North-south divergence within Godlewski’s Bunting coincides with the uplift of the Tibetan Plateau

Genetic study uncovers deep genetic divergence within the Godlewski’s Bunting.

A few weeks ago, I wrote about the genetic structure in some corvid species (see here). Several species, such as the Rook (Corvus frugilegus), the Jackdaw (Corvus monedula and Corvus dauuricus) and the Eurasian Magpie (Pica pica), show a striking divergence between eastern and western populations. A recent study in the journal BMC Evolutionary Biology reports a similar pattern in the Godlewski’s Bunting (Emberiza godlewskii) with one important difference: the divergence is orientated north-south.


Godlewski’s Bunting © Jargal Lamjav | Wikimedia Commons


Five Genetic Markers

On the bushy slopes of China, you can sometimes catch a glimpse of the Godlewski’s Bunting. Although this small passerine is widely distributed in central China, little is known about its genetic structure and evolutionary history. That is why, Jiande Li and colleagues collected 190 samples across the range of this species. They sequenced three mitochondrial genes and two nuclear introns. The analyses of these markers revealed a deep divergence between two lineages.

The genetic split was dated to about 3.26 million years ago, which coincides with the uplift of the Qinghai-Tibet Plateau (QTP). This vast plateau probably divided the Godlewski’s Bunting into a northern and southern population. A similar pattern has been observed in the Tibetan Partridge (Perdix hodgsoniae).


Genetic analyses reveal a deep divergence within the Godlewski’s Bunting. From: Li et al. (2019) BMC Evolutionary Biology



The authors did not find strong evidence for historical gene flow, suggesting that both populations went their separate ways after the initial split. Their independent evolutionary paths are nicely illustrated by the demographic analyses: the northern lineage exhibited an intensive expansion whereas the southern population showed a lower rate of population growth. These differences can be attributed to habitat availability during the late Pleistocene. Ecological niche modelling indicates that the northern population had a bigger area at its disposal compared to the southern population.

In summary, the deep divergence observed in the Godlewski’s Bunting can be explained by a series of geological events (mainly the uplift of the QTP) and subsequent environmental changes during the ice ages.



Li, J., Song, G., Liu, N., Chang, Y., & Bao, X. (2019). Deep south-north genetic divergence in Godlewski’s bunting (Emberiza godlewskii) related to uplift of the Qinghai-Tibet Plateau and habitat preferences. BMC Evolutionary Biology19(1), 161.


Further Reading on Deep Genetic Divergences


Analyses of museum specimens uncover hybrid jays in Brazil

Ornithologists identified hybrids between Plush-crested Jay and the White-naped Jay.

In 2015, I estimated that about 16 percent of bird species hybridize. In that paper, I also wrote that “these numbers are most probably underestimates, given our generally poor knowledge of the breeding biology of several bird groups, such as cryptic tropical species.” There are probably numerous bird hybrids waiting to be discovered in the tropical regions. A recent study in the journal Zoologia reports such as case: two putative hybrids between the Plush-crested Jay (Cyanocorax chrysops) and the White-naped Jay (C. cynanopogon) in Brazil.


A Plush-crested Jay in Argentina © Tim Sackton | Flickr


Intermediate Specimens

In 1954, Pinto described a new taxon – called Cyanocorax chrysops interpositus – based on a single specimen. He considered is an intermediate form between Plush-crested Jay and the White-naped Jay (hence the name interpositus). A few decades later, John Hardy questioned the existence of this taxon and argued that it probably concerned aberrant specimens of the White-naped Jay (e.g., molting birds or subadults). Or could they have been hybrids?

Recently, Cristiane Apolinario and Luis Fabio Silveira found two museum specimens with intermediate plumage patterns. They analyzed the plumage characters and the geographical locations of these specimens. The birds showed intermediate traits when compared to the two Cyanocorax species. Specifically, the dark grayish brown color of the wings and light blue color of the neck. Moreover, both specimens were found in a contact zone between Plush-crested Jay and the White-naped Jay.


