With or without gene flow? Studying speciation in the Grey-headed Bullfinch species complex

Has there been past gene flow between populations on the Asian mainland and Taiwan?

In 2008, Albert Phillimore and his colleagues concluded that “allopatric speciation is the dominant geographic mode of speciation in birds.” Allopatric speciation refers to the situation where two populations become geographically isolated and genetically diverge, ultimately giving rise to new species. In recent years, however, the focus of speciation research has shifted from a purely geographical perspective (e.g., allopatry, parapatry and sympatry) to the consideration of gene flow. Geographical isolation is still an important component of speciation, but diverging populations often continue to exchange genes during the process. The high incidence of divergence-with-gene-flow examples has led to the idea that this might be the dominant mode of speciation in birds.

Land Bridges

The presence of some gene flow during speciation appears to have become the null hypothesis that many ornithologists start from. For instance, a recent study in the journal Molecular Phylogenetics and Evolution reconstructed the evolutionary history of Grey-headed Bullfinch (Pyrrhula erythaca) species complex. Different populations can be found on the Asian mainland (subspecies erythaca and erythrocephala) and on the island Taiwan (subspecies owstoni). During the Pleistocene ice ages, land bridges connected Taiwan with the mainland, potentially allowing gene flow between these populations. We can thus expect to find some signatures of past gene flow between the Grey-headed Bullfinch populations.

However, genetic analyses clearly separated the mainland and island populations. This separation does not completely rule out past gene flow, so the researchers performed coalescent modelling to test different speciation scenarios. This exercise pointed to a strictly allopatric speciation model. It seems that there has been no gene flow between the Asian mainland and Taiwan.

Sampling locations of the different populations in the Grey-headed Bullfinch species complex. Genetic analyses revealed a clear separation between island and mainland populations. From: Dong et al. (2020) Molecular Phylogenetics and Evolution.

Sky Islands

Why did these populations not exchange DNA despite the land bridges between Taiwan and the Asian mainland? The answer lies in their habitat preferences. Reconstructing the past distributions of these populations revealed that they never overlapped. The mainland populations resided in the mountainous areas and could not expand their ranges to the lowlands. Birds in these “sky islands” were thus isolated from lowland populations, such as the birds expanding from Taiwan. The researchers conclude that “unlike lowland species, incipient sky island species might have had
limited opportunities for intermittent secondary contact and gene flow during late Pleistocene sea-level fluctuations.” Indeed, other highland species, such as the Vinaceous Rosefinch (Carpodacus vinaceus) and the Taiwan Rosefinch (C. formosanus) also diverged without gene flow. The allopatric speciation model is alive and kicking!


Dong, F., Li, S. H., Chiu, C. C., Dong, L., Yao, C. T., & Yang, X. J. (2020). Strict allopatric speciation of sky island Pyrrhula erythaca species complex. Molecular Phylogenetics and Evolution153, 106941.

Featured image: Grey-headed Bullfinch (Pyrrhula erythaca) © Robert tdc | Wikimedia Commons

Splitting the Long-tailed Rosefinch into a Chinese and a Siberian species

Genetic and morphological data support the recognition of two distinct species.

“We echo calls for integrative taxonomy in which genomic and phenotypic data are considered on equal footing when delimiting species.” This concluding remark was stated by Carlos Daniel Cadena and Felipe Zapata in their recent review paper on species delimitation. I wholeheartedly agree with this statement. In fact, I have advocated this integrative approach to taxonomy in other blog posts (see for example here). The rationale behind this approach is quite straightforward: different taxonomic concepts and methods are combined in drawing species limits. Within this context, two general frameworks can be used: integration by congruence and integration by cumulation. The congruence approach entails that different data sets, such as molecular and morphological characters, support the decision to recognize certain taxa as valid and distinct species. In the cumulation approach, evidence from different data sets is gathered, concordances and conflicts are explained within the specific evolutionary context of the taxa under study, and based on the available evidence a decision is made.


