What to do with the wisent in the Caucasus?

For an update of my take on to this subject, go here. 

The Caucasus mountains were home to another subspecies of wisent, Bison bonasus caucasicus, until was exterminated in the first half of the 20^thcentury (it is also considered a separate species by some authors). Nowadays, wisents have been reintroduced in the western Caucasus reserve, and this population is controversial for its special history. In this post I am going to explain why, have a look at the arguments against this population, why I consider it beneficial instead and what to do with it for the future. 

First and most importantly it is to note that the modern wisent went through a severe genetic bottleneck event. All modern wisents descend from only 12 founder individuals and thus the genetic basis of the species today is extremely narrow. The consequences of this a considerable inbreeding depression affecting skeletal growth leading to skull asymmetry, deformation of the male gonads, increased rate of stillbirths, decreased female fertility and reduced resistance against diseases and parasites. They are particularly vulnerable to posthitis, balanoposthitis, foot-and-mouth disease, cattle tuberculosis, bluetongue disease and others. 20% of the mortalities in the Bialowieza Forest are caused by diseases. The inbreeding depression is an immediate danger for the long-term survival of the species and an obstacle for the establishment of populations in the wild [1]. It is not rare that reintroduction attempts fail due to these effects or that whole stocks in zoos diminish because of diseases. Therefore, the species is still in danger of extinction [1]. 

That is why during the population crash in the 1920s and 1930s wisents were crossbred with American bison systematically in order to prevent an inbreeding depression. When an international herd book for pure wisent was set up, most of the hybrids were exterminated (and the expected inbreeding depression came). However, a herd of hybrids was released in the Caucasus in 1940. Subsequently the wisent percentage in the herd was increased by culling of hybrid bulls and release of pure wisents (absorptive breeding), so that the bison percentage in the modern herd is estimated to be as low as 5%. However, the hybrid influence is definitely recognizable (see here, here or here for individuals with a clear bison influence; it is not that much visible in these for example)* 

* It is interesting that the genealogic percentage is estimated that low while their phenotype is looks exactly intermediate between both species. One explanation might be that individuals with a high portion of bison genes might simply have a higher evolutionary fitness and thus the phenotypic influence of bison is still present despite absorptive breeding. 

Some authors suggest a culling of the population. There are a few arguments on why those hybrids are supposed to be maladapted and have been a bad choice for the Caucasus ecosystem: 

- allegedly the hybrids lack mountainous adaptions due to the influence of the plains bison

- allegedly, the plains bison influence made them less resistant to cold 

- allegedly, the plains bison influence has a destructive influence on the local flora 

First of all, Lowland wisent (B. b. bonasus, the only remnants of this population) do not show the mountainous adaptions of the Caucasus wisent either (which was smaller, had shorter and more rounded hooves), so the bison influence is probably not to blame on that. Furthermore, the claim that they are less cold tolerant due to bison influence is most likely incorrect as American bison resist temperatures down to -40° Celsius. Whether or not they have a destructive influence on the flora is probably subjective. The only dietary difference between American and European bison is that the American species consumes more grass than the European one. However, in the ecosystem there once were two other grazer species, aurochs and horses, so that the impact from the hybrid bison cannot be destructive for this ecosystem as it still lies within the spectrum covered by wisent, aurochs and horse. As we know, large herbivores do have an impact on the vegetation – they tend to open the habitat and stop or reduce forest growth. This is considered beneficial for European landscapes and biodiversity (intermediate disturbance hypothesis) which is why large herbivores, wisents among them, are (re)introduced in many nature reserves. Ironically, the same kind of influence that is considered beneficial elsewhere is considered a damage in the Caucasus reserve, serving as an argument to cull the population. Pure wisent would probably do exactly the same. 

Actually, I see no objective ecologic justification for culling this population and no alleged maladaptation as a result of hybridization. The sole remaining reason why this population is considered a threat is their hybrid ancestry. 

Back in the 1920s and 1930s, when there was no international herd book, hybridization was indeed a threat for the genetic integrity of the whole species. The Barbary lion, for example, is a subspecies which died out on genetic level as there are probably no remaining pure individuals due to hybridization. However, nowadays the situation is different. The pedigree of each wisent considered pure is documented in the pedigree book, and wisents that are not listed in the pedigree book are ignored to death anyway (this concerns about 700 wisents in Europe). Therefore, the existence of a wild hybrid population in the Caucasus is not a danger to captive pure herds (however, there is a neighbouring pure herd in the region, but I come back to that later). It is probably the mere existence of the hybrids that irritates some authors so that they suggest the culling of the whole population. 

Nevertheless, I want to look into the positive aspects of this population.  The inbreeding depression we see in the wisent is the result of the high degree of homozygosity in the population which leads to an expression of the effects of deleterious alleles. This can only be overcome by the introduction of new alleles in order to reduce the frequency of the deleterious alleles. Hybridization introduces new alleles and the closest living relative of the species is the American bison, so this species would offer as a possibility to increase genetic diversity. 

