Saturday, 14 September 2013

Over-purity as a danger for the Wisent?


Ok, this is a little bit off-topic, but it is bovine-related and certainly a very important issue that I don’t want to miss here.

It is well-known that the Wisent went through a dramatic bottleneck in the 1920s; only 54 individuals remained, and these descend from only 12 ancestors [1]. The contribution of these ancestral individuals to the modern population is uneven and dominated by one pair in particular, so that the modern gene pool is even smaller [1].

The small genetic diversity and the high degree of inbreeding is regarded as one of the main dangers to the global wisent population. Inbreeding affects the skeletal growth, leads to skull asymmetry, deformation of the male gonads, increases the rate of stillbirths, decreases female fertility and the resistance against diseases and parasites [1]. Wisents are vulnerable to diseases such as posthitis and balanoposthitis, foot-and-mouth disease, cattle tuberculosis, bluetongue disease and others. Epidemics are an acute danger to wisent populations, even in captivity. In the Bialowieza Primeval Forest, about 20% of the mortalities are caused by diseases [1].

The modern Wisent population is separated into two genetic lines. One is of pure bonasus individuals, and the other one has introgression of one single caucasicus bull. Curiously, the inbreeding effects are more severe in the LC-line. In the Lowland line the inbreeding coefficient is equal to 44%, in the Lowland-Caucasian line 26% [1].

"Kaukasus", the last pure Caucasian wisent
Line breeding separates the very small gene pool into two even smaller sub-pools and is something that usually would be avoided in the conservation of a species that is highly inbreed and homozygoteous. The reason behind this is to preserve the pure members of the lowland line, although the introgression of only one bull of a different subspecies eighty years ago probably would have little effect on the global wisent population, except that the genetic diversity would increase (what is, in fact, necessary to preserve the species). While the L line is a closed pool, the LC line is “open” and therefore pure lowland bison are constantly mixed in. This leads to a further decrease of genetic diversity, because the Caucasian influence gets increasingly diminished [1]. Therefore, line breeding increases the problem of inbreeding and homozygosity.
Therefore, one way to prevent the further loss of genetic diversity that I propose is to stop the line breeding by “opening” the L line, so that the two very small gene pools could fuse into a larger one and to prevent that the Caucasian influence disappears altogether. The affect of this influence of only one bull on “pure” Lowland wisents would probably be very small, as both bonasus and caucasicus belong to the same species and show only slight phenotypic and ecologic differences. It confuses me that there are efforts to separate subspecies and subspecies hybrids (with hardly any recognizable difference except inbreeding-related issues) in an endangered species with a critically small gene pool like the Wisent, while there is no such action in a genetically diverse, healthy and not endangered species like the American Bison, of which the two subspecies also intermixed in some populations (f.e. Wood Buffalo National Park) or not even to purge out the influence of domestic cattle in the American bison.

Another but certainly controversial step to increase the genetic diversity of the wisent is to cross-in single American bison and mate the results with pure Wisents again until the American influence isn’t recognizable anymore. In German there is the nice term “Verdrängungszucht” for this kind of breeding, what could be translated with “expulsion breeding” or so. The mere existence of such hybrids, or individuals with “unproven pedigree” are regarded as a threat for the Wisent in the action plan for the conservation of this species by the Polish Academy of Science [1], although it certainly would compensate the larger, immediate danger of the small genetic pool. It is true that uncontrolled and nontransparent hybridization, f.e. in a feral population, is an indirect danger for the Wisent as a species, but controlled introgression of the closely related American species might be helpful in overcoming the severe inbreeding depression of the European bison.
In the early 20th century, hybrids of wisent and Am. Bison, but also domestic cattle hybrids, were not rare at zoos and were in fact a threat for the conservation of the species, because there was the danger that hybrids and pure wisents become all mixed up and indistinguishable. That’s why a pedigree book for the Wisent was set up in 1931 – the first pedigree book for any endangered species – to ensure that the Wisent will survive in its original form, un-altered by uncontrolled hybridization [2]. Therefore, it is understandable why hybridization per se is still regarded as a threat to the Wisent, but today it is also apparent that the high degree of inbreeding and the resulting low resistance to diseases and parasites and other negative consequences are a drastic and immediate danger for the global population. Controlled introgression by few hybridization events would be one way to add genetic diversity to the wisent gene pool, but what other effects would controlled hybridization and back-crossing have on the Wisent?