Five Subspecies

The best way to highlight the importance and usefulness of integrative taxonomy is to see it in action. Luckily, a recent study in the Journal of Ornithology applied this strategy to the Long-tailed Rosefinch (Carpodacus sibiricus). The distribution of this species extends across a large part of eastern Asia. Based on its discontinuous distribution and some subtle differences in plumage, five subspecies have been proposed: the northern sibiricus, ussuriensis and sanguinolentus, and Chinese endemics henrici and lepidus. Simin Liu, Chentao Wei and their colleagues collected samples from all five subspecies and performed detailed genetic, morphological and acoustic analyses to determine how distinct these subspecies are. Perhaps some can be elevated to species rank?

The discontinuous distribution of the Long-tailed Rosefinch. The symbols correspond to different sampling locations for particular subspecies. Colors refer to resident (green) wintering (blue) and breeding (yellow) areas. From: Liu et al. (2020) Journal of Ornithology.


Two Clades with Similar Songs

Genetic analyses of the mitochondrial gene COI uncovered two main clades that correspond to the northern and southern grouping of subspecies. The northern clade consists of sibiricus, ussuriensis and sanguinolentus, while the southern clade comprises henrici and lepidus. Interestingly, the subspecies ussuriensis and sanguinolentus form a mixed group, suggesting that they should be considered one subspecies instead of two. The other three subspecies are clearly distinct lineages.

In contrast to the genetic analyses, there were no clear differences in songs. The authors write that “Overall, there was much overlap among the taxa and no clear separation was found, and there was no clear division between the songs of the northern and southern groups.” The lack of song divergence might be due to the recent origin of these groups (ca. 1.36 million years ago) or their allopatric distribution. The birds might not need species-specific songs because they rarely encounter other subspecies. There might thus be no strong selection that could lead to different songs.

The genetic analyses uncovered two main groups (left figure). All subspecies form distinct lineages, except for ussuriensis and sanguinolentus. There were no clear differences in songs between the subspecies (right). From: Liu et al. (2020) Journal of Ornithology.


Particular Plumage Patterns

What about morphological differences? Previous studies indicated subtle variation in plumage patterns. Although the authors did not perform a quantitative morphological analysis, they do describe notable differences between the northern and southern groups.

While adult males from the northern group have the entire forehead and crown silvery-pink, in the southern group the feathers of the forehead are silvery-pink, whereas the crown is reddish. The mantle of northern birds is pink to deep red with moderately broad brown streaking, while the mantle of southern birds is more brownish and less reddish. The northern taxa have broader median and greater covert wing bars, while the wing bars of southern birds are relatively narrow. Finally, the three outermost tail feathers are extensively white in northern birds, while in southern birds only the outermost feathers are extensively white, and the white part only covers less than half the length of the second outermost tail feathers.

Based on the gathered evidence, the researchers propose to split the Long-tailed Rosefinch into two species, namely the Siberian Long-tailed Rosefinch (C. sibiricus comprising the subspecies sibiricus and sanguinolentus), and Chinese Long-tailed Rosefinch (C. lepidus comprising the subspecies henrici and epidus). Would you agree?

The different subspecies show some subtle differences in plumage patterns. From: Liu et al. (2020) Journal of Ornithology.


Evolutionary History

Regardless of whether the northern and southern group will be recognized as distinct species, it is worthwhile to have a closer look at their evolutionary history. This north-south division between a Siberian-Japanese clade and a Chinese clade has been documented in other bird species and can probably be attributed to the mountains of northern and central China. The combined effects of the geographical isolation of these mountains and the changing vegetation during the Pleistocene turned this area into a formidable barrier for passerines, resulting in genetic divergence between separated populations.  Similarly, these two taxa in the southern group likely diverged in separate mountain ranges: henrici in the Hengduan mountains and lepidus in the Qinling Mountains and Yan Mountains.

Within the northern group, we see a east-west divide between sibiricus and ussuriensis/sanguinolentus. This pattern can be explained by historical glacial isolation in Siberia. It is possible that the eastern and western groups were connected by gene flow in the past. Indeed, one ussuriensis (in yellow) individual is nested within the sibiricus (in blue) group. Whether this concerns a misidentified individual or a signature of gene flow remains to be determined. I am secretly hoping for the latter explanation.



