Scottish Wildcats and other hybrids – wild and protected, or, domesticated and not worthy of protection?
Scottish Wildcats (Felis silvestris silvestris) have long been a contentious species in the world of conservation and highlight a need for better guidelines when it comes to the decision to conserve highly hybridised species. With current advances in genetic analyses it is becoming easier to assess the extent of hybridisation in populations; however the inaccuracies of these methods still produce controversy. In this review the problems which arise in deciding whether or not to deem these species worthy of protection and the subsequent issues concerning the prevention of further hybridisation are discussed. The Scottish Wildcat itself is a prime example of these issues and although currently protected it is not known how best to conserve this species, or whether the extent of its hybridisation with the domestic cat has led it to be so genetically distant from original Wildcats that they are no longer worthy of protection, which would imply that the Scottish Wildcat species is, in effect, extinct.
Hybridisation and its impacts on conservation efforts
The subject of hybridisation and whether hybrids should be protected has long been an issue in conservation. This problem is affecting the conservation of certain species such as the Scottish Wildcat which has been under protection under the Wildlife and Countryside act (1981), due to the difficulty of detecting whether a particular member of that species is a purebred or a hybrid. This was highlighted in a recent court trial where the shooting of possible Wildcats did not result in conviction is it could not be determined if the cats were domestic-Wildcat hybrids or actual Wildcats.(2)
It therefore implies that to retain the species under protection either the hybrid itself also needs to be protected, or the hybridisation of that endangered species needs to be completely prevented. It also needs to be determined as to the maximum extent of hybridisation allowable in an animal which causes it to still be classed as a member of the original species. This measurement has been a matter of some debate; up until recently hybridisation has been determined by morphological aspects, which for the Scottish Wildcat has proved inaccurate(17). Pelage characteristics in the Scottish Wildcat have previously been used to classify hybridisation(15), however it has been suggested that the use of these characteristics may be confounded by selection of Wildcat pelage by domestic cat breeders(7). Black and non-tabby Wildcats have been found, whilst many cats with tabby pelages exhibit varying morphological characteristics.(5) In future it has been suggested that on morphological characterisation other features such as cranial volume be used in conjunction with pelage.(2)(4)(17)(5) Over recent years however the capability to genetically compare and thus classify these animals has improved, with the use of Linkage Disequilibrium and unlinked marker analysis using microsatellites and AFLPs.(1)(11)(10)
The question as to whether a hybrid itself should be protected is also a matter of contention. It seems probable that the best way to do this would be to classify the cause of the hybridisation and to decide from there. Allendorf et al (2001) have classified hybridisation into two types; natural, and anthopogenic (caused by the activities of man), which cover three subsets each. Type 1, 2 and 3 are natural hybridisation, whilst 4 to 6 are anthopogenic. Type 1 describes a taxon which has occurred naturally from two other species. Type 2 hybrids are caused by occasional natural introgression which has not formed a new taxon. Type 3 hybrids occur along hybrid zones where the territories of two species are adjacent. These tend to be stable as in the case of the red and yellow shafted Colaptes auratu in North America which interbreed in a hybrid zone(18). The hybridisation does not extend out of this zone, presumably due to environmental or sexual selection against the hybrids. Type 4 hybridisation causes infertile F1 progeny so does not affect the population further than causing loss of reproductive effort. This may or may not be detrimental to the survival of the species. Type 5 and 6 form hybrid ‘swarms' where either most of the organisms show various severities of hybridisation leaving a few, generally isolated, pure populations as in type 5, or where complete admixture of the species has occurred (with no remaining pure organisms)(1)(16). Type of hybridisation has an effect on decisions to conserve species, depending on whether the hybridisation is evolutionary, or whether it is detrimental, and will result in total loss of the species.
It varies as to whether hybridisation is beneficial or has a negative impact on organisms. It appears that hybridisation can cause evolution(14)(20) and can be used in genetics to prevent inbreeding post bottleneck events where little of a species remains(26). Conversely, hybridisation can cause loss of a species; due to loss of genes which define a species, outbreeding depression, or in hybridisation without introgression a loss of reproductive effort(1).