The European bison and the American bison are closely related and can interbreed without any fertility problems. Because of this, several authors treated them as one species in the past. Phenotypic differences are apparent; the American bison has a more longish and massive body, more opulent fur on the head forelegs and also the horns are not as long but thicker as in the Wisent, among other differences. However, both species are ecologically similar, except that grasses make up a higher portion in the diet of the American bison. The Wood bison, B. b. athabascae, inhabits a similar habitat as the Wisent did in ancient Europe. In 1940, hybrids of American and European bison were released in the Caucasus. After controlled culling and subsequent replacement with pure wisents, the portion of American blood within the Caucasus population is now estimated being only about 5%, although the American influence is still slightly visible in the phenotype of the animals. Allegedly this population has a destructive influence on the local flora because of the hybrid origin. I am not familiar with the facts behind this claim, but I am sceptic about it because according to the food choice of the A. bison, the only difference to be expected is that they eat a higher amount of grasses than pure wisents would do – and originally there were two other species of grazers in the Caucasus that relied on grasses to a large extent (aurochs and wild horse). But of course does the presence of herbivores change the frequency of certain plant species, because herbivores decimate some species more than others. This is to be expected in every ecosystem, and this observed change in the plant community might be interpreted as a “damage” if someone expects the animal to cause damage. It is further claimed that the population released in the Caucasus is less tolerant to cold and less adapted to mountainous habitat because of the influence of the American bison. But the lacking adaption to the mountainous habitat probably isn’t due to the American influence in particular, but the Caucasian Wisent very likely had special adaptions to its habitat that are not present in the Lowland Wisents as well. For example, it was smaller, had shorter higher hooves and a less shaggy coat [3]. The claim that the American influence made them less resistant to cold is very likely incorrect, since American Bison resist temperatures down to - 40° Celsius.

Wisents with American bison introgression in the Caucasus (Photo by Sergej Trepet) 
In order to conserve the Wisent as a species but to increase the genetic diversity by controlled hybridization, not a patchwork of American and European features should be the objective, but a homogenous Wisent population with slight American introgression that is not visible. This is possible, as we know from the fact that many modern American bison populations experienced introgression from domestic cattle in the past, but the cattle apparently left hardly a trace in the phenotype, behaviour or ecology of the bison (however, this isn’t the case for all herds). Controlled hybridization followed by “expulsion breeding” by constant back-crossing with pure wisents can result in a wisent population that looks like the wisent, behaves like the wisent and has the ecology of the wisent, but is more genetically diverse than the highly inbreed “pure” populations. Individuals that show clear traces of the American bison can be selected out. When American bulls are used and only their female offspring is chosen for further breeding, the entrance of “foreign” Y chromosomes is effectively prevented (vice versa for the mitochondrial DNA in cows).
What would be the effect on the genetic structure of the Wisent? As a population geneticist would say, its allele frequency would slightly change. But as we know through modern genetics, populations always change (genetic drift). The modern wisent is necessarily genetically different from the Wisent of the 19th century before the bottleneck event. And the Wisent of the 19th century was genetically different from that of the Bronze Age et cetera.

Surely, uncontrolled and nontransparent hybridization of wisent with American bison or even cattle, be it in the wild or captivity, is a threat for the conservation of the species. But a controlled and transparent breeding plan like described above might be seen as a chance for the Wisent to gain more genetic diversity to overcome the menacing effects of inbreeding in the species. Perhaps the European bison Pedigree book one time will allow a third genetic line with American introgression besides the Lowland line and the Lowland-Caucasian line, where every interspecies mating is transparent and recognizable. In this case it would always be possible to distinguish between wisents with introgression and those without, and the amount of introgression is always transparent as well. If the Pedigree book is against such a step, there is still the possibility to set up a new breeding book for that lineage. Surely this would be controversial and also cause disaffirmation, but if it turns out that Wisents with slight American introgression are healthier and more resistant to diseases than their “pure” counterparts and show no apparent signs of hybridization (neither in their phenotype, behaviour or ecology), maybe there will be shift in looking at this strategy to safe the wisent, for which, as the conservation plan states, “the danger of extinction still remains”. Maybe it will also cause a different look at the 700 wisents that are not registered in the Pedigree book and also the population in the Caucasus. The latter population has been living in the wild for more than 70 years now and grew to magnificently large numbers (though poaching is a serious problem), and therefore is certainly precious. Culling of bulls and replacing them with pure Wisents could further reduce the phenotypic effect of the American bison introgression.

