Holy Cow! Hybridization Facilitated Domestication and Adaptation of Cows

New study finds exchange of crucial genes between several cow species.

Humans are good at two things: telling stories and domesticating animals. A recent paper in Nature Ecology & Evolution explores both talents by studying the domestication of cows. Dong-Dong Wu and colleagues sequenced the genomes of several cow species (genus Bos) and uncovered a history heavily influenced by hybridization. The interbreeding of several cow species led to the exchange of particular genes, each with its own story to tell.

A quick word of caution. Genome-wide analyses often uncover interesting genes and it is very tempting to tell a story about these genes. We should be careful not to make up just-so-stories, no matter how plausible they might sound. Every gene story should be the starting point for further analyses. This is nicely illustrated by the first example.

The evolutionary history of cows. Arrows indicate introgression events (from Wu et al. 2018)

 

High Altitude Cows

Hybridization between yak and Tibetan cattle resulted in the introgression of genes involved in adaptation to high altitude (EGLN2 and HIF3α). Yaks have probably lived on the Tibetan plateaus for millions of years and have numerous adaptations to cope with the high altitude, such as enlarged lungs and hearts. Introgression of high-altitude-genes to Tibetan cattle helped these animals to survive on the Tibetan plateau.

Sounds plausible, right? The authors provide some extra evidence for this gene story. They compared the blood parameters in Tibetan cattle with and without the yak-like genes. Cattle with the introgressed genes showed higher lower haemoglobin levels and red blood cell counts, indicating adaptation to high altitude.

Interestingly, similar patterns have been documented in humans and dogs: Tibetans acquired genes from Denisovans, while the Tibetan mastiff received genes from Tibetan wolfs. In all cases, the beneficial genes came from related species that were already adapted to living at high altitudes.

A yak on the lookout.

 

Domestication Genes

Comparing the genomes of zebu cattle and gayal pointed to introgression of the gene SYN3. Doesn’t ring a (cow) bell? Knocking out this gene in mice results in animals that display less fear. This makes the gene particularly relevant for domestication, as domesticated animals show reduced fear towards humans.

Hybridization between zebu cattle and bali cattle resulted in the exchange of similar ‘domestication genes’ (SEPT5 and GP1BB). Again, knocking out SEPT5 in mice leads to reduced anxiety.

The zebu has been domesticated for much longer than gayal and bali cattle. The authors speculate that introgression of these genes facilitated successful domestication of the latter two species.

Hybridization between zebu cattle (picture) and other species, such as gayal and bali cattle, might have facilitated domestication of the latter.

 

The Changing View of Species

These examples show that hybridization can be an important player in adaptation and domestication. The authors conclude:

The changing view of the basic properties of species has profound implications for animal breeders and conservation biologists alike. Introgression and admixture has previously been considered a detrimental process to avoid. We now know that it is an important natural process of significant importance for adaptation.

 

References

Wu, D.-D., Ding, X.-D., Wang, S., Wojcik, J.M., Zhang, Y., Tokarska, M., Li, Y., Wang, M.-S., Faruque, O., Nielsen, R., Zhang, Q. & Zhang, Y.P. (2018) Pervasive introgression facilitated domestication and adaptation in the Bos species complex. Nature Ecology & Evolution.

 

Exploring gene tree discordance with lizards

Interesting new method to study gene tree discordance.

Different genes tell different stories. When you construct phylogenetic trees for several genes, chances are that you end up with a collection of discordant gene trees. This discordance can be the result of several biological processes, including hybridization. [If you want to know more about gene tree discordance, check out these excellent papers by Maddison (1997) and Degnan & Rosenberg (2009).] A recent paper in Journal of Evolutionary Biology introduces a new method to study this phenomenon.

 

Lizards

Melisa Olave and her colleagues explored the occurrence of hybridization in the South American lizard genus Liolaemus. This group of lizards comprises no less than 267 species and is distributed from southern Peru to southern Chile. Hybridization has been documented between numerous species. The current study focuses on hybridization between members of the boulengeri complex and the rothi complex.

Based on two mitochondrial genes and 12 nuclear loci, the researchers uncovered current and past hybridization between several species (check the paper if you are interested in which species exchanged genes). This hybrid history leads to high levels of gene tree discordance. To explore this phenomenon, they introduce a new statistic: the extra lineage contribution (XLC) statistic.

A member of the species-rich Liolaemus genus.

 

Exploring Gene Tree Discordance

Basically, the XLC quantifies the contribution of each sample (individual or allele) to the amount of gene tree discordance. Without going into technical details, the statistic calculates how many extra lineages are needed to reconcile a given gene tree with the species tree. The statistic ranges from 0 to 1, where 0 means no contribution and 1 indicates maximum contribution to gene tree discordance. If you want to try this approach on your own data, there is a R function available here.

