Let me take a selfie: Scientists discover hybridization in a selfing fish

Newly discovered site in the Bahamas houses a hybrid between two groups of mangrove rivulus fish.

Self-fertilization is extremely rare in vertebrates. The mangrove rivulus is the only known vertebrate that routinely reproduces by selfing (teenagers taking selfies do not count). Given this peculiar mode of reproduction, hybridization should be rare. Or so you would think…

 

Three Groups

The mangrove rivulus currently comprises two species (Kryptolebias marmoratus and K. hermaphroditus), but can be divided into three main groups:

  1. Northern group in Florida and the Caribbean that corresponds to K. marmoratus
  2. Southern group in Brazil that corresponds to K. hermaphroditus
  3. Central group in the Caribbean that probably corresponds to a third species
rivulus.jpg

A selfing vertebrate, the mangrove rivulus (from: http://www.wikipedia.com/)

 

Natural Hybrids

A laboratory experiment already showed that hybridization between fish from the central group and K. hermaphroditus is possible. But does it also occur in nature? A recent study in the journal Biology Letters answers this question: yes!

Andrey Tatarenkov and his colleagues discovered a site in San Salvador (the Bahamas) where members from the central group and K. marmoratus coexist. This finding is already quite special because the three groups of rivulus were not known to co-occur. Genetic characterization of this population revealed a hybrid individual: a cross between a male K. marmoratus and a hermaphrodite of the Central group. Further analyses suggested that this hybrid has been selfing for two generations.

selfing hybrid.jpg

The hybrid (OY9 in the red circle) is genetically intermediate between K. marmoratus (left) and the central group (right). Pink squares are individuals from the newly discovered site in the Bahamas (from: Tatarenkov et al. 2018 Biology Letters)

How common hybridization is in this population and if there is gene flow between the different species/groups remains to be investigated.

 

References

Tatarenkov, A., Earley, R.L., Taylor, D.S., Davis, W.P. & Avise, J.C. (2018) Natural hybridization between divergent lineages in a selfing hermaphroditic fish. Biology Letters, 14:20180118.

 

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Several hybridization events shaped the evolution of Neotropical flycatchers (genus Elaenia)

Genetic analyses reveal at least two cases of hybridization in Elaenia flycatchers.

Reconstructing the evolutionary history of particular groups of species is still an important endeavor in biological research. Early studies used single genes (mostly mitochondrial ones) to build evolutionary trees. The possibility of sequencing multiple genes – or multilocus data – was a promising development, but revealed an unexpected pattern: different genes tell different stories. The disagreement between genes can be caused by rapid speciation events or hybridization. Both processes lead to similar genetic patterns and are difficult to tease apart. Hence, current research focuses on disentangling rapid speciation from hybridization. A recent study in Molecular Phylogenetic and Evolution attempted to do just that for Elaenia flycatchers.

 

21 Species

Flycatchers of the genus Elaenia are widespread throughout the Neotropics. Based on morphological data, they were divided into 18 species. Recent molecular work has uncovered some cryptic species, bringing the total of recognized species to 21. Qian Tang and colleagues sequenced nine loci for these 21 species to reconstruct their evolutionary past.

The analyses uncovered several instances of disagreement between genes. To figure out whether these results could be explained by rapid speciation or hybridization, the authors used the software package JML. This program can detect hybridization by comparing scenarios with and without gene flow between species. JML uncovered two cases of hybridization, involving yellow-bellied elaenia (E. flavogaster) and white-crested elaenia (E. albiceps).

yellow-bellied elaenia - hbw

A Yellow-bellied Elaenia on the lookout (from: http://www.hbw.com/)

 

Some Hybridization Events

The first case of possible hybridization concerns yellow-bellied elaenia and members of a subgroup with three species: small-billed elaenia (E. parvirostris), brownish elaenia (E. pelzelni) and large elaenia (E. spectabilis). It was not possible to pinpoint which of these three species hybridized with the yellow-bellied elaenia, although there were some indications that it was probably the large elaenia.

The second case was more straightforward. The white-crested elaenia mostly likely interbred with the small elaenia (E. pallantangae). This conclusion is supported by recent reports of hybrids between these species in Ecuador and Bolivia.

White-crested Elaenia - wiki.jpg

A White-crested Elaenia (from: http://www.wikipedia.com/)

 

References

Tang, Q., Edwards, S.V. & Rheindt, F.E. (2018) Rapid diversification and hybridization have shaped the dynamic history of the genus Elaenia. Molecular Phylogenetics and Evolution.

 

This paper has been added to the Tyrannidae page.

Coal tits exchange genes in central Europe

Genetic study of European coal tits reveals gene flow across a continental contact zone.

Hybridization is often studied in the context of hybrid zones. After a period of geographical isolation, populations might come into secondary contact and interbreed. In Europe, this scenario has been documented for numerous animal and plant taxa. The classical papers by Godfrey Hewitt (see for example herehere and here) describe an intriguing story of how populations were pushed in southern refugia by expanding ice sheets during the Quaternary (the geological period starting about 2.5 million years ago). Possible refugia included the Iberian peninsula, Italy and the Balkans. When the climate warmed and the ice retreated, these populations expanded from their refugia and recolonized the European continent. Organisms from different refugia met each other in different contact zones (see figure below).

hewitt map.jpg

Four examples of how hybrid zones (HZ) can be established as populations expand out of their southern refugia: (a) meadow grasshopper, (b) European hedgehog, (c) brown bear, and (d) common chub. From: Hewitt (2004).

