What are the impacts of interspecific hybrids on species conservation

Rates of hybridisation are increasing dramatically worldwide because of human activities such as the translocation of organisms, habitat fragmentation and modification. As a result, many species have faced, or are facing, extinction. However, hybridisation is also a natural process which has long been recognised as playing an important role in the evolution of plants, and recent studies have found that hybridisation has also played an important role in the evolution of animals.Thus, conservationists need to distinguish between species that have arisen through recent, anthropogenic means and those that have arisen through ancient, natural hybridisation.

Conservation policies need to protect the latter species, and also reduce rates of anthropomorphic interspecific hybridisation. Humans often translocate organisms and introduce them into new areas, often with catastrophic effects on the native species. This problem is exemplified by the introduction of the ruddy duck Oxyura jamaicencis from North America into Europe.This species is closely related to the white-headed duck O.

eucocephala which is commonly found in Britain and north-western Europe. If these two species meet they interbreed, and the abundance of the ruddy duck suggests that the outcome would be the eventual extinction of the native white-headed duck by genetic mixing1. The increasing utilisation of land for human activities such as agriculture, mining and forestry, has meant that habitats are becoming increasingly fragmented. Fragmentation of species' habitats results in reduced population sizes, which, for some species more than others, can mean that they become quite rare.Hybridisation between rare and common species has two potentially harmful consequences for the conservation of biological diversity.

If the F1- or later-generation hybrids are partly sterile or have reduced vigour, then the rare species may be endangered by outbreeding depression. That is, rare populations may have reduced fitness due to gamete wastage in the formation of unfit individuals (this is particularly true of organisms that produce vast numbers of gametes, like plants and fish).In this way, the rare species becomes extinct through demographic means: small populations are more vulnerable to extinction. On the other hand, if the hybrids are fertile and vigorous, hybridisation may lead to the genetic assimilation of the rare species by a numerically larger one. In this way, the rare species becomes extinct through genetic means.

Early conservation policies generally did not allow the protection of hybrids, however, the recent recognition of the historical role of hybridisation as an evolutionary process, has caused a re-evaluation of these policies.An early series of interpretations of the US Endangered Species Act (ESA) concluded that a species or subspecies that had undergone hybridisation with another named entity was prohibited from protection as a federally endangered species or subspecies. The view was taken that 'impure' species containing 'foreign' genetic material did not merit protection as they would not help recover the listed species, and may jeopardise its continued existence. Strict and prolonged adherence to this policy would have discontinued conservation programs and reintroduction strategies for many plants and animals.

However, based on scientific information on hybridisation, this Hybrid Policy was withdrawn, and a new more flexible policy was proposed: The Intercross Policy (1996). The overall goal of this revised policy is to maintain flexibility in interpretation and to allow policy to be guided by scientific understanding of hybridisation. However, the fact that this policy has not yet been approved, illustrates the difficulty in writing a hybrid policy that is flexible enough to apply to all situations, but that would still provide helpful recommendations.In order to fully understand the impact of interspecific hybrids have on species conservation, it is important to distinguish between the different categories of interspecific hybridisation: those that are a natural part of the evolutionary legacy of taxa, and those that are due to human effects.

The former group of species should be eligible for protection, however, the latter can be further divided into categories which have different consequences from a conservation perspective. Allendorf et al. divide 'natural' hybridisation into three categories.Type 1 hybridisation results in natural hybrid taxa that have arisen by natural genetic admixture2.

Species resulting from such historical hybridisation events should be eligible for protection, just like any other species. For example, the Virgin River roundtail chub Gila seminuda originated from hybridisation between G. elegans and G. robusta in the Pleistocene, as is listed as endangered under the ESA. Allendorf et al. classify introgression3 that is natural, but does not lead to a creation of a new taxon type, as type 2 hybridisation.

