What selection pressure is acting on hybrids between Audubon’s and Myrtle Warbler?

Another attempt to characterize the selection pressure acting on warbler hybrids.

What form of selection is acting on hybrids between Audubon’s Warbler (Setophaga coronata auduboni) and Myrtle’s Warbler (S. c. coronata)? It is a question that is haunting several American ornithologists. Genetic analyses of a hybrid zone between these species indicate that there is some selection against hybrids, but the exact mechanism remains a mystery.

Some weeks ago I wrote about a paper that tested whether parasites might be involved. The answer was negative, so the search for the exact selection mechanism continues. The latest attempt was recently published in the journal The Auk.


An Audubon’s warbler (from: https://www.allaboutbirds.org/)


Comparing Classes

David Toews and his colleagues wanted to know if there are any differences in viability between male and female hybrids or between different age classes. If they uncover differences, this might provide important insights into what kind of selection is acting on the hybrids.

Females might be less fit compared to males. This pattern – known as Haldane’s Rule – has been observed in several bird species. If Haldane’s Rule also applies to these warblers, we would expect to find more early-generation male compared to female hybrids.

There might also be differences between age classes due to variation in migration strategies. If difference species follow distinct migration routes, hybrids might opt for an intermediate – and possibly sub-optimal – route. This could increase the mortality rate among hybrids. If this is the case, we would expect more early-generation hybrids before their migration.


A female Myrtle warbler (from: https://www.allaboutbirds.org/)



To test these two expectations, the researchers used triangle plots (I have written about these before). Here is the crystal-clear explanation from the paper:

“In these plots, individuals near the top of the triangle are first-generation hybrids (i.e. they are heterozygous at nearly all the highly divergent sites). Individuals falling along the right and left edges of the triangle are backcrosses to the parental forms; individuals within the center of the triangle are F2, F3, and subsequent hybrid classes.”


A triangle plot to deduce the genetic ancestry of hybrids (from Toews et al. 2018, The Auk)


And the selection pressure is …

These triangle plots were compared between the different classes (males vs. females and pre-migration vs. post-migration) and revealed…no differences. There seems to be no selection against a particular sex or age class. Hence, the quest for the hybrid warbler selection pressure will continue.



Toews, D.P.L., Lovette, I.J., Irwin, D.E. & Brelsford, A. (2018) Similar hybrid composition among different age and sex classes in the Myrtle-Audubon’s warbler hybrid zone. The Auk, 135: 1133-1145.


The paper has been added to the Parulidae page.

Crisscrossing Europe: The genetics of crossbills in the western Palearctic

What drives genetic differentiation in European crossbills?

Crossbills are a textbook example of how adaptation to different resources can result in genetic differentiation. I remember reading a 2003 paper by Craig Benkman during my Masters in Antwerp. This article, entitled ‘Divergent selection drives the adaptive radiation of crossbills‘, featured a figure showing how groups of crossbills with different beak morphologies are adapted to different species of pine (see below). Later research showed that these distinct beak shapes result in several call types, which consequently leads to assortative mating (i.e. birds prefer a partner with the same call). In the end, this culminates in the build-up of genetic differentiation between the call types, the onset of ecological speciation!

This fascinating system has been studied for years in North America. But what about the crossbills in Europe? Do they show similar patterns? Thomas Parchman and his colleagues crossed the Atlantic to figure this out. Their findings recently appeared in the Journal of Evolutionary Biology.


Different groups of crossbills are adapted to different species of pine (from: Price 2008).


Should I stay of should I go now?

The European subspecies of the common crossbill (Loxia curvirostra) mostly feed on the Aleppo pine (Pinus halepensis), which occurs around the Mediterranean. Three subspecies are sedentary: balearica on Mallorca, poliogyna in northern Africa and hispana in Spain. The northern subspecies curvirostra, however, often undertakes long-distance movements when food resources are sparse. These nomadic ventures can be quite impressive, as noted by the English monk Matthew Paris:

“In 1254, in the fruit season, certain wonderful birds, which had never before been seen in England, appeared, chiefly in the orchards. They were a little bigger than Larks, and eat the pippins of the apples [pomorum grana] but no other part of them… They had the parts of the beak crossed [cancellatas] by which they divided the apples as with a forceps or knife. The parts of the apples which they left were as if they had been infected with poison.”