 

German Coal Tits 

The establishment of a secondary contact zone has several possible outcomes: (1) the formation of a narrow hybrid zone, (2) a broad zone of intergradation, or (3) merging of both lineages. A recent study in the Biological Journal of the Linnean Society explored which of these outcomes best described the situation of the coal tit (Periparus ater).

The genetic analysis of this small passerine revealed that all German populations were a mixture of southern and northern populations. This amalgamation of coal tit genes was not restricted to a narrow contact zone, but expanded across a wide area of intergradation. This genetic pattern is supported by morphological data from previous studies that show how different subspecies gradually change from north to south.

1200px-Coal_tit_UK09

A Coal Tit (from http://www.wikipedia.com/)

 

Isolated Island Populations

In addition, island populations of the coal tit were genetically distinct from the mainland birds. The population on Cyprus (subspecies cypriotes) is a genetically and morphologically distinctive form. It probably dates back to an ancient colonization event. The genetic differences between the populations on Corsica and Sardinia (subspecies sardus) and the mainland are more subtle. These islands might have received – or are still receiving – gene flow from continental birds.

 

References

Tritsch, C., Stuckas, H., Martens, J., Pentzold, S., Kvist, L., Lo Valvo, M., Giacalone, G., Tietze, D.T., Nazarenko, A.A. & Päckert, M. (2018) Gene flow in the European coal tit, Periparus ater (Aves: Passeriformes): low among Mediterranean populations but high in a continental contact zone. Biological Journal of the Linnean Society, 124(3):319-338.

 

The paper has been added to the Paridae page.

 

 

 

On avian hybrids in the low countries

English summaries of two recent papers in Dutch journals.

Recently, I published two papers on avian hybrids in the Netherlands and Belgium. Because both articles were written in Dutch, I decided to provide short summaries here. The full texts are available through my personal website or in the references below.

 

Hybrid Geese in the Netherlands

The first paper appeared in the Dutch journal Limosa and concerns sightings of hybrid geese in the Netherlands. Based on data from the website waarneming.nl (the Dutch version of eBird), I gathered the observations of hybrid geese between 2005 and 2016. To be on the safe side, I only considered hybrids that were approved by the admins of the website and I corrected for observer bias in winter (when most birders report geese).

 

Grauwe Gans x Canadese Gans

Hybrid between Greylag Goose and Canada Goose

 

In total, 24 hybrid combinations were reported. The most common hybrids were Barnacle Goose x Canada Goose and Greylag Goose x Canada Goose. The former is often observed in the province of Noord-Holland where a mixed population breeds yearly. Hybrids between Greylag Goose and Canada Goose are mostly seen around Dutch cities, such as Nijmegen, Rotterdam and Groningen.

Next, I tested some hypotheses on the seasonal occurrence of goose hybrids. I expected that hybrids involving migrating species are mostly observed in winter, whereas hybrids with exotic species are observed year-round. And this is exactly what I found. For example, hybrids between Bean Goose and Greater White-fronted Goose are only seen in winter (see figure below).

kolgans x rietgans

Hybrids between Greater White-fronted Goose and Bean Goose are only reported in winter (from Ottenburghs 2018, Limosa)

 

Hybrids Raptors in Belgium and the Netherlands

My second avian hybrids paper was published in De Takkeling, the journal of the Dutch Raptor Working Group (edited by Rob Bijlsma). My approach was similar to the study on hybrid geese. This time, I collected sightings of hybrid raptors in the low countries. In contrast to geese, not that many hybrid raptors have been reported. This could be due to the rarity of these hybrids or the fact that they are difficult to identify in the field. Most hybrid raptors concerned falcons, which are mostly likely escapees from falconers. Other notable hybrids were Red Kite x Black Kite and Hen Harrier x Pallid Harrier.

hybrid falcon

Falconers often cross different species. Here is a gyr x saker falcon hybrid. (from https://commons.wikimedia.org/)

 

References

Ottenburghs, J. (2017) Waarnemingen van Hybride Ganzen in Nederland tussen 2005 en 2016. Limosa, 90(4):167-174. [PDF]

Ottenburghs, J. (2018) Hybride roofvogels in België en Nederland. De Takkeling. 26(2):178-182. [PDF]

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.

cows.jpg

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.

yak.jpg

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.

zebu.jpg

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.

1200px-Kaldari_Liolaemus_tenuis_01.jpg

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 LiolaemusJournal 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.

sporophila art

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.

Hybrid examples.jpg

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 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.

lynx-hare

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!

 

hare.jpg

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.

Jackrabbit2_crop.JPG

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.

 

sailfin.jpg

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?

graph pires.jpg

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.

 

terns

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.

 

Chinese_crested_tern_colony.jpg

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 bernsteiniIbis

 

This paper had been added to the Charadriiformes page.