For example, hybridisation between phenotypically distinct species of land snails Partula tainiata and P. suturalis inhabiting islands of French Polynesia has resulted in species from one island resembling each other genetically more than they resemble conspecifics from other islands. Clark et al. (1998) concluded that this apparent paradox was best explained by 'molecular leakage, the convergence of neutral and mutually advantageous genes in two species through occasional hybridisation'.Populations resulting from type 2 hybridisation contain alleles from other taxa, but ongoing hybridisation is not increasing the frequency of those alleles. Such introgression is part of the evolutionary process and should not preclude protection of taxa that result from this type of hybridisation.

Finally, hybrid zones4 which are stable and persist over long periods of time by a balance between dispersal of parental types and selection against hybrids, are classified as type 3 hybridisation. Species that result from these types of hybridisation are eligible for protection, as they are the result of the natural course of evolution.The remaining three types of interspecific hybridisation involve situations in which human activities have caused hybridisation. Situations where F1s are primarily detected is classified as type 4 hybridisation. In this case, we are seeing hybridisation without introgression because the hybrids are partly/completely sterile. Thus, hybridisation is not a threat through genetic mixing, but through the wasted reproductive effort which poses a demographic risk.

For example, the endangered bull trout Salvelinus confluentus hybridises with the introduced brook trout S. ontinalis.However, the F1 generation is sterile, so that the wasted reproductive effort has accelerated the decline of the bull trout. The last two types of hybridisation (types 5 and 6) involve the presence of hybrid swarms5, and can be considered as two stages of the same process.

Type 5 describes the situation when hybridisation has begun only recently or is geographically restricted so that parental populations still exist. Type 6 describes the situation if conservation action is not taken, and all the populations become hybrid swarms, resulting in complete admixture.These two types can be considered as one, as once hybridisation has begun, it is extremely difficult to stop (especially if hybrids are fertile and mate both amongst themselves and with parental individuals). After a few generations, this process will result in a hybrid swarm in which essentially all individuals are of hybrid origin.

These hybrid swarms can form even if there is selection against hybrids because all the progeny of hybrid individuals will be hybrids. Thus, it is of primary importance to distinguish between natural and anthropogenic hybridisation, as anthropogenic hybridisation is causing extinction of many taxa.It follows then, that it is crucial for conservationists to distinguish between natural and anthropogenic hybrids, as conservation of the latter will contribute to extinction of the 'natural' parental species and waste limited resources available for conservation. However, this important distinction is often very difficult, and this is exemplified by the controversy surrounding the origin of the red wolf Canis rufus.The red wolf was originally found throughout southern USA. Habitat disruption and reduction of red wolf numbers allowed coyotes C.

atrans to invade the range of the red wolf, and subsequent hybridisation between the two led to the loss of almost all red wolf populations through genetic mixing. It was thus listed as endangered under the ESA in 1967. However, molecular genetic analysis of red wolves led to the suggestion in 1991 that the red wolf is a hybrid taxon resulting from the hybridisation between grey wolf C. lupus and coyotes. The controversy has focused on whether the introgressive hybridisation with coyotes is ancient or recent.According to Nowak and Federoff (1998), red wolves are not a result of hybridisation between grey wolves and coyotes, as evidence shows that the red wolf is not intermediate between grey wolves and coyotes (as would be expected under type 1 hybridisation).

They suggest that the red wolf could have resulted from type 2 hybridisation in which some coyote genetic material became introgressed into red wolf. Thus, according to this ancient divergence theory, the red wolves are not artefacts of anthropocentrically influenced hybridisations with coyotes, rather they existed historically and only recently have hybridised with coyotes.Thus, the authors consider them worthy of distinct conservation strategies. On the other hand, some biologists do not consider the red wolf to be phylogenetically distinct, but rather the result of extensive hybridisation between grey wolves and coyotes. This theory is rooted in a molecular analysis that found that red wolves have no alleles unique from either grey wolves or coyotes. Roy et al.