This new statistic provides a useful tool to explore the contribution of particular individuals and genes to the discordance between gene trees and the species tree. A valuable resource in our quest to understand the evolutionary importance of hybridization.

 

References

Olave, M., Avila, L.J., Sites, J.W., Morando, M. (2018) Hybridization could be a common phenomenon within the highly diverse lizard genus Liolaemus. Journal of Evolutionary Biology, 31:893-903.

Are hybrids between capuchino seedeaters fertile?

A recent study uses captive breeding records to assess hybrid fertility in capuchino seedeaters.

If you explore this website (which I encourage you to do), you will notice that many avian hybrids have been documented. The latest estimate suggests that about 16% of bird species has hybridized with at least one other species. But are these hybrids also fertile? In many cases, we don’t have a direct measure of hybrid fertility and viability. A recent study in PLoS One tries to assess the fertility of Sporophila hybrids using captive breeding experiments.

 

Capuchino Seedeaters

The genus Sporophila contains 11 species of capuchino seedeaters that evolved in the last million years. The species differ in their male plumage, as illustrated by the excellent drawings by Jillian Ditner below. Based on abnormal plumage patterns, some hybrids have been documented in the wild. But nothing is known about their fertility. Leonardo Campagna and his colleagues compiled breeding data between 2006 and 2016 to explore hybrid fertility.

The variation in plumage patterns in eleven species of capuchino seedeaters. (Drawings by Jillian Ditner, Campagna et al. 2018)

 

Hybrid Fertility

The results showed that hybrid crosses had a higher hatching success than the pure ones. This might seem counter-intuitive, but the lower hatching success of conspecific pairs is probably a consequence of inbreeding in captivity. Nevertheless, the data show that in general Sporophila hybrids are fertile.

Further analyses revealed that hybrid crosses produced an excess of males and that some hybrid females were infertile. This observation is in line with Haldane’s Rule, which states that in hybrids, the sex with two different sex chromosomes (in birds, the females with ZW) will be the first to suffer from infertility or inviability.

 

Plenty of Plumage Patterns

Let’s focus on the plumage of the hybrids. In short, there was a lot of variation: some hybrids looked like their parents, some were intermediate and others showed completely new plumage patterns. This explains why it is so difficult to observe hybrid seedeaters in the wild. Some hybrids are just indistinguishable from the pure species.

Two male F1 hybrids. Can you guess which species hybridized here? You can find the answer at the end of the post.

 

A Final Lesson

The dataset in this study was not ideal to explore hybrid fertility in these birds. The authors write that ‘breeding records [were] originally compiled by hobbyist aviculturalists during efforts to establish lines of captive-born capuchinos that would alleviate the trapping pressure of wild birds from illegal pet trade.’  But I think they used the data to its full potential.

It does provide us with an important lesson: if possible, collaborate with bird breeders. These people have years of experience and often produced a wealth of data waiting to be analysed. During my PhD, I worked with waterfowl breeders to obtain blood samples from different goose species. I could not have finished my PhD without them!

 

References

Campagna, L., Rodriguez, P. & Mazzulla, J.C. (2018) Transgressive phenotypes and evidence of weak postzygotic isolation in F1 hybrids between closely related capuchino seedeaters. PLoS One, 13(6):e0199113.

 

This paper has been added to the Thraupidae page.

 

Solution to F1 hybrid pictures:

• Left = S. palustris (zelichi morph) x S. hypoxantha
• Right = S. ruficollis x S. cinnamomoea

Hybridizing hares: How the snowshoe hare got its brown coat

A cool example of adaptive introgression in the seasonal camouflage of snowshoe hares.

If you have ever taken an ecology course, you should know the snowshoe hare (Lepus americanus). Together with its predator, the lynx (Lynx lynx), the snowshoe hare is a textbook example of predator-prey interactions: “When the population size of the hare increases, there is more food for the lynx to eat. As a result the lynx population also increases. The large lynx population will kill more hares so the hare population decreases. This will also cause the hare population to decrease.”

The classical example of predator-prey interactions between lynx and snowshoe hare (from: http://www.occc.edu)

 

Camouflage

During winter, snowshoe hares are white, well-camouflaged against the snowy background. But when the snow melts, some hares molt into a brown fur, allowing them to blend in again. Keeping their white fur in a brownish landscape would make them an easy prey (nicely shown here). But the genetics of this seasonal camouflage were unknown. A recent paper in Science explores this uncharted territory and stumbles upon a fascinating result.

 

Finding the genes

To understand the genetics of fur color, you first need to know which genes underlie the trait. Therefore, Matthew Jones (University of Montana) and his colleagues sequenced the genomes of several snowshoe hares and tested which genetic markers associated with coat color. The researchers found a single region on chromosome 4, containing among others the pigmentation gene Agouti.