In my opinion, studies comparing the food choice of American bison, European bison and hybrids should be set up. Also it is necessary to investigate the resistance of the hybrids against diseases and other negative effects of inbreeding (the existing population in the Caucasus could serve as a model) and to investigate which of the two subspecies of the American bison is better-suited for such an attempt. This could be a scientific basis for a breeding experiment executing controlled and transparent introgression into the Wisent pool as described above without affecting it as a species in order to overcome the most serious and immediate threat for the conservation of the species.

Here's a video of the wisents in the Caucasus with bison introgression: 




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
  • [2] Jan Raczynski, Malgorzata Bolbot (2009): The European Bison Pedigree Book.
  • [3] Ninell Melkadze, Nargiza Ninua, Izabella Skhirtladze (2009): Catalogue of the type specimens of Caucasian large mammalian fauna in the collection of the National Museum of Georgia


13 comments:

  1. What are some of the phenotypic differences between the lowland and lowland-caucasian lines? Can you look at a Wisent and know which line it most likely came from?

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    1. There is no difference to tell them apart (except that LC cows have a more deformed skeleton, but this isn't visible in living animals). It's even hard to distinguish pure Caucasian wisents from Lowland wisents at first glance, based on the few photos of living animals (http://www.bisonbonasus.ro/pdf/ebpb.pdf page 6 shows a photo of the bull "Kaukasus"). One difference is that the Caucasian wisent has curly hair on the rear as well, but there is no clear difference in the Lowland line and Lowland-Caucasus line regarding that feature. The separation of these two lines serves no real point and just reduces the genetic diversity even further, therefore it should be abandoned IMO.

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  2. I think I agree with your opinion that the two lines should be merged for the sake of genetic diversity. Is there even any evidence that the Caucasian was a true subspecies of Wisent? Has there been any DNA testing on museum specimens? If not, could the Caucasian wisent simply have been a regional variation of the lowland wisent? Just becuase there are may have been some phenotypic and behavioral differences, doesn't mean the two are true subspecies. If that study has not been done, perhaps it should be and if subspecies designation was never truly warranted, it may be more likely that people would be willing to merge the two lines.

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    1. That's a good point, it could indeed be a regional variation or maybe there was a continuum between the Caucasus type and the Lowland type. Indeed such genetic testing should be done in order to convince more people of the need to merge the two lines. But perhaps that still wouldn't generate enough genetic diversity in order to overcome the inbreeding depression, therefore my proposal of controlled introgression into the Wisent pool.

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  3. I see this purity madness in other organisms as well. Lumping the two populations is sound. Some very modest introgression with with the American cousins, say, 1/1000 per generation would indeed strengthen the gene pool trough hybrid vigour. But purity is somehow important to people despite the biological irrelevancy of it.

    I am curious though. You reject this option for Bos primigenius. The domestic lineages probably all have some basic domestic genes fixed. Wild variants of those loci could be obtained from other extant wild Bos cattle. Slight introgression with a lot of expulsion breeding, as you described, could solve a lot of your current problems.

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    1. Good to see that we agree on the wisent subject!
      Regarding the aurochs, I also consider it very likely that domestic cattle, taurine and zebuine, do not preserve all relevant genes that were present in the aurochs. Getting them from related Bos species would be exciting and I played with that thought several times (f.e. the Java banteng has a very strong sexual dimorphism, stronger and more stable than in any taurine or zebuine cattle), but to put that into practice it should be proven that Banteng, Gaur or any other member of the Bos-Bison clade carry genes that were present in the aurochs in the same form but are absent in domestic cattle. I consider that a possibility that should be tested. Mind, however, that the ecologic and behavioural differences between the aurochs and Banteng/Gaur and especially bisons is considerably larger between the European and American bison - some authors even suggested that both should be considered one species, and some that even today.

