are that: (1) hybridization events between European mink and polecats were rare and only detected in areas where European mink is rare and currently presumed extinct; and (2) no hybrids were found in the Seugne River despite the high number of European mink and polecats captured.
As was expected in a bottlenecked species (Nei et al. 1975), European mink exhibited a lower allelic differentiation than polecats, both in allozymes and in microsatellites. The effective number of microsatellite alleles per locus in polecats was twice higher than in mink (mink=1.45 and polecat=3.09). Nevertheless, the two species were easily discriminated from allozymes and microsatellites and showed many private alleles. Reviewing the power of resolution of genetic markers discriminating between species and hybrids, Boecklen and Howard (1997) noticed that using four or five markers should provide sufficient power. Here, two lines of evidences (allozymes and microsatellites) suggest that hybridization events occurred between polecats and European mink. The high level of private alleles most likely resulted from a basic divergence. By contrast, mitochondrial DNA analysis failed to resolve the relationship between polecats and European mink, revealing only one haplotype. Furthermore, that no distinct lineages were found in both species is suggestive of either a recent speciation (Davison et al. 2000) or a result of interspecific mitochondrial recent introgression (Sato et al. 2003). Little difference within species has also been demonstrated in gray wolves using mtDNA (Vila et al. 1999). Actually, the use of highly variable markers such as microsatellites should be more effective than mtDNA to allow the recognition of evolutionary significant units for conservation (Moritz 1994; Crandall et al. 2000). Because of the differential survival of the heterogametic sex or nucleocytoplasmic incompatibility, mtDNA markers should not be regarded as neutral and can be misleading when it comes to quantifying introgression.
The European mink range is actually fragmented into two population units: an eastern population unit from Oural and Estonia to the Black Sea, already subdivided into small units; and a western population (Youngman 1982; Saint-Girons 1991). The pure European mink population, which is still relatively abundant on the Seugne River, seems to constitute a key element in defining an evolutionary significant unit for the western European mink population. Although microsatellite data suggested European mink-polecat hybridization events, only a single case evidenced such a natural hybridization in the northern range. Moreover, for three microsatellite loci, the shared alleles are common in mink but rare and only found in heterozygous polecats; thus, we may hypothesize that several hybridization events occurred, especially in the north of the current range. Actually, the occurrence of hybrids means that at least some rare mink survived until now into small, restricted populations. Although only suspected through morphological identification, the existence of wild hybrids (up to 3%) between these two species has been reported in Russia (Ternovsky 1977; Tumanov and Zverjev 1986; Maran and Henttonen 1995). Anyway, a method to identify conclusively the level of natural hybridization between polecats and European mink is required.
The low divergence between the two taxa suggested that M. lutreola and M. putorius are sister species (Sato et al. 2003). The close relationships within the polecat group (M. putorius, M. furo, M. eversmannii, M. nigipes, and M. lutreola) support that these species constituted a holoarctic species complex, forming a syngameon according to Templeton's definition (1989). Experimental hybridization has established that polecats, ferrets, Steppe polecats, and European mink are able to produce fertile hybrids (Ternovsky 1977). However, natural hybridization between native species is hardly ever reported from the wild. Kit (Vulpes macrotis) and swift fox (V. velox) populations were thought to hybridize (Mercure et al. 1993), and genetic introgression was described between Martes martes and M. zibellina (Davison et al. 2001). The debated case of the red wolf Canis rufus seems also to originate from natural hybridization between coyote and gray wolf (Wayne and Jenks 1991; Nowak 1992; Reich et al. 1999). Mate recognition mechanisms could significantly contribute to prezygotic isolation and, questioning the significance of Mayr's biological concept of species, Paterson (1993) proposed that the evolutionary event for speciation first originated from a new mate recognition system while other mechanisms reducing interbreeding were incidental consequences. The hybridization may be favored by convergence in mating recognition system. The reason why European mink could hybridize with polecats may be found in phenotypic convergence. Polecats display a sympatric divergence, differentiating a "typical" morphotype from a "dark" phenotype; and the dark animals were both smaller and associated with forest brooks (Lodé 2001a), a habitat also selectively used by the European mink (Zabala et al. 2003). Nonetheless, here the rarity of hybridization events in European mink suggests that change or convergence in mating behaviors was poorly efficient to facilitate interbreeding.