Further analyses, including a captive breeding experiment, showed that the uncovered genes acted like typical Mendelian traits. Hares that stay brown in winter have two recessive alleles (aa), while hares that turn white in winter have at least one dominant allele (Aa or AA). The textbook example of predator-prey dynamics also turned out to be a textbook example of Mendelian inheritance!

 

A snowshoe hare between white and brown fur (from: http://www.conservationmagazine.org)

 

Enter the jackrabbits

Comparing white with brown snowshoe hares revealed that the region in chromosome 4 was markedly different. This could be due to long-term maintenance of this polymorphism or introgression from another species. The results pointed to the latter possibility: the brown winter coats of the snowshoe hare were likely acquired through hybridization with black-tailed jackrabbits (L. californicus). This introgressed gene helped them to better cope with snowless conditions. A very nice example of adaptive introgression.

Hybridization with black-tailed jackrabbits probably led to the brown coat color of the snowshoe hare (from: http://www.wikipedia.com/)

 

References

Jones, M.R., Mills, L.S, Alves, P.C., Callahan, C.M., Alves, J.M., Lafferty, D.J.R., Jiggins, F.M., Jensen, J.D., Melo-Ferreira, J. & Good, J.M. (2018) Adaptive introgression underlies polymorphic seasonal camouflage in snowshoe hares. Science, 360:1355-1358.

How trees can drive fish speciation in the Amazon

New study tests Wallace’s intuition that water type can mediate fish diversification.

When I say ‘evolution’, you say ‘Darwin’. However, many people forget that the theory of evolution by natural selection was co-discovered by Alfred Russell Wallace. In fact, Darwin and Wallace presented their ideas in a joint paper entitled: “On the Tendency of Species to form Varieties; and on the Perpetuation of Varieties and Species by Natural Means of Selection.”

 

Wallace’s Intuition

Despite being less well-known than Darwin, Wallace contributed significantly to our current knowledge on evolution. For example, he identified a faunal divide in the Indonesian archipelago: the western part has animals of Asian origin, while the eastern part houses Australian animals. This dividing line is now known as the Wallace Line.

He also did fieldwork in the Amazon basin where he classified rivers based on their color and clarity: white, black and clear. When describing fish fauna in the Rio Negro (which is unsurprisingly a black river) he remarked that “Being a black-water river, most of its fishes are different from those found in the Amazon.‘

This suggestion – that fish speciation could be mediated by water type – was put to the test by Tiago Pires and colleagues in a recent paper in the Journal of Evolutionary Biology. They performed breeding experiments with the sailfin tetra (Crenuchus spilurus), a fish species that is comprised of two lineages: one restricted to the black Rio Negro and another that swims throughout several Amazonian white water rivers.

 

Two sailfin tetras in an aquarium (from: https://www.pinterest.co.uk/)

 

Breeding experiments

The researchers recorded the reproductive success of 322 couples, trying out three different combinations: two Rio Negro fish, two Amazon fish or a mixed couple. All aquariums were filled with water from the Rio Negro river. The results were clear (see figure below), fish from the Rio Negro has a higher reproductive success compared to the other combinations. There seems to be some degree of reproductive isolation between the two lineages.

What could have caused the lower spawning rate in the Amazon fish? The researchers think that these fish probably suffered from physiological issues in the black water (remember that all aquariums were filled with Rio Negro water). This water has a lower pH compared to the clear Amazon water. Rio Negro fish are adapted to this pH, Amazon fish are not. It would be interesting to see the results if the couples were swimming in white water. Would the Rio Negro fish then show lower reproductive success?

The outcome of the breeding experiments. Rio Negro fish show higher reproductive success compared to Amazon fish and mixed couples (from Pires et al. 2018)

 

What about the trees?

This study endorses Wallace’s intuition: Amazonian water type can mediate fish speciation. But what do trees have to do with all of this? The black waters are formed by incomplete decomposition of leaf litter from surrounding forests that grow on sandy soils. Hence, local forest and soil composition determine the water type of the river, which in turn drives fish diversification and speciation. So, indirectly trees drive fish speciation.

 

References

Pires, T.H., Borghezan, E.A., Machado, V.N., Powell, D.L., Ropke, C.P., Oliveira, C., Zuanon, J. & Farias, I.P. (2018) Testing Wallace’s intuition: water type, reproductive isolation and divergence in an Amazonian fish. Journal of Evolutionary Biology, 31:882-892.

Genetic Analyses confirm Hybridization in a Threatened Tern Species

New study finds evidence for hybridization between two tern species.

The global population of Chinese Crested Terns (Thalasseus bernsteini) comprises less than 100 individuals. All known breeding populations on mainland China and Taiwan are found within colonies of Greater Crested Terns (T. bergii). It is no surprise that mixed pairs were observed in these colonies. A new study in the ornithological journal Ibis now provides genetic evidence for hybridization.

