Monday, 12 February 2018

Biological basics pt.II: Hybridization and its role in evolution

Having had a look at how species are usually defined, this post is on the result of the reproduction between two distinct species – hybrids. More precisely, with this post I want to illustrate the role of hybridization in evolution and to show that hybrids are neither Frankenstein creations of bored farmers or zoos, or signs of the apocalypse (as hybrids of polar bears and brown bears are sometimes presented in the media). I also want to go into the role of hybrids in conservation with reference to one particular case, the wisent Bison bonasus.

The role of hybridization in speciation

Speciation is the event of the evolution of a new species. Most species evolve either through anagensis or cladogenesis. Anagenesis refers to the case of one species directly evolving into another. Cladogenesis is the evolution of new species by the split into new evolutionary lines, called clades, caused by reproductive isolation. In both cases, the genotype gets transformed by mutation, selection and genetic drift. But there is a third way a new genotype and a new species can involve, hybridization. In this case a new genotype is formed by the mixing of alleles respectively genes between species that are not too distantly related so that they are not (fully) reproductively isolated yet. Usually hybridization is constrained by pre- or postzygotic isolation mechanisms, and even when two species produce fully fertile offspring the hybrids may have a lower reproductive fitness than their parent species because they are less suited to the ecological niches of their parent species respectively. But in some cases, such as during the shift of environmental conditions or colonizing a new environment, hybridization and the resulting new genotype can be advantageous.

The plant kingdom is rich with such examples, especially polyploid hybrids such as Tragopogon miscellus. Both T. dubius and pratensis have been brought to North America by man, hybridized in nature and formed a stable hybrid via polyploidization in the 1940s, T. miscellus. In this case a novel species has been created. Other plant examples are to be found in the “genera” Brassica and Triticum.

There are not only examples for plant species that evolved through hybridization or introgression (introgression is when hybridization leads to an influx of genes into one gene pool), but also plenty for mammals.

The “genus” of modern Capra, goats, evolved through hybridization between the ancestors of Capra and Hemitragus, a closely related group, and as a result all modern Capra share Hemitragus mtDNA1.

The phylogenetic tree of Equus apparently also experienced at least four events of hybridization or introgression (the kiang and the donkey lineage, the Somali wild ass and the Grevy’s zebra, the African asses and the mountain zebra)2.

The Caribbean bat species Artibeus schwartzi is a stable, locally adapted and morphologically distinct hybrid of three congeneric bat species3.

In elephantid evolution, there must have been some interbreeding as was recently revealed by ancient genomes. Palaeoloxodon antiquus interbred with both the woolly mammoth Mammuthus primigenius as much as with the Asian elephant Elephas maximus4.

Mutual introgression and hybridization has been confirmed between the Alerigan mouse Mus spretus and three subspecies of the house mouse Mus musculus5.

Even in marine mammals there is at least one confirmed case of speciation through hybridiziation: the clymene dolphin Stenella clymene is a hybrid species of the spinner dolphin Stenella longirostris and the striped dolphin Stenella coeruleoalba6.

The phylogeny of modern bears has experienced mutual hybridiziation as well, between the Asiatic black bear and the ancestor of polar, brown and American black bear7.  Brown bears and polar bears repeatedly admixed ever since they split up phylogenetically8.
All recent Panthera species evolved under continuous intermixing between their evolutionary lines9.

Moving to species more relevant for the topics of this blog, bovines, we also have some examples in this group. Cambodian banteng populations share mitochondrial genetic material of the Kouprey, which they acquired probably through introgressive hybridization during the Pleistocene10. It is also well-supported by genetic evidence that the wisent is a hybrid of aurochs and Pleistocene bison, to be precise the maternal lineage was founded by aurochs and the paternal by bison11,12. 

Last but not least concerning mammals, we humans Homo sapiens are a prime example for hybridization and introgression as well. Human populations north to the Sahara interbred with Neanderthals, and as a result about 1-4% of the genome of non-African people is inherited from Homo neanderthalensis13. In some Asian populations we also find 4-6% inherited from the Denisova people (a yet undescribed species)14, and there is evidence of gene flow from a third archaic population15. So the diverse modern human global population is the result of intermixing with at least even three different species.

Before going too much into detail, there is also evidence from birds and other vertebrate groups. As an example, Darwin finches are known to hybridize, which influences each others’ evolution16.  In 2017, a Science paper announced the rapid speciation of a new Darwin’s finch lineage through hybridization17.