The possible causes of hybridisation in the Scottish Wildcat
Wildcats occur across Europe and appear to not be undergoing such hybridisation in countries such as Portugal, Germany and Italy(9)(7). Wildcats in Scotland on the other hand appear to be suffering type 5 or type 6 hybridisation (explained previously)(1). This is more probable to be type 6 as no Wildcats have been found which can be classed as pure(2). Hybridisation in Scotland has most likely been due to increased population by humans which causes habitat (and thus population) fragmentation, a subsequent lack of prey, and the increased amount of domestic cats being brought into the area. All of these bring more Wildcats into more contact with domestic cats; habitat fragmentation will produce more ‘hybrid zones'(1)(18) and so increase hybridisation.
The genetic distinction between the Scottish Wildcat and the domestic cat
Whether or not Wildcats are worthy of conservation depends on their similarity to domestic cats. It is unknown whether the current Wildcats are the descendants of an original Wildcat population in Scotland, a divergence from domestic cats, or whether they are now more closely related to domestic cats due to interbreeding.(2) As such, genetic analyses have been carried out to determine the extent of the relationship between domestic cats and Wildcats in various regions of Europe.(2)(4)(5)(7)(8)(9) Of these, the most comprehensive in relation to the Scottish Wildcat is that by Beaumont et al.
Pierpaoli et al (2003) have shown using Bayesian Cluster analysis that the Scottish Wildcat is part of two distinct clusters in relation to other European Wildcats; one of these clusters being distinctly composed of ‘hybrid cats'. As such it is difficult to compare genetic analyses carried out on mainland European Wildcats with that of the Scottish Wildcat; the Scottish Wildcat is itself recognised as a subspecies of the European(2). However for the purpose of comparisons of the effectivity of genetic analyses, and of similar issues will be considered.
Beaumont et al (2000) utilised unlinked microsatellite analysis as described by Pritchard et al (2000) which allows the inference of the amount of genetic material inherited by an individual from one of the two populations (i.e. ancestral Wildcat or domestic). These results implied that portions of the genome of the Wildcats largely came from one population, whilst that of the domestics came from the other(2) which definitively implies two separate populations exist. However, this method of analysis does not take into account more historical introgression. Unlinked markers lose their genetic disequilibrium rapidly; genetic disequilibrium is a key assumption for this model and as a result the model may only recognise introgression resulting from a small number of previous generations. Falush et al (2003) have since suggested the use of a ‘linkage model' which solves this problem. This model incorporates the use of linked markers, i.e. those that exhibit linkage disequilibrium. This is sensible in studies such as these, as chromosomes are inherited as ‘chunks', therefore you expect to see a portion undergoing linkage disequilibrium. As a result, this model gives a higher resolution when looking at the origins of specific regions of the chromosome. Currently, it does not appear that anyone has undertaken study of Scottish Wildcats using this improved model, however it has been used to study hybridisation issues in Italian and Hungarian Wildcats(7). It has also been implied that the study by Beaumont et al (2000) may not have used enough loci in its analysis, thus leading to a possible underestimate of the extent of hybridisation(12).
Considering that the Wildcats appear to exist in two distinct populations Beaumont et al also produced ordination comparisons using Euclidean distance to represent the allele sharing distance between individuals. This resulted in the realisation that there are two main populations of Wildcat in Scotland; one appears highly related to the domestic cat groups, whilst the other is very distant. The existence of a purer population implies the Scottish Wildcat is a member of the category 5 hybridisation described earlier. This means that if extensive conservation efforts are to go ahead it may be sensible to focus on the distinct population using methods such as preventing further hybridisation by neutering domestic cats within the area(4).