Hybridization of course introduces alleles specific (=diagnostic) for the foreign species, but could also introduce alleles on loci that are not relevant for the differences between wisent and bison as such but where wisent are homozygous for deleterious alleles. Thus, hybridization, when the right alleles are introduced, can help to overcome the inbreeding depression of the wisent affecting development, fertility and resistance against diseases without affecting its genetic integrity and thus be beneficial for its chances of survival as a species. Of course rampant hybridization without any kind of selection just produces a phenotypic and genotypic mosaic or mess, which is why some sort of directive selection would result in the desired goal: increasing the genetic fitness of the wisent without grossly affecting its genetic integrity as a species. Therefore just keeping those hybrids in zoos without any selective breeding would lead to technically nothing. However, in the population in the Caucasus, we have something special or even ideal acting upon their gene pool: natural selection. The start-up population was a bunch of hybrids from zoos, but since 1940 they experienced more than 70 years of natural selection. It is likely that the frequency of deleterious wisent alleles on the respective loci has decreased as a result of the higher fitness of newly introduced alleles from American bison, therefore decreasing the effects of the inbreeding depression. To put it simply, those hybrids with a healthier genetic make-up have a selective advantage over those with a high degree of deleterious alleles. I therefore expect the hybrid wisents in the Caucasus to be healthier, more resistant against diseases and have less problems with fertility and development than pure but highly inbred wisents. I strongly opt for studying the health and fitness of this population. As far as I know, this has not been studied before as there is little scientific interest in hybrids, especially for those in the wild. If the hybrid population in the Caucasus is indeed healthier and more evolutionary fit than inbred pure wisents, conservationist have one way to interpret it that can be expressed in two ways:

- Non-hybrid wisents are pure but dangerously inbred. Hybrid-influenced wisents are not pure but healthy and evolutionary fit. 

- Non-hybrid wisents are dangerously inbred but pure. Hybrid-influenced wisents are healthy and fit but not pure. 

In any case, the hybrid population in the Caucasus is probably the largest (in their best times up to 2300 animals) and healthiest wisent population since the population crash in the 1920s due to hybridization and several decades of natural selection. I am definitely not suggesting to crossbreed wisent and bison rampantly and simply release them in the wild. One argument against the hybrid wisents would be the phenotypic mosaic they are displaying which is probably the result of lacking selection on diagnostic wisent traits. The goal should be a population of wisents with increased fitness (i.e. reduced frequency of deleterious alleles) due to hybridization without any recognizable phenotypic influence from American bison in ecology, morphology or behaviour*. 

* Bison and wisent have different modes of combat behaviour. Bison butt their heads against each other while wisents fight more in a cattle-like manner by pushing and pulling with their horns. I know of now records on how the Caucasus population behaves in this respect. 

This could be achieved in a large-scale breeding project, but for the Caucasus population the solution is to increase the wisent portion in the gene pool while retaining their wild state, so that the fitness-increasing alleles donated by bison keep on replacing the deleterious alleles. One way would be to continue the absorptive breeding by culling wild hybrid bulls and releasing pure wisent bulls in the population. The problem is that this way is comparably un-directed. It would increase the wisent alleles in the gene pool, but the diagnostic wisent alleles as much as the deleterious alleles that are to be purged out. Therefore another possibility would be to release a sufficient number of pure wisents that merge into the hybrid population, so that the wisent genes find their way into the population by natural selection alone without human help. This way the survival chance for beneficial alleles is higher while the wisent percentage is still increased. This could be done several times in subsequent decades, until no American bison influence is visible in the population. 

As I wrote above, there is a neighbouring population of pure wisents in the Caucasus. The authors of the action plan for the conservation of the wisent 2002 fear an intermix between the pure and the hybrid population because they consider the hybrids, as written above, worthless and ecologically maladapted (for which, as I explained, there is no basis). I, however, hopethat there will be an intermix. It would be beneficial for both populations: beneficial alleles might enter the pure population while the wisent percentage in the hybrid population will increase. 

Although hybridization has been proven to be part of evolution in nearly all groups of related vertebrate species where it has been exanimated (see here), it is still deemed the absolute doom in conservation. This is, at one hand, probably a relict of the 19^thcentury picture of nature as a stable household system as much as the lesson from cases where uncontrolled hybridization indeed threatened or threaten the genetic integrity of endangered species. However, in the wisent it is the extremely narrow genetic base that threatens the long-term survival of the species. A rigorous study of the fitness and health of the Caucasus population could indeed provide a good argument for cautiously increasing the genetic diversity in the wisent via bison introgression in single controlled populations. Due to the pedigree book, the influence would be transparent anyway (a separate herd book for these new lines could be set up). 

In the eyes of others, it is more sensible to shoot them all and replace them with a population pure wisents that have the same fitness problems as anywhere else and might crash at any time.  

If anyone was to ask me personally which kind of animal I would prefer, a wisent that is 1/8 or 1/16 bison on both its parental sides and therefore healthier and more evolutionary fit or a pure wisent that is highly inbred with all the according problems, I would, honestly, go for the first option. 

I already covered the wisent population in the Caucasus in these two posts: 

- Over-purity as a danger for the wisent? 

- Donate for the wisent in the Caucasus! 

Literature

[1] Mammal Research Institute, Polish Academy of Science: European Bison Bison bonasus: Current state of the species and an action plan for its conservation. 2002