Now I have listed plenty of examples that show that hybridization and introgression played a role in the evolution of many different species and species groups, even and especially us humans, and there would probably be more if more were tested. The role of hybridization in vertebrate speciation should be considered well-supported by these recent studies.

Hybridization in nature

Natural hybridization not only occurs when lineages diverge or environments shift, but also happen in nature on daily basis in certain cases. I am going to go over these examples now.
Precisely I am talking about hybrid zones that exist when neighbouring closely related species interbreed. Classic examples are fire-bellied toads (Bombina), where the species Bombina bombina and Bombina variegata have a hybrid zone through Europe where their habitat overlaps. The hybrids are fully fertile, but have reduced evolutionary fitness. This limits the reproductive success of the hybrids, otherwise there would be a continuum between species. A wild case of natural hybridization in amphibians is Pelophylax. Pelophylax lessonae and P. ridibundus often overlap in range and produce fertile hybrids. These hybrids, known as the edible frog, however, passes on only one complete parental chromosome set and therefore never produces stable hybrids but the backcrossed offspring “reverts” to the parental species. Thus, edible frogs are classified as a kleptospecies, Pelophylax kl. esculentus.
In Canis, there is also frequent hybridization in the wild between the species. Gray wolves hybridize with golden jackals (for the reference, see the Species concept article), coyotes (the hybrid populations have been described as a separate species, Canis rufus, which is now called into question), and, as long as you regard them as a separate species, Timber wolves. Another mammal hybrid zone is that between the polar bear and brown bear, which has been addressed above already. Among megaherbivores, African savannah elephants Loxodonta africana and forest elephants Loxodonta cyclotis hybridize readily in overlap zones and form hybrid populations4.
Another classic example of a hybrid zone is that between the carrion crow (Corvus corone) and the hooded crow (Corvus cornix), which differ in plumage colour but are otherwise very closely related. Both species are also often listed as subspecies of one species or even only colour variants, but the subspecies issue will be treated in a separate post.
There are also plenty of examples from other animal groups and of course also plant species that form hybrid zones.

A special case that involves hybrid zones is that of a ring species. The ring species concept refers to a group of neighbouring populations that might also be recognized as distinct species (in which case it is more of a species ring instead of ring species), along an ecologic or geographic gradient. Directly neighbouring populations or species can interbreed, but not those at the respective ends of the chain. Examples for a ring species or species ring are salamanders of the genus Ensatina or the bird species Phylloscopus trochiloides.

Hybridization in conservation

Hybridization is also relevant for conservation. It is mostly considered a problem, even called “genetic pollution”. Why is that, considering that hybridization seemingly is a natural element of evolution and occurs frequently in the wild? There are, one the one hand, good reasons for that which I am going to outline now. But there are also examples and circumstances that should allow a reconsideration of regarding hybridization/introgression as “genetic pollution”.  

When cases of hybridization or introgression are referred to as genetic pollution it is because it is of anthropogenic cause either through invasive species, domestic animals or migration caused by climate change. A consistent influx of alien genetic material alters the allele frequency and diminishes the autochthonous genetic material, the genetic integrity, to a level that a species can go extinct on a genetic basis. This is especially a danger in populations or species that are already endangered. One example for a subspecies that has been lost through hybridization is the Barbary lion, Panthera leo leo. It is extinct in the wild, and in captivity zoos did not pay attention on not to mix subspecies. Nowadays, many lions in captivity that are managed without subspecies classification descended from Barbary lions, but there are no pure representatives of the clade anymore19. There has been announcements for a project to genetically breed-back the pure form, but the project seems to have died a silent death.
Mallard ducks Anas platyrhynchos have been introduced in various regions of the world, and they threaten the genetic integrity of numerous autochthonous species, such as A. rubripes, A. fulvigula, A. wyvilliana and A. superciliosa. American ruddy ducks Oxyura jamaicanensis threaten European A. leucocephala20.
The endangered Californian tiger salamander Ambystoma californiense is threatened by hybridization with the introduced Barred tiger salamander A. tigrinum, and the hybrids themselves cause ecological problems21. From the same salamander group, the Axolotl, is very endangered as well, and in aquarist keeping they sometimes are consciously crossed with tiger salamanders to produce more colour variants. Due to the lack of a transparent breeding book, this could become a problem for the species’ genetic integrity.