When they hybridize with domestic species, endangered wild species may suffer from outbreeding depression, losing their specific adaptation to peculiar environmental constraints (Frankham et al. 2002). Hybridization with feral dogs exposed wolves (Vila and Wayne 1999) and threatened populations of Ethiopian wolves (Canis simensis) to a loss of their original genetic adaptations (Gottelli et al. 1994; Sillero-Zubiri et al. 1996). Furthermore, in carnivores, females are highly philopatric, but males are often closely related (Gompper et al. 1998; Lodé 2001b). Thus, the mating system of mustelids, in which mating in adjacent home-range is favored, is found poorly efficient to retain genetic diversity (Lodé 2001b). The natural interspecific hybridization between the native polecat and the endangered mink may entail outbreeding depression because hybrids were less fertile (Tumanov and Zverjev 1986). Thus, as suggested by the fact that no mink with polecat alleles were found, hybridization may result in a progressive assimilation of European mink by polecats, thus producing a "hybrid sink," especially when hybrids or backcrosses can not transmit mink alleles. The fact that hybrids showed many microsatellite "polecat" alleles supports this hypothesis. But occurring through an apparent natural process, it may be argued that hybridization may not be a problem (Allendorf et al. 2001), especially if hybrids are fertile. Arnold et al. (1999) demonstrated that natural hybridization, by introducing new genetic diversity into an endangered population, increased the average fitness of the individuals. Alternatively, hybridization may result in extinction when there is no habitat differentiation between taxa (Wolf et al. 2001).
Actually, our results suggest that hybridization may be linked to the mink population bottleneck. If hybridization results from a low efficient SMRS, many hybrids should be found when the species breed in the same habitat. On the Seugne River, the two native species bred sympatrically, with no hybridization events. Alternatively, if hybridization results from a lack of mating partners, hybrids should be more rare and rather present in areas where at least one of the two species is scarce. In western France, mink and polecats hybridized in areas where mink were scarce, thus supporting this second hypothesis. When a species is rare, individuals may be unable to mate within their own species, thus enlarging the opportunity for mating with individuals from closely related species. It may be suspected, then, that hybridization between polecats and European mink may proceed more and more frequently as European mink decline.
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Conclusion |
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Natural hybridizations occurred very rarely, beyond the level of detection by our capture design. Pure European mink and polecat populations still inhabited streams in western France, and hybridization events were only detected in areas where European mink were found to be very scarce. Thus, in western France, the two species have remained genetically distinct. Our results suggest that the hybridization events may be attributable to the scarcity of mating partners resulting from the severe bottleneck in European mink populations.
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Acknowledgments |
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We especially thank M. Ben-David and J. Secondi for helpful comments. Y. Benoit, M. Berthereau, S. A. Chaput-Bardy, B. Hamon, P. Fauret, D. Le Jacques, V. Potiron, C. Ricoult, J.-A. Rio, and F. Thomas provided valuable help throughout the study.
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Footnotes |
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Corresponding Editor: Stephen O'Brien
Received December 19, 2003
Accepted August 26, 2004
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References |
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Allendorf FW, Leary RF, Spruell P, and Wenburg JK, 2001. The problems with hybrids: setting conservation guidelines. Trends Ecol Evol 16:613–622.[CrossRef]
Arnold ML, 1992. Natural hybridization as an evolutionary process. Ann Rev Ecol Syst 23:237–261.[CrossRef][ISI]
Arnold ML, 1997. Natural hybridization and evolution Oxford: Oxford University Press.
Arnold ML, Bulger MR, Burke JM, Hempel AL, and Williams JH, 1999. Natural hybridization: how low can you go and still be important?. Ecology 80:371–381.[CrossRef][ISI]
Biase FH, Franco MM, Goulart LR, and Antunes RC, 2002. Protocol for extraction of genomic DNA from swine tissues. Gen Mol Biol 25:313–315.
Boecklen WJ and Howard DJ, 1997. Genetic analysis of hybrid zones: numbers of markers and power of resolution. Ecology 78:2611–2616.[CrossRef]
Brusgaard K, Holm LE, and Lohi O, 1998. Two polymorphic mink (Mustela vison) dinucleotide repeat loci. Anim Genet 29:468–469.[ISI][Medline]
Crandall KA, Bininda-Edmonds ORP, Mace GM, and Wayne RK, 2000. Considering evolutionary processes in conservation biology. Trends Ecol Evol 15:290–295.[CrossRef][Medline]
Crozier RH, 1997. Preserving the information contents of species: genetic diversity phylogeny and conservation worth. Annu Rev Ecol Syst 28:243–268.[CrossRef][ISI]
Davison A, Griffiths HI, Brookes RC, Maran T, Macdonald DW, Sidorovich VE, Kitchener AC, Irizar I, Villate I, Gonzalez-Esteban J, Cena JC, Cena A, Moya I, and Minano SP, 2000. Mitochondrial and palaeontological evidence for origins of endangered European mink, Mustela lutreola. Anim Conserv 3:345–355.