(1996) argue that if the red wolf is a hybrid promoted by the expansion of European settlement in North America, then it may not deserve conservation status.Allendorf et al. conclude that, given that genetic evidence can not provide a clear answer, the red wolf is an 'evolutionary entity' worthy of protection as it is a component of the evolutionary legacy of canids. Once a situation where interspecific hybrids have arisen through anthropogenic effects is recognised, many controversial questions arise when developing the conservation plan.

For example, how many interspecific hybrids can be present in a population before we consider it to be 'impure'? In other words, what proportion of admixture is acceptable?No general answer can be given which will apply to all situations, as the amount of admixture that precludes protection varies with each situation. For instance, the smaller the number of pure populations6 within the species, the greater the conservation and restoration value of any hybridised populations. In addition, the greater the phenotypic differentiation between the hybridised population and remaining pure populations, the greater the conservation value of the hybridised population. Another important factor to consider is whether the continued existence of hybridised populations poses a threat to remaining pure populations.The greater the perceived threat, the lower the value of the hybridised population.

Another important question that needs to be addressed by conservationists is whether parental individuals can be 'rescued' from the hybrid population, and then be used in founding new populations or in captive breeding. This approach can work well if the hybrids are sterile, so that the population consists of parental individuals and F1 hybrids. In this way, testing at a sufficiently large number of diagnostic loci, the parental individuals can be used for recovery.Hybrid species resulting from anthropogenic causes can sometimes be used as a tool in conservation. For instance, small populations which have recently gone through a bottleneck will contain little genetic variation, and so it is sometimes advisable to increase this variation by intentional hybridisation. For example, a headwater population of topminnow Poeciliopsis monacha that had lost all detectable heterozygosity because of a population bottleneck caused by drought, was being outcompeted by a sympatric asexual hybrid taxon of the same genus.

Experimental replacement of 30 females with 30 females of a downstream population that had high heterozygosity restored the original heterozygosity and the competitive ability of the sexual population. This method must be used with extreme caution as the purposeful introgression could cause the loss of local adaptations and lower the mean fitness of the target population. Intentional hybridisation is appropriate when the population has lost substantial genetic variation though genetic drift and the detrimental effects of inbreeding depression are apparent.Populations from as similar as an environment as possible should be used as the donor population to reduce the risk of the target population losing local adaptations. Perhaps ironically, the threats of hybridisation to a rare species have received greater attention in the animal literature, such that all the examples used so far are of animals. It is ironic as hybridisation is more frequent in plants than it is in animals.

In plants, interspecific hybridisation can not only affect the preservation of native species through genetic mixing, but can sometimes give rise to new, sometimes invasive, species.This can have profound implications for the conservation of existing species. Some of the best evidence for the introgressive origin of new plant taxa comes from studies of the evolutionary consequences of interspecific hybridisation involving a parent or parents of alien origin. For example, Spartina alternifolia is a saltmarsh grass which was introduced to the British Isles from North America where it hybridised with a local native species, S.

maritima.The infertile hybrid S. ? townsendii spread by vegetative propagation, but at the end of the nineteenth century underwent chromosome doubling to produce a new, fertile species S. nglica. S. anglica has now largely replaced S.

alternifolia and S. ? townsendii, and has substantially reduced the range of S. maritima. Moreover, it has colonised areas of muddy salt flats that were previously devoid of any higher plant. Thus, the evolution of new taxa as a result of hybridisation can have devastating consequences for rare plant species. In conclusion, hybridisation is a natural part of evolution, and taxa that have arisen through natural hybridisations should be eligible for protection.

However, increased anthropogenic hybridisation is causing extinction of many taxa by both replacement and genetic mixing.Studies to determine whether a hybrid is 'natural' or 'anthropogenic' require thorough characterization of the distribution of genetic diversity within both parental species and within the area of suspected hybridisation. Typically multiple markers should be employed to characterize the frequency of hybridisation, the directionality of hybridisation (e. g.

comparing uniparentally and biparentally inherited markers), and the degree to which introgression has occurred. Once this has been determined, an appropriate conservation plan can be established.