One of hybrid specimens (number 2) between Plush-crested Jay (1) and the White-naped Jay (3). Notice the brownish color of the wings and the white-blue pattern on the neck of the hybrid. From: Apolinario & Silveira (2019) Zoologia


Hybrid Zone?

The morphology and the geographical location of these specimens suggest that they are hybrids. But genetic data are needed to confirm this conclusion. Nevertheless, this interesting finding raises the possibility of a hybrid zone between these species. But why hasn’t this putative hybrid zone been found earlier? The authors offer two possible explanations: (1) the hybrids are too similar to the parental species to detect or (2) hybridization between these species is very rare. I think it is time for a trip to Brazil…


White-naped Jay © Hector Bottai | Wikimedia Commons



Apolinario, C., & Silveira, L. F. (2019). Hybridism between Cyanocorax chrysops and Cyanocorax cyanopogon (Aves: Corvidae) in Brazil. Zoologia, 36, 1.

Hardy JW (1969) A taxonomic revision of the New World jays. The Condor 71(4): 360–375.

Ottenburghs, J., Ydenberg, R. C., Van Hooft, P., Van Wieren, S. E., & Prins, H. H. (2015). The Avian Hybrids Project: gathering the scientific literature on avian hybridization. Ibis, 157(4), 892-894.

Pinto, O. (1954) Resultados ornitológicos de duas viagens científicas ao estado de Alagoas. Papéis do Departamento de Zoologia 12(1): 1–98.


This paper has been added to the Corvidae page.

Asian Leaf Warbler might carry mitochondrial DNA of an extinct species

Deep mitochondrial divergence can be explained by ghost introgression.

Extinct species can leave traces in the genomes of modern species. Human DNA, for example, contains genetic material from at least two extinct species, Neanderthals and Denisovans. And last year scientists found remnants of Cave Bear DNA (about 0.9 to 2.4 percent) in modern Brown Bears. These patterns are the result of ancient hybridization events between the species under investigation. Given the common occurrence of hybridization in birds, we can expect to find similar cases in our feathered friends. A recent study in the journal Molecular Biology and Evolution provides evidence for such a case.


Tickell’s Leaf Warbler © PJeganathan | Wikimedia Commons


Species Complex

The Tickell’s Leaf Warbler species complex contains three species: the nominal Tickell’s Leaf Warbler (Phylloscopus affinis), the Alpine Leaf-warbler (P. occisinensis) and the Sulphur-bellied Warbler (P. griseolus). The Alpine Leaf-warbler was only recently recognized as a distinct species, mainly based on divergence in the mitochondrial DNA. Analyses of this circular genome revealed that the Alpine Leaf-warbler diverged from the Tickell’s Leaf Warbler about four million years ago. However, the nuclear genome of these species is very similar, pointing to a speciation event only 600,000 years ago.

This phenomenon is called deep mitochondrial divergence (DMD) and can be caused by several evolutionary processes. Let’s have a look at the possibilities.


An example of deep mitochondrial divergence (DMD) in Asian Warblers. (a) Clear divergence between the three species based on mtDNA. (b) No divergence in nuclear DNA between affinis and occisinensis. From: Zhang et al. (2019) Molecular Biology and Evolution


Male-biased Disperal

When females stay in the breeding areas and males disperse widely, mitochondrial DNA (which is only inherited through the female line) can diverge while the nuclear genome (which is inherited from both parents) remains undifferentiated. However, this scenario is unlikely because females are generally the dispersing sex in passerines. So, we can easily reject this explanation.


Ancient Divergence

DMD can be due to an ancient differentiation event of mtDNA that did not involve nuclear DNA. This has been observed in some brood-parasitic birds and seems to be associated with host shifts of females. Because females show different behavior while males keep mating randomly, only female-linked traits (such as mtDNA and the W-chromosome) diverge. This results in mitochondrial divergence without nuclear differentiation. Because Leaf Warblers don’t show such female-specific behavior, the authors deem it unlikely that ancient divergence can explain DMD.