On the origin of Wildcats
It is unknown when Wildcats and domestic cats diverged from one another in evolution. This is particularly difficult to calculate due to the recent hybridisation and introgression of genes. Beaumont et al have suggested two values for the divergence point. Using an assumed mutation rate of 5x 10-4 and the single step mutation model (24)a value of 10590 years ago was produced(2). This was before domestic cats were introduced to the UK and therefore would classify the Wildcat with a reason to be protected, as they have a distinct history. This model assumes that one population split spontaneously into two populations, both of a similar size and as such is prone to wrong estimates and is affected by introgression. It has also been shown to be less accurate than some models for use in closely related populations and therefore may not be the best method for this study.(24)On the other hand, using Nei's D model (25)produced a value of 1260 years ago. This is likely to be an underestimate as this model assumes no homoplasy occurs which is unlikely. This value implies the two species diverged whilst in contact with one another and thus denotes that the Wildcat diverged from the domestic cat post its introduction into the UK and may have subsequently been isolated, undergoing genetic drift to become as it is today. Whichever of these values is more accurate will have implications as to whether the Wildcat is considered worthy of protection status, or whether it is deemed a subset of domestic cats and thus not a species in itself. It is not possible to accurately estimate divergence time as it is unlikely that any Wildcats which could be classified as ‘pure' exist, and as gene frequencies of Wildcats prior to hybridisation are not known, it is impossible to classify these organisms as anything other than a population of individuals with unique genetics.(2)
Organisms with similar issues
There are many organisms facing extinction due to hybridisation, such as the red wolf which has similar issues as the Scottish Wildcat; habitat loss has reduced the population of these red wolves to the point where they require protection to prevent extinction. They were also being threatened by hybridisation with coyotes. As a result genetic analyses using microsatellites(21) and mitochondrial DNA(22) were carried out, which indicated that the red wolf may have originated from hybridisations between the coyote and the grey wolf. However this is not for definite, as it is possible that the three species have similar microsatellite loci due to having a relatively recent common ancestor. (22)(21)These studies caused controversy as it was not known whether the observed hybridisation was historic and evolutionary, or recent and anthopogenic (human induced) which has an effect in the decision whether to conserve a species. This type of survey has also been criticised as it may have not been able to take into account a decrease in heterozygosity and subsequent loss of rare alleles specific to the red wolf due to its small, segregated population sizes(21). The red wolf itself has since been protected by the ESA. (22)However this was a specific case; hybrids themselves are not generally protected. Since their protection, the new problem with red wolves is how to prevent further novel hybridisation with coyotes. Even if it is decided that the Wildcat should stay protected the problem of preventing further hybridisation will also affect them.
Another example of genetic analyses contributing to the understanding of whether hybridisation is driving a population towards extinction is that seen in European domestic dogs and wild wolves. Mitochondrial studies have detected hybridisation between the two(13)(23) and as a result further analyses were used to determine the extent to which hybridisation may be affecting the declining population of wolves. Using microsatellite analysis and the linkage disequilibrium analysis described above(6)(11) Veradi et al (2006) have been able to suggest that although the hybrids are interfertile, the two populations remain distinct; wolves and domestic dogs fit into separate clusters under all models tested.(13) It was also shown that very few hybrid individuals were detected, and were generally confined to the periphery of the population habitat, implying that in some respect the hybridised individuals are at a disadvantage(13), and that it is likely that few hybrids backcross into either population(23). It is therefore unlikely that hybridisation is a threat to the integrity of the wolf species at this moment in time. However, these populations will continue to be monitored as the declining ratio of effective population size compared to the observable population size is low, and thus hybridisation may become an issue in the future due to a lack of reproductively active wolf individuals.(23)
This review has highlighted a number of issues concerned with the conservation of hybrids, including the problems in classifying the extent of hybridisation within individuals and within a population and the subsequent issues in maintaining effective conservation strategies once a population is deemed worthy of protection. It is seemingly very difficult to accurately identify the actual origins of species such as the Scottish Wildcat or the Red Wolf,(2)(21)(22) and as such it is controversial as to whether species such as these are deserving of the large finance required to conserve a species. It is therefore necessary to further advance methods of genetic analysis to decrease inaccuracies which occur during these methods, to more precisely identify the time of divergence of closely related species and also to increase the accuracy in detecting the amount of an individual's genome which comes from a particular population. As far as the Scottish Wildcat is concerned, it will remain controversial as to whether Wildcats are worthy of conservation until analysis can be performed more accurately. It is also unlikely that any conservation methods will be effective until these analyses are improved as the distinction between domestic cats and Wildcats is currently unclear, and as a result conservation cannot go ahead without difficulties and controversy.