Moving back to mammals, another well known example of “genetic pollution” is the American bison. When the American bison went through the severe bottleneck at the end of the 19th century, herd keepers  experimented with cattle hybridization. Nowadays, nearly all herds tested contain genetic traces of domestic cattle22. The phenotypic legacy of this domestic cattle introgression can occasionally be seen in modern bison, it mostly shows in deviant horn shapes or tails longer than the norm for bison (see here, for example) although in most cases the introgression is invisible. However, bison with cattle introgression may have a fitness disadvantage under fully pure bison because they have a lower body mass in the wild23.

Now we come to the animal that concerns me the most, the European bison or wisent. In the 1920s, the species almost vanished due to hunting and habitat destruction, and all modern wisent descend from only 12 individuals. During this massive bottleneck event, there was intransparent hybridization with American bison and also domestic cattle. It was feared that pure wisents are going to disappear, which is why a breeding book was set up. Nowadays, the danger of pure wisents becoming swamped out by hybrids has been banned. Most modern wisent have a confirmed pedigree. They are pure but their extremely narrow gene pool is a drastic danger for the existence of the species. Epidemics and developmental problems cause high mortality rates or miscarriages both in the wild and zoos which is seen as a danger for the long-term survival of the species24. The hybridization with American bison back in the 1930s have mostly been executed in order to increase the genetic diversity and therefore reduce the impact of the severe inbreeding depression. While most of the hybrids have been culled later on, there is a Wisent population in the Caucasus mountains that still contains about 5% American introgression. It is phenotypically recognizable to some degree (see here). These “hybrids” are frowned upon some conservationists for phenotypical and ecological reasons that I cast in doubt in this post, and are the largest connected wild population of wisents with the longest history. Although it has not been directly tested, I think there is good reason to assume this population is healthier and has a higher evolutionary fitness due to the increased genetic diversity that is also under natural selective pressure. Therefore I actually consider this population very valuable, while some conservationists propose its extermination as it might be a danger for the purity (and thus genetic scarcity) of neighbouring wisent populations. In my opinion, the health and fitness of the Caucasus population should be evaluated, and if it indeed turns out to be higher or considerable higher than in pure and thus highly inbred wisents, which I assume to be likely, one might consider creating a third wisent breeding line with controlled transparent hybridization that aims to conserve the genetic integrity of the species but at the same time provide new allelic variation to overcome its sensitivity to diseases and developmental problems. I proposed this in the post linked above, and also donated for the wisent in the Caucasus.
Because it is my fear that the drastically narrow genetic diversity of the wisent might one day lead to animals that are pure on the one hand but not robust enough to establish and maintain wild or even captive populations, and that the wisent one day might not be able to survive on the long-term sight.

The main problem is the academic acceptance. All the studies I have cited in this posts are of recent years, therefore the numerous examples that underline the role of hybridization and introgression in species are known only since a short period of time. It will require some further studies and more years to pass until this knowledge has found its way into mainstream science and consciousness, and once it becomes accepted, it will start to influence conservational practise. Part of the problem also is that the out-dated concept of the 19th and 20th century of nature as a stable, balanced system that only changes in once in considerable geological timespans and of species as static entities with a clear, always tree-like phylogeny seems to be prevalent in the mind of many conversationalists, although modern science establishes a concept of nature as a dynamic system of constant changes that can also occur in a short period of time.
Conservationists have good reasons to condemn hybridization and introgression in most cases, especially uncontrolled in the wild, but there are also cases, such as in the wisent, where controlled and transparent hybridization or introgression could actually be beneficial for the survival of the species.