Davison A, Birks JDS, Brookes RC, Messenger JE, and Griffiths HI, 2001. Mitochondrial phylogeography and population history of pine martens Martes martes compared with polecats Mustela putorius. Mol Ecol 10:2479–2488.[CrossRef][Medline]
DeMarais BD, Dowling TE, Douglas ME, Minckley WL, and Marsh PC, 1992. Origin of Gila seminuda (Teleostei : cyprynadae) through introgressive hybridization: implication for evolution and conservation. PNAS USA 89:2747–2751.
Dowling TE and Secor CL, 1997. The role of hybridization and introgression in the diversification of animals. Annu Rev Ecol Syst 28:593–619.[CrossRef][ISI]
Fleming MA, Ostrander EA, and Cook JA, 1999. Microsatellite markers for American mink (Mustela vison) and ermine (Mustela erminea). Mol Ecol 8:1352–1354.[CrossRef][Medline]
Frankham R, Ballou JD, and Briscoe DA, 2002. Introduction to Conservation Genetics Cambridge: Cambridge University Press.
Gompper ME, Gittleman JL, and Wayne RK, 1998. Dispersal, philopatry, and genetic relatedness in a social carnivore: comparing males and females. Mol Ecol 7:157–163.[CrossRef][Medline]
Gottelli D, Sillero-Zubiri C, Applebaum GD, Roy MSD, Girman J, García-Moreno J, Ostrander EA, and Wayne RK, 1994. Molecular genetics of the most endangered canid: the Ethiopian wolf, Canis simensis. Mol Ecol 3:301–312.[Medline]
Grant PR and Grant BR, 1992. Hybridization of bird species. Science 256:193–197.
Lodé T, 1999. Genetic bottleneck in the threatened western population of European mink Mustela lutreola. Ital J Zool 66:351–353.
Lodé T, 2001a. Genetic divergence without spatial isolation in polecat Mustela putorius populations. J Evol Biol 14:228–236.
Lodé T, 2001b. Mating system and genetic variance in a polygynous mustelid, the European polecat. Genes Genet Syst 76:221–227.[CrossRef][ISI][Medline]
Lodé T, 2002. Endangered species as indicator for freshwater quality: a fractal diagnosis using fragmentation within European mink population. Arch Hydrobiol 155:163–176.
Lodé T and Peltier D, 2004. Genetic neighbourhood and effective population size in the endangered European mink Mustela lutreola Biodiv Conserv (In press).
Lodé T, Cormier JP, and Le Jacques D, 2001. Decline in endangered species as an indication of anthropic pressures: the case of European mink Mustela lutreola western population. Environ Manage 28:727–735.[Medline]
Maran T and Henttonen H, 1995. Why is the European mink (Mustela lutreola) disappearing? A review of the process and hypotheses. Ann Zool Fenn 32:47–54.
Maran T, Macdonald DW, Kruuk H, Sidorovich V, and Rozhnov VV, 1998. The continuing decline of the European mink Mustela lutreola: evidence for the intra-guild competition hypothesis. Symp Zool Soc Lond 71:297–323.
Mercure A, Ralls K, Koepfli KP, and Wayne RK, 1993. Genetic subdivisions among small canids—mitochondrial-DNA differentiation of Swift, Kit, and Arctic Foxes. Evolution 47:1313–1328.[CrossRef][ISI]
Moritz C, 1994. Defining evolutionarily significant units for conservation. Trends Ecol Evol 9:373–375.[CrossRef]
Murphy RW, Sites JW, Buth DG, and Haufler CH, 1990. Proteins. I: isozyme electrophoresis In: Molecular systematics (Hillis and Moritz eds.). Sunderland: Sinauer Press: 45–126.
Nei M, Maruyama T, and Chakraborty R, 1975. The bottleneck effect and genetic variability in populations. Evolution 29:1–10.