Geographical Isolation

The occasional movements of curvirostra into the distribution of other subspecies could potentially lead to hybridization and gene flow. To test this idea, the researchers compared genetic data from these European subspecies using a genotyping by sequencing (GBS) approach. The results indicated that balearica and poliogyna were clearly different from the other subspecies, probably because they are geographically isolated in Mallorca and northern Africa, respectively.


Two crossbills on a pine tree (from: http://www.wikipedia.com/)


Resource Competition

The degree of genetic differentiation between the Spanish hispana and the northern curvirostra suggests that other factors than geographical isolation are at play. The Spanish birds differ in beak morphology from their northern relatives because they are adapted to the local pine trees, which provide a stable food source. When nomadic curvirostra crossbills arrive in Spain, they would be outcompeted by the locally adapted hispana birds. This might prevent interbreeding and thus promote genetic divergence.


Parrot Crossbill

Finally, the researchers also compared the northern subspecies with the parrot crossbill (L. pytyopsittacus), a species that occurs in the same area. Previous analyses found no clear genetic differences between these species. The present study did uncover some genetic differentiation, suggesting that a few genomic regions are responsible for the morphological differences between common crossbill and parrot crossbill. A pattern that has been observed in other bird species as well (see for example wagtails and crows). Pinpointing these differentiated regions – and checking if they are related to adaptation to local pine species – is a promising next step. Fingers crossed!


A parrot crossbill – picture by Tom Melling (from: http:www.flickr.com/)



Parchman, T.L., Edelaar, P., Uckele, K., Mezquida, E.T., Alonso, D., Jahner, J.P., Summers, R.W. & Benkman, C.W. (2018) Resource stability and geographic isolation associated with genome divergence in western Palearctic crossbills. Journal of Evolutionary Biology


Are yellow-rumped warbler hybrids more susceptible to parasite infections?

Do parasites drive avian speciation?

Life as a hybrid is not always easy. They might be infertile or unattractive to potential partner. Or they might have a higher chance of dying. In other words, hybrids often have lower fitness compared to ‘pure’ species. But what factors determine this decrease in hybrid fitness? A recent study in the journal Ecology and Evolution focused on parasites.


One subspecies (coronata) of the Yellow-rumped Warbler complex (from: http://www.allaboutbirds.com)


Yellow-rumped Warblers

The Yellow-rumped Warbler (Setophaga coronata) complex comprises four subspecies (coronataauduboninigrifrons and goldmani). The first two interbreed along a narrow hybrid zone in British Columbia. Previous work indicated that there is selection against hybrids, but the exact mechanisms could not be unraveled. Camille-Sophie Cozzarolo (University of Lausanne) and her colleagues tested the hypothesis that hybrids are more susceptible to parasite infections. Specifically, they focused on haemosporidian parasites of the genera Haemoproteus, Leucocytozoon, and Plasmodium that are transmitted by dipteran flies.



On the one hand, hybrids might be an easy target for parasites because they lack the resistance that ‘pure’ species have evolved (this has been shown in black duck x mallard hybrids). On the other hand, the increased genetic diversity in hybrid genomes might confer an advantage when they get infected. In the present study, the authors expected that hybrids between coronata and auduboni will be infected more. In this way, parasites are (partly) driving the speciation process.


The other subspecies (auduboni) of the Yellow-rumped Warbler complex (from: http://www.wikipedia.com)



Contrary to their expectations, the researchers found no support for their parasite-driven speciation hypothesis. Hybrids did not have a higher infection prevalence. Instead elevation was the most important predictor of prevalence. This is probably because the vectors of certain parasites (particularly Leucocytozoon) thrive at higher elevations where they find suitable water bodies for reproduction.

In the case of Haemoproteus parasites, there was an effect of hybrid index (i.e. the genetic background of the birds). The probability of infection in coronata strongly increased with elevation. Possibly, coronata individuals do not cope well with high elevations, making them more vulnerable for infection.