However, a recent study on the Savannah Sparrow (Passerculus sandwichensis) showed that divergent mitochondrial lineages can originate within a large panmictic population (see this blog post). They estimated that an effective population size of more than 350,000 is necessary for this to occur. The analyses of the Leaf Warblers show a peak in effective population size around 500,000, indicating that the mitochondrial divergence could have arisen within a large population.


Sulphur-bellied Warbler © Imran Shah | Wikimedia Commons


Ghost Introgression

The final possible explanation for DMD is ghost introgression: an extinct species of Leaf Warbler hybridized with the ancestor of present-day birds, resulting in the exchange of mtDNA. This idea is supported by some peculiar patterns in the nuclear genome. The researchers find several diverged regions in the nuclear genome and consider these remnants of the ancient hybridization events that resulted in the mtDNA transfer.

Although a scenario of ancient introgression is certainly possible, I am not sure if the researchers can reach this conclusion based on the current evidence. The possibility of DMD arising in a sufficiently large population (as explained above) makes me hesitant to declare the ghost introgression hypothesis as the winning explanation. More research is needed to discriminate between these explanations. One could, for example, test different introgression scenarios using Approximate Bayesian Computation (ABC) with deep learning, which has been done on human data. To be continued…



Barlow et al. (2018). Partial genomic survival of cave bears in living brown bears. Nature Ecology & Evolution, 2(10), 1563.

Benham & Cheviron (2019). Divergent mitochondrial lineages arose within a large, panmictic population of the Savannah sparrow (Passerculus sandwichensis). Molecular Ecology. 28(7), 1765-1783.

Martens et al. (2008). Intraspecific differentiation of Sino-Himalayan bush-dwelling Phylloscopus leaf warblers, with description of two new taxa. (P. fuscatus, P. fuligiventer, P. affinis, P. armandii, P. subaffinis). Vertebrate Zoology. 58(2):233-265.

Mondal et al. (2019). Approximate Bayesian computation with deep learning supports a third archaic introgression in Asia and Oceania. Nature communications10(1), 246.

Zhang, D. et al. (2019). “Ghost Introgression” As a Cause of Deep Mitochondrial Divergence in a Bird Species Complex. Molecular Biology and Evolution.


This paper has been added to the Phylloscopidae page.

The Smell of Speciation: Chickadees prefer the scent of their own species

Could odor cues promote reproductive isolation?

To understand the origin of new bird species, ornithologists have mainly studied characters such as plumage color and song. If birds look or sound different, they probably represent distinct species. But what about less obvious features? What about smell? Recent work has shown that odors play an important role in avian ecology and evolution (see this paper for a nice review). In songbirds, olfactory cues are most likely produced by the uropygial gland. This organ is situated at the base of the tail and secretes complex mixtures of chemicals (generally called preen oil). Could these oils contribute to avian speciation? A recent paper in the journal Ecology and Evolution put this idea to the test.


A Black-capped Chickadee perching on someone’s hand. © Chris | Flickr



Alex Van Huynh and Amber Rice focused on two chickadee species: the Black Capped Chickadee (Poelice atricapillus) and the Carolina Chickadee (P. carolinensis). These North American passerines interbreed along a hybrid zone, which has been studied extensively (you can check out the Paridae page for an overview). Because Black-capped Chickadee and Carolina Chickadee look very similar and can learn each others songs, these characters might not be reliable indicators in mate choice. Individuals can easily pick the ‘wrong’ species. Perhaps these birds use odor to chose their partner?



The researchers tested this hypothesis with an elegant experiment. They collected wild chickadees from the hybrid zone and placed them in a Y-shaped maze. Each arm of the maze contained the odor of one species (which was blown into the maze from a box containing a bird). Next, the researchers noted how much time the birds spend in the respective arms of the maze.