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  4. The American Bison is actually still quite rare in its pure form, found only in two small herds. Large numbers of American Bison are actually hybrids descended from bos cattle found on the ranches. Hybrids of Bos and Bison always look like Bison so they are not detected before genetic testing. It is inconvenient to breed back pure American Bison to the numbers that the hybrids currently have. Herds are in private hands apart from Yellowstone Bison each herd has hybrid traits. The US is trying to keep hybrids and pure appart.
    Tiger subspecies found in US Zoos are deliberately bred within the sub species to increase total numbers, generic mixed Tigers are not bred, so numbers fall as they die off. Hybrid Bos Bison could be eliminated this way herd by herd, ranchers would want subsidisation and specialist controls to prevent re hybridisation.
    Lowland Wisent is the healthier of the 2 lines despite only descending from 3 females and 4 males. Currently only 1 y-dna line survives intact for the Lowland Wisent. The other 3 founders contribute low dna amounts according to the models. One of the 3 males still has an extant line in the Caucasian Lowland Line. In the 2nd line with the poorer health all 12 founders contributed although only 3 male lines out the original 5 survive. Caucasian Bull lineage occurs irregularly so active selection for that is desired. Equal found balance of extant lines is also desirable to preserve any un-purged diversity. These proposed actions are similar to attempts for rebalancing genetics of Icelandic Sheep Dog. A massive population boom lead to unequal genetic inheritance similar to the Lowland Bison.
    From my perspective the best way to increase diversity would be to set up a captive breeding group (in both populations keeping subspecies seperate) with deliberate intent to rebalance founder genetics and actively breed for single line mutations and diversity. This would require that separate groups be formed to further entrenched inbreeding for SNP genetic drift to be actively selected thus taking the breeding groups away from each other. Then when new reintroductions can occur the genetic distance is enough that there is diversity. All groups should start with equal founder representation and then be allowed to continue each line but be forced to diverge from other groups following different SNPs mutation lines.
    Currently the rebalancing has not been achieved. Lowland Wisent is managed in in breeding groups found in different places and continue to breed within these groups, then individuals from several groups are sent to a new release zone to start a new colony of Wisent then later top ups of individuals from different groups are sent in to be small herds and increase the diversity.
    As a further note the breeding population can be selected in captive populations to deliberately foster genetic mutations and to keep rare genes. This is done in other captive breeding programs. If active DNA analysis and testing is done then diversity can be achieved in some groups through genetic drift, whilst in a control group maintain the group foundation genes by preventing drift can be used. It is through these selective breeding for health and dna checking SNPs that you can foster diversity without needing to outbreed.
    Highland Bison: In the Caucuses the USSR did try to breed an American Bison with into a line of Caucasian Lowland Wisent. They live in a population one side of the mountain whilst the Russians maintain that the Pure Lowland Caucasian Wisent in another herd on the other side cannot be reached by the other group due to terrain. DNA testing is needed to see if that is true. Your proposition can be tested on that isolated group.
    Some scientists want the "Highland Wisent" to be recognised as a different subspecies and efforts be made to separate it from the 2 subspecies. It is currently unknown if the Highland Wisent was descended from American Bison with cattle genes although this is probably likely as the hybridisation was in the post WW2 years.

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    1. I am going to answer both your comments here now.
      First of all, it is AFAIK not entirely true that A. bison with hybrid origin long ago are phenotypically undetectable. Some of those individuals have deviant, thin horn shapes resembling domestic cattle, or longer tails. The numbers I heard for bison having domestic cattle in their ancestry ranged from about two thirds to 90%. But except for those little, rare "imperfections", I don't see anything dramatic about that. It nearly has no impact and I see no reason for working against it. I read of a paper that suggested that some bison with cattle ancestry might have disadvantages in the wild as it turned out that those with cattle mitochondria are lighter on average than others, but if its really true that they have disadvantages of any consideration population dynamics will take care of that itself.
      My knowledge on all those ancestral wisent lines in the modern population is not that profound, for the reason that I have problems with the weight we should put on genetic markers. The assumption that preserving and balancing ancestral lines (btw, that would not be an increase of diversity but just preventing further loss) based on phylogenetic markers will help to not make things worse is sound. But it also includes the assumptions that all genes within an individual or line get inherited as one genetic package. This is not the case as genes are getting passed on by chance. And what really matters are the genes that play a role in immunology, development etc. and the avoidance of deleterous alleles. Therefore coincidence may work for us or against us.
      As for the "Highland wisent". I (and I hope any down-to-earth zoologist) consider it baseless to describe this evolutionarily young bunch of hybrids as a separate species, as is the claim that they have adapted to the ecosystem in a way special to those adaptions that wisent or wood bison have.
      Regarding what to do with the caucasus population, I simply want them to "live long and prosper". If they'd one they merge with a pure neighbouring wisent population I would actually consider it a good thing. They would become more wisent than they are now and the advantageous genes they posses thanks to hybridization and subsequent selection would be spread among a larger population. But blind purist fanactics will be against that and try to prevent it, and it is my greatest fear that the Caucasus population will be killed (or poached) off out of ignorance or negligiance.