Liu, S., Wei, C., Leader, P. J., Carey, G. J., Jia, C., Fu, Y., Alström, P & Liu, Y. (2020). Taxonomic revision of the Long-tailed Rosefinch Carpodacus sibiricus complex. Journal of Ornithology, 161(4), 1061-1070.

Featured image: Long-tailed Rosefinch (Carpodacus sibiricus) © Попов Евгений | Wikimedia Commons

Solving the genetic mystery of the mosaic canary

Which genes are responsible for this peculiar plumage pattern?

Good scientific research resembles a thrilling mystery novel. Gathering clues, testing potential leads and critical thinking enable both detectives and scientists to solve the challenging questions. A recent study in the journal Science nicely illustrated this approach. The mystery: the genetic basis of red plumage coloration in captive canaries. These red canaries are the result of crossing the Common Canary (Serinus canaria) with the Red Siskin (Spinus cucullatus). Bird breeders have selected for this color pattern – commonly known as the mosaic phenotype – by consecutive backcrossing the hybrids with “pure” Common Canaries. Over time, the genome of resulting red canaries is largely Common Canary-DNA with a dash of Red Siskin. And this dash of DNA probably contains the genes responsible for the red plumage color.

Consecutive backcrossing between the Common Canary x Red Siskin hybrid and “pure” Common Canaries results in a genome that mainly consists of Common Canary DNA (light green) with a bit of Red Siskin-DNA (dark green). From: Gazda et al. (2020) Science.


Zooming in

Using a series of genomic techniques, the researchers zoomed in on the Red Siskin-DNA in the mosaic canaries. They narrowed the search down to a genomic region (on scaffold NW_007931177) with 52 genetic variants that were different between canaries with yellow and red feathers. The mosaic phenotype is a recessive trait, meaning that mosaic birds have the same genetic variant on both chromosomes (in other words, they are homozygous). This insight provides another important clue to solve the mystery. Which of the 52 genetic variants are homozygous for the Red Siskin in the mosaic canaries? Focusing on these homozygous variants pointed to a genomic region of about 36,000 DNA-letters, containing three genes: PTS (6-pyruvoyltetrahydropterin synthase), BCO2 (b-carotene oxygenase 2), and TEX12 (testis-expressed protein 12).

The genetic basis of red coloration is homozygous for Red Siskin DNA. This knowledge allowed the researchers to zoom in on a particular region with homozygous variants (highlighted in the black box). From: Gazda et al. (2020) Science.


Gene Expression

Now that we have three main suspects (PTS, BCO2 and TEX12) we can explore a next lead: differential gene expression. Mosaic males and females show distinct plumage patterns. Males accumulate more red pigment in their feathers than females. Hence, we can expect that the genes controlling red color are differently expressed in males and females. The researchers took a closer look at the expression patterns of PTS, BCO2 and TEX12 in regenerating feather follicles. One gene showed decreased expression in males compared to females: BCO2. Did we find the culprit?!

We know that BCO2 codes for an enzyme that plays an essential part in the degradation of carotenoids, the pigments responsible for red coloration. In mosaic males, this enzyme is not very active and does not break down many carotenoids, resulting in the accumulation of red pigment in the feathers. The mosaic phenotype is thus the outcome of sex-specific differences in BCO2-activity, suggesting that it is controlled by other regulatory sequences (the genetic on-and-off switches). These regulatory elements remain to be identified. We might have found the murderer, but we are still looking for the brains behind the crime.

Two genes (PTS and TEX12) did not show significant differences in gene expression between males and females (top boxes). The third gene (BCO2), however, was less active in males compared to females. Interestingly, the difference in gene expression was only apparent in feather follicles (lower left box) and not in the liver (lower right box). From: Gazda et al. (2020) Science.



Gazda, M. A. et al. (2020). A genetic mechanism for sexual dichromatism in birds. Science368(6496), 1270-1274.

Featered image: A mosaic canary © Fernando Zamora Vega | Shutterstock