The results indicated that birds spend more time in the odor arm of their own species, suggesting that these birds can discriminate between species based on smell. Previous studies have reported similar results in other bird species, such Waxwings and Crimson Rosellas. But this is the first evidence of olfaction-based species discrimination in a natural hybrid zone.


The results from the experiment for (a) males and (b) females. Birds spend more time in the odor arm that contains the smell of their own species. From: Van Huynh & Rice (2019) Ecology and Evolution


The scent of hybrids

The results from this experiment are consistent with a possible role of odors in avian speciation. However, more work is needed to validate this idea. For example, what is the scent of hybrids? If hybrids smell different from ‘pure’ species, they might be less attractive and unable to find a partner. This selection against hybrids could increase genetic divergence between the species. In any case, this study shows that there is more to avian speciation than meets to eye (and ear).


A Carolina Chickadee © Dan Pancamo | Flickr



Caro, S. P., Balthazart, J., & Bonadonna, F. (2015). The perfume of reproduction in birds: chemosignaling in avian social life. Hormones and behavior68, 25-42.

Mihailova, M., Berg, M. L., Buchanan, K. L., & Bennett, A. T. (2014). Odour-based discrimination of subspecies, species and sexes in an avian species complex, the crimson rosella. Animal Behaviour95, 155-164.

Van Huynh, A., & Rice, A. M. (2019). Conspecific olfactory preferences and interspecific divergence in odor cues in a chickadee hybrid zone. Ecology and Evolution.

Zhang, Y. H., Du, Y. F., & Zhang, J. X. (2013). Uropygial gland volatiles facilitate species recognition between two sympatric sibling bird species. Behavioral ecology24(6), 1271-1278.


This paper has been added to the Paridae page.

Is there a hybrid zone between subspecies of the Scarlet Macaw?

A genetic study took a closer look at this colorful parrot.

Linneaus described The Scarlet Macaw (Ara macao) in 1758. The father of modern nomenclature considered it a monotypic species (i.e. no subspecies). However, a study of museum specimens led to the recognition of two subspecies: cyanoptera and macao. The former subspecies, which ranges from southern Mexico to central Nicaragua, is more robust and has a wide band of yellow feathers on its wing. The other subspecies can be found from southern Nicaragua to Brazil and has more pronounced green coloration on the wing. In 1994, David Wiedenfeld described an intergradation of these color variants in southern Nicaragua and norther Costa Rica. Could this be a hybrid zone?


The Scarlet Macaw © Morrisdelta | Wikimedia Commons


Hybrid Zone

A recent study in the journal Ibis used mitochondrial DNA to check whether there is a hybrid zone. Analyses of 100 samples revealed a clear distinction between the two subspecies, which probably diverged between 320,000 and 850,000 years ago. There was, however, no evidence for a hybrid zone. The subspecies were clearly separated in southern Nicaragua and did not share any mitochondrial variants.


Population Structure

Interestingly, the northern subspecies (cyanoptera) showed more population structure than the southern subspecies (macao). In the map below, you can see more mitochondrial haplotypes (represented by different colors) in cyanoptera compared to macao. The authors suggest that the cyanoptera populations were isolated into separate refugia during climatic oscillations. The macao populations, on the other hand, remained more stable during these shifts in climatic conditions.


Population structure in the Scarlet Macaw. The northern subspecies (cyanoptera) shows more fragmented population structure compared to the northern subspecies (macao). From: Schmidt et al. (2019) Ibis



Schmidt, K. L., Aardema, M. L., & Amato, G. (2019) Genetic analysis reveals strong phylogeographic divergences within the Scarlet Macaw Ara macaoIbis. Early View.


This paper was added to the Psittaciformes page.


Classifying Corvids: Peculiar phylogeographic patterns in the crow family

“And the crow once called the raven black.”

— George R. R. Martin

“As the crow flies” is a common expression to refer to the linear distance between two points. When you consider the current distribution of several crow species (family Corvidae), you will notice that they can fly a long way. Indeed, many corvids have wide distributions, sometimes ranging from Western Europe all the way to Eastern Siberia. This makes corvids excellent study systems for phylogeography, the study of the historical processes responsible for the contemporary geographic distributions of individuals. A recent paper in the Russian Journal of Genetics and Breeding nicely reviews the recent work on several members of the Corvidae.