 

A Chinese Crested Tern mounting a Greater Crested Tern (picture by Lin Chen; Yang et al. 2018)

 

DNA analyses

Jia Yang and colleagues collected DNA samples from five Chinese Crested Terns, six Greater Crested Terns and three putative hybrids. The two species – which turned out the be sister species – shared little genetic variants, while the putative hybrids showed an intermediate genetic make-up. The analyses thus clearly showed that hybridization occurs. But it is not certain whether the hybrids are fertile and backcrossing occurs.

 

Curse or blessing?

Hybridization might pose another threat to the already endangered Chinese Crested Tern. Although it depends how you look at it. On the one hand, gene flow from Greater Crested Terns might introduce new genetic variation into the small gene pool of the Chinese Crested Tern. A kind of genetic rescue. On the other hand, hybridization might lead to genetic assimilation and eventually extinction.

If hybrids are sterile, hybridization will definitely be a threat. Producing sterile offspring is a waste of reproductive potential. And if there are less than 100 individuals left, you don’t want to waste anything.

 

A breeding Chinese Crested Tern (from http://www.wikipedia.com/)

 

Hubb’s Principle

Finally, the behavioural mechanism responsible for hybridization between these tern species is Hubb’s principle, where species with a small population size are more likely to mate with a more abundant species because members of its own species are difficult to find. When explaining this in the paper, the authors refer to my 2016 review paper where I introduce this concept in the context of goose hybridization. I really appreciate the citation (and recommend others to cite it as well…)

 

References

Yang, J., Chen, G., Yuan, L., Huang, Q., Fan, Z., Lu, Y., Liu, Y. & Chen, S. (2018) Genetic evidence of the world’s most endangered tern, the Chinese Crested Tern Thalasseus bernsteini. Ibis

 

This paper had been added to the Charadriiformes page.

Do land bridges facilitate gene flow between island populations?

A new study on henna-tailed jungle-flycatcher and golden whistler might hold the answer to this question.

Most research on the Pleistocene ice ages has been focused on the Northern hemisphere where huge packs of ice covered the land. But what happened in the tropics? When large parts of the world’s seawater is locked up in ice, the worldwide sea levels will drop. In some regions, such as Australasia, this led to the formation of land bridges between islands. These bridges might enable previously isolated populations to come into contact and exchange genes. But do land bridges always lead to gene flow?

 

Sulawesi Islands

To answer this question, Kritika Garg and colleagues traveled to two Sulawesi islands: Peleng and Taliabu. These islands belong to different archipelago’s but have been connected by land bridges during the Pleistocene. The researchers looked for two bird species: the henna-tailed jungle-flycatcher (Cyornis colonus) and the golden whistler (Pachycephala pectoralis).

The golden whistler (from http://www.wikipedia.com/)

 

Introducing the Study Species

The golden whistler comprises a large radiation of numerous taxa across Melanesia. This study focuses on two subspecies: clio on Taliabu and pelengensis on Peleng. When it comes to diet, the golden whistler is a generalist that can easily switch between insects and seeds.

The henna-tailed jungle-flycatcher is divided into two subspecies which live on separate islands: one subspecies (colonus) occurs on Taliabu, while you can find the other subspecies (pelengensis) on Peleng. In contrast to the golden whistler, the henna-tailed jungle-flycatcher is specialized on catching insects in the air (hence the name flycatcher) and does not readily switch to a seed diet.

The henna-tailed jungle-flycatcher (from http://www.hbw.com/)

 

Land Bridge = Genetic Bridge?

The researchers collected DNA from henna-tailed jungle-flycatcher and golden whistler to reconstruct their evolutionary history. There was little evidence of genetic exchange between the jungle-flycatcher subspecies. Island populations of the golden whistler, however, have been exchanging genes during the Pleistocene. Genes mainly flowed from Peleng to Taliabu.

The differences in gene flow dynamics probably depend on the ecology of the species. The specialized jungle-flycatcher is known for its poor dispersal capacities. Because of its strictly insectivorous diet, it does not venture outside forests often. So, chances of crossing a land bridge are slim. The golden whistler, however, is a generalist that has little problems exploring new territories, including land bridges.

This study nicely shows that the existence of a land bridge does not automatically lead to genetic bridge between previously isolated populations. Other factors, such as ecology, should be taken into account.

 

References

Garg, K.M., Chattopadhyay, B., Wilton, P.R., Prawiradilaga, D.M. & Rheindt, F.E. (2018) Pleistocene land bridges act a semipermeable agents of avian gene flow in Wallacea. Molecular Phylogenetics and Evolution, 125:196-203.

 

The paper has been added to the Pachycephalidae page.