Nowak RM, 1992. The red wolf is not a hybrid. Conserv Biol 6:590–592.[CrossRef]
O'Brien SJ and Mayr E, 1991. Species hybridization and protection of endangered animals. Science 253:251–252.
O'Connel M, Wright JM, and Farid A, 1996. Development of PCR primers for nine polymorphic American mink Mustela vison microsatellite loci. Mol Ecol 5:311–312.[CrossRef][Medline]
Pasteur N, Pasteur G, Bonhomme F, Catalan J, and Britton-Davidian J, 1987. Manuel technique de génétique par électrophorèse des protéines Paris: Lavoisier.
Paterson HEH, 1993. Evolution and the recognition concept of species: collected writings Baltimore, MD: Johns Hopkins University Press.
Peltier D and Lodé T, 2003. Molecular survey of genetic diversity in endangered European mink Mustela lutreola. C R Biol 326:49–53.
Randler C, 2002. Avian hybridization, mixed pairing and female choice. Anim Behav 63:103–119.[CrossRef]
Reich DE, Wayne RK, and Goldstein DB, 1999. Genetic evidence for a recent origin by hybridization of red wolves. Mol Ecol 8:139–144.[CrossRef][Medline]
Rhymer JM and Simberloff D, 1996. Extinction by hybridisation and introgression. Annu Rev Ecol Syst 27:83–109.[CrossRef][ISI]
Rothe GM, 1994. Electrophoresis of enzymes, laboratory methods London: Springer-Verlag.
Saint-Girons MC, 1991. Le Vison sauvage Mustela lutreola en Europe Collection Sauvegarde Naturelle 54: European Council, Brussels.
Sato JJ, Hosoda T, Wolsan M, Tsuchiya K, Yamamoto M, and Susuki H, 2003. Phylogenetic relationships and divergence time among Mustelids (Mammalia, Carnivora) based on nucleotide sequences of the nuclear interphotoreceptor retinoid binding protein and mitochondrial cytochrome b genes. Zoolog Sci 20:243–264.[CrossRef][ISI][Medline]
Sillero-Zubri C, Gottelli D, and McDonald DW, 1996. Male philopatry, extrapack copulations and inbreeding avoidance in Ethropian wolves (Canis simensis). Behav Ecol Sociobiol 38:331–340.[CrossRef][ISI]
Stone G, 2000. Phylogeography, hybridization and speciation. Trends Ecol Evol 15:354–355.[CrossRef]
Storfer A, 1999. Gene flow and endangered species translocation: a topic revisited. Biol Cons 87:173–180.[CrossRef]
Templeton A, 1989. The meaning of species and speciation: a genetic perspective In: Speciation and its consequences (Otte D and Endler JA, eds). Sunderland, MA: Sinauer; 2–27.
Ternovsky DV, 1977. Biology of mustelids (Mustelidae) Novosibirsk, Russia: Nauka Publication.
Thornhill NW, 1993. The natural history of inbreeding and outbreeding. Theoretical and empirical perspectives Chicago: University of Chicago Press.
Tumanov IL and Zverjev EL, 1986. Present distribution and number of the European mink in the USSR. Zool Zhur 65:426–435.
Vila C and Wayne RK, 1999. Hybridization between wolves and dogs. Conserv Biol 13:195–198.
Vila C, Amporin IR, Leonard JA, Posada D, Castroviejo J, Petrucci-Fonseca F, Crandall KA, Ellegren H, and Wayne RK, 1999. Mitochondrial phylogeography and population history of the grey wolf Canis lupus. Mol Ecol 8:2089–2103.[CrossRef][Medline]
Wang R, Painter JN, and Hanski I, 2002. Amplification of DNA markers from scat samples of the least weasel Mustela nivalis nivalis. Acta Theriol 4(Warsz) 7:425–431.
Wayne RK and Jenks SM, 1991. Mitochondrial DNA analysis implying extensive hybridization of the endangered red wolf Canis rufus. Nature 351:565–568.[CrossRef]
Wolf DE, Takebayashi N, and Rieseberg LH, 2001. Predicting the risk of extinction through hybridisation. Conserv Biol 15:1039–1053.[CrossRef]
Youngman PM, 1982. Distribution and the systematics of the European mink Mustela lutreola Linnaeus 1761. Acta Zool Fenn 166:1–48.
Zabala J, Zuberogoitia I, Garin I, and Aihartza J, 2003. Landscape features in the habitat selection of European mink (Mustela lutreola) in south-western Europe. J Zool 260:415–421.[CrossRef]
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