A Carrion Crow © Andreas Trepte | Wikimedia Commons


Carrion and Hooded Crow (x2)

Let’s start with a textbook example: the hybrid zone between Western Carrion Crow (Corvus corone) and Hooded Crow (C. cornix). This contact zone runs from Scotland, through Denmark, Germany, the Czech Republic and Hungary, to Italy. Genomic analyses of this species pair revealed that they differed in just a few genomic regions, representing less than 1 percent of the genome. One of these differentiated regions contains contains genes involved in pigmentation and visual perception which might explain why these species mate assortatively (i.e. choose a partner with the same plumage pattern).

Interestingly, a similar hybrid zone occurs in Siberia. Here, Hooded Crow interbreeds with the Eastern Carrion Crow (C. orientalis). Genomic analyses of this hybrid zone showed that different genomic regions were differentiated compared to the European situation. This finding indicates that the genetic basis of speciation is highly species-specific and context-dependent. You can read this blog post for more information about this hybrid zone comparison.

Previous work on the Siberian hybrid zone also revealed that the Collared Crow (C. pectoralis) had the same mitochondrial haplotype as the southeastern Carrion Crow population. Perhaps it acquired this haplotype through hybridization?

crow hybrid zone

The locations of the European and Siberian hybrid zones between Hooded Crows and Carrion Crows. From: Vijay et al. (2016) Nature Communications


Medieval Transport?

An interesting hypothesis concerns the Azure-winged Magpie (Cyanopica cyanus). This beautiful bird has a peculiar distribution: one population occurs on the Iberian Peninsula while the other population is restricted to Eastern Asia. Some researchers argued that Portuguese and Spanish sailor might have transported these birds from Asia during Medieval times. Analyses of the mitochondrial gene cytb showed that these populations diverged more than three million years ago. This finding rejects the hypothesis of human-mediated transport. These birds probably had a wider distribution that was broken up during the Pleistocene ice ages.

The two populations are currently recognized as distinct species: the Asian Azure-winged Magpie (Cyanopica cyanus) and the Iberian Azure-winged Magpie (Cyanopica cooki).


A pair of Iberian Azure-winged Magpies © Mario Modesto Mata | Flickr


Comparative Phylogeography

Azure-winged Magpies are not the only corvids that show million-year-old divergences. A comparative study uncovered similar patterns in other species, such as the Rook (Corvus frugilegus), the Jackdaw (Corvus monedula and Corvus dauuricus) and the Eurasian Magpie (Pica pica). All of these corvids show significant divergence between eastern and western populations. Such divergence was absent for other species, including the Raven (Corvus corax), the Siberian Jay (Perisoreus infaustus) and the Nutcracker (Nucifraga caryocatactes). What could explain these patterns? The author of this review – Alexey Kryukov – thinks ecological differences might hold the key:

All species of the first group preferably nest in semi-open habitats and forest edges, while the second group (single-group species) live mainly in forests. The raven (C. corax) is an ubiquist. We arrived at the conclusion that a prominent factor influencing the pattern of genetic differentiation seems to be the preference for either open to semi-open habitats (the west-east pattern) or forest dominated habitats (the single group pattern). Separated refuge areas (western and eastern) during cold periods led to accumulation of diversity.


Comparative phylogeography of several corvid species shows a common east-west pattern (indicated in red and blue) in some species. Other species (in black) do not show this pattern. The explanation to this phylogeograhic phenomenon might be ecological. From: Haring et al. (2007) Molecular Phylogenetics and Evolution



Kryukov, A. P. (2019). Phylogeography and hybridization of corvid birds in the Palearctic Region. Journal of Genetics and Breeding, 23(2), 232-238.


This paper has been added to the Corvidae page.