1 Ropiquet, Hassanin: Hybrid origin of the Pliocene ancestor of wild goats. 2006.
2 Jonsson et al.: Speciation with gene flow in equids despite extensive chromosomal plasticity. 2014.
3 Larsen, Marchan-Rivadeneira, Baker: Natural hybridiziation generates mammalian lineage with species characteristics. 2010.
4 Ewen Callaway in Nature News: Elephant history rewritten by ancient genomes. DNA from extinct species forces rethink of elephants’ family tree. 2016.
5 Ulrich, Linnenbrink, Tautz: Introgression patterns between house mouse subspecies and species reveal genomic windows of frequent exchange. 2017.
6 Amaral et al. 2014: Hybrid speciation in a Marine Mammal: The Clymene Dolphin (Stenell clymene).
7 Kumar et al. 2017: The evolutionary history of bears is characterized by gene flow cross species.
8 Miller et al. 2012: Polar and brown bear genomes reveal ancient admixture and demographic footprints of past climate change.
9 Figueiro et al. 2017: Genome-wide signatures of complex introgression and adaptive evolution in the big cats. 
10 Hassanin & Ropiquet 2007: Solving a zoological mystery: the kouprey is a real species.
11 Verkaar, Nijman, Beeke, Hanekamp, Lenstra: Maternal and Paternal Lineages in Cross-breeding bovine species. Has Wisent a Hybrid Origin?. 2004.
12 Soubrier et al.: Early cave art and ancient DNA record the origin of the European bison. 2016.
13 Federico Sanches-Quinto et al. 2012: North african populations carry the signature of admixture with Neanderthals.
14 Reich et al. 2010: Genetic history of an archaic hominin group from Denisova cave in Siberia.
15 Hammer et al. 2011: Genetic evidence for archaic admixture in Africa.
16 Grant, Grant 2015: Introgressive hybridization and natural selection in Darwin’s finches.
17 Grant et al. 2017: Rapid hybrid speciation in Darwin’s finches.
18 Gonzalez 2012: The pariah case: some comments on the origin and evolution of primitive dogs and on the taxonomy of related species.
19 Barnett et al. 2006: The origin, current diversity and future conservation of the modern lion (Panthera leo).
20 Rhymer 2006: Extinction by hybridization and introgression in anatine ducks.
21 Ryan, Johnson, Fitzpatrick 2009: Invasive hybrid tiger salamander genotypes impact native amphibians.
22 Derr, 2006: American bison: the ultimate genetic survivor.
23 Derr et al. 2012: Phenotypic effects of cattle mitochondrial DNA in American bison.
24 Mammal Research Institute, Polish Academy of Science: European Bison Bison bonasus: Current state of the species and an action plan for its conservation. 2002


  1. Hi Daniel, very detailed and interesting as always. With regard to the high mortality rates and developmental problems of wisent, do you know if this is observed over all populations of wisent, is it stabilising over time or getting worse? With increases in population sizes in some areas is the treat of inbreeding reduced or is the small effective population still insurmountable? Its amazing that Chillingham cattle survived!

    1. Hi, as far as I remember the report was not specifically on that. But considering the very high inbreeding coefficient (two randomly chosen wisents on this world are more closely related to each other than average human siblings), it could be well possible that larger populations suffer from the same problems. AFAIK, the second largest population in the wild is that in Tschernobyl. Perhaps that one is not well-studied due to its low accessibility.
      Chillingham cattle survived because when they went through the severe bottleneck event there was consequent artificial selection against weak and sick animals, thus deleterious alleles have been purged out. This is called purging and is also used when creating inbreeding lines in laboratory mice. Chillingham cattle are now pretty robust against foot-and-mouth disease, because they had it several times, but it is suspected they would be very sensitive to other diseases because of their narrow genetic base.

    2. Full siblings have an coefficient of 50%, and for Wisent :
      "44%, in the Lowland-Caucasian line 26%"
      (as you quoted in one of your articles)[1]
      So are there still healthy animals, or are they all already ill at some degree ?
      If it's about health, would it make sense to cross them with american Bison, or would this just result in diseases getting spread ?
      Regarding health, maybe it could make sense to cross both Plains and Wood-Bison with Wisent, with the amount of each admixture beeing related to the genetic diversity of each subspecies ?


    3. Thanks for correcting me, has been a while that I wrote the article. I had the numbers incorrectly in mind.

  2. If scientists can get a hold of some Wisent DNA from a Wisent that lived prior to the bottleneck, and if there was funding for it, then I am confident it would be possible to add back diversity using genetic rescue. These types of projects are starting be explored in America for animals such as the Black Footed Ferret; which also went through a massive bottleneck.

    That being said, I have no real issues with controlled hybridization with american bison to add in some diversity. I would want to keep the introgression levels around 1-2% max to minimize the risk of changing the character of the Wisent. The main reason I would oppose hybridization though is just that so many people, and governments, do not value hybrid animals.

    1. I actually proposed that idea in 2015
      Adding a sufficient amount of pre-bottleneck diversity into the modern wisent gene pool would be my first option before hybridization, but it is way more expensive and effortful. The problem is that probably too few people would care about this option.

  3. Then maybe it's the question if gene-editing will be developed fast enough before serious diseases through inbreeding are all around ? So maybe time is the enemy ?
    I wonder if 1-2% will have enough effect, maybe someone should do serious math about it if it's already the situation now that health could be traded off purity. I won't be surprised if an "0" is missing behind these numbers...