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  5. As you said the rebalancing of the population does not create diversity but it prevents loss of diversity which is a key step. Genetically when it comes to population bottle necks the important thing is to have founder representation found at a good balance to allow sub populations to split off and come back together having diverged somewhat.

    With inbreeding in a closed population old and new inbreeding are considered two different things. Old inbreeding is not considered as important on the negative side of things due to the purging effect on the survivors. That is if there are survivors who bred through the bottle neck mutations will arise in individual populations due to SNP and with geographical bottle necks differences will grow over a long period of time due to drift between populations.

    New inbreeding is risky due to the possibility of a population dying due to adverse recombination. The only way to deal with new inbreeding is to conceive frequently as genetic recombinations may provide enough healthy individuals to outlast a inbreeding depression as the unfit animals die off.

    We can consider the main foundation of the population the major inbreeding event. Due to the distance of the time in terms of generations between then and now that old inbreeding does not matter so much as it was survivable. Preserving the smaller gene pool is a bonus for future breeding.

    The newer generations are interesting in that when a population is selected to be rewilded they choose one male and four unrelated females as the basis. Unrelated that is in terms of non siblings. It is expected that some variation from the breeding groups has arisen in SNP mutation (only small in number per individual) or genetic drift has altered the balance between these groups so that the new herd can stand a little further inbreeding.

    Assuming this continues without change over the further 30-40 years I look forward to a genetic study of these herds to see what variation the population has and whether they avoided hybridisation with the other bison herds or domestic cattle.

    Due to the recombination of genes I agree with you that even if you estimate known percentage base of an individual due to pedigree there is still a large distance between the founder and the current lineages. Preservation would involve creating a subpopulation of known direct line individuals with high percent ancestry and breeding them together to increase that population number before reintroducing them back to the main herd.

    I am happy for the Caucasian-lowland population to merge with the lowland population as there is not enough genetic difference to proclaim the Caucasian-lowland a distinct population. Regarding the "Highland Bison", I would not want to see that merge into the general population of either of them as it is a hybrid of a three species (Bos, Bison and Bonasus) regardless of the balance. However they can be left to do their own thing in their own region.

    Thanks for the response.

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  6. http://www.nature.com/articles/ncomms13158

    The point you're making here is now backed by sound evidence that modern Bison bonasus originated from at least one hybridisation event between Bos primigenius and Bison priscus (and as you know Bison priscus is directly ancestral to both American subspecies). So, in this new light, the introgression of an american individual or two shouldn't seem as radical as those who keep the pedigree may have previously thought, even Bison bison with introgression from cattle would be suitable as essentially the wisent is the result of a step bison population with aurochs introgression. These large bovines obviously interbreed on occasion in the wild and don't differ too much in their ecology, so perhaps 'purity' is a moot point all together.

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  7. Hi Daniel,

    I work for the Nature Conservancy's Cool Green Science blog. We've got an upcoming post about European bison and I'm planning to use the image you shared of Kaukasus. I haven't seen it anywhere else, so I'm going to link back to your post in the caption.

    Please let me know if this is a problem - lfeldkamp[at]tnc[dot]org

    Thank you!

    Cheers,
    Lisa

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    1. Hi Lisa,

      I got that picture of Kaukasus from this this website: https://www.biolib.cz
      But you can of course link back to my post as well. Unfortunately I can't remember any precise information on the photo (who took it or where it is from).

      Cheers,

      Daniel

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