Black flies (familu Simuliidae) are the main vectors of Leucocytozoon parasites (from: http://www.bugguide.net/)


Publication Bias

So, it seems unlikely that haemosporidian parasites play a key role in selecting against coronata auduboni hybrids. Although the outcome of this study is negative (it would have been very cool if parasites are driving bird speciation), it is important that this paper has been published. Only reporting positive results will lead to a publication bias and a skewed perspective on the role of parasites in bird evolution.



Cozzarolo, C.S., Jenkins, T., Toews, D.P.L., Brelsford, A. & Christe, P. (2018) Prevalence and diversity of haemosporidian parasites in the yellow-rumped warbler hybrid zone. Ecology and Evolution


This paper has been added to the Parulidae page.

Mixing in the Marshes: King rail and clapper rail hybridize in Virginia

Cryptic introgression between two rail species in Virginia.

Distinguishing between king rail (Rallus elegans) and clapper rail (R. crepitans) is challenging, to say the least. These secretive birds have similar diets, calls and morphology. In general, however, king rails are slightly larger and have a more deep rust-colored plumage compared to clapper rails. Despite their morphological differences, genetic studies indicated that these rails do represent distinct species.

king rail.jpg

A king rail (from: http://www.allaboutbirds.com/) © Luke Seitz



King and clapper rail prefer different kinds of wetland. King rails are mostly found in a diverse range of habitats from freshwater to brackish marshes, whereas clapper rails live exclusively in brackish and saltwater marshes. But where they overlap, they interbreed (as exemplified by the picture below showing a mixed pair). Stephanie Coster (West Virginia University) and her colleagues wanted to know if occasional hybridization results in gene flow between these species. Their results recently appeared in the journal Ecology and Evolution.

The researchers sampled birds across a salinity gradient on the east coast of the US. The genetic analyses – based on mtDNA and 13 nuclear markers (SNPs) – revealed several admixed individuals in Virginia. Most of these birds were backcrosses to clapper rail, indicating that hybrids are fertile.


A mixed pair of clapper rail (left) and king rail. Picture taken by Robert Ostrowski (from: Coster et al., 2018)


Wave-front Dynamics

The uncovered genetic patterns fit an evolutionary history proposed by Storrs L. Olson in 1997. He envisioned that an ancestral population of king rails was adapted to freshwater. Birds at the periphery became isolated due to rising sea levels and adapted to salty environments. These birds would evolve into clapper rails. Later on, this new lineage expanded into brackish habitats, thereby displacing the resident king rails.

Initially, the expanding clapper rails are outnumbered by king rails, leading to hybridization. As the expansion proceeds, king rails and previously produced hybrids are engulfed by clapper rails, thereby overturning the numerical imbalance. Consequently, hybrids have a higher chance of backcrossing with clapper tails, resulting in a genetic wake of introgressed genes following the wave-front of the expanding clapper rails.


A clapper rail (from: https://www.audubon.org/)



Coster, S.S., Welsh, A.B., Costanzo, G., Harding, S.R., Anderson, J.T., McRae, S.B. & Katzner, T.E. (2018) Genetic analyses reveal cryptic introgression in secretive marsh bird populations. Ecology and Evolution.


The paper has been added to the Gruiformes page.

Looking for genetic differences between Araripe and helmeted manakins in Brazil

Is it possible to detect genetic differences between Antilophia manakins?

One of the outstanding questions in biology is the relationship between genotype and phenotype: how does the genetic make-up of an individual translate into physical characteristics? This question becomes even more daunting when comparing different species. Some species pairs are genetically distinct but look almost exactly the same (so-called cryptic species), whereas other species pairs are genetically nearly identical but look totally different. A recent study in Molecular Ecology explores the latter situation in Antilophia manakins.


Black and White

In Brazil, you can find two species of manakin that look quite distinct. Males of the Araripe manakin (A. bokermanni) are white, whereas the plumage of Helmeted manakin males (A. galeata) is black. Despite the obvious color differences, genetic studies – using mtDNA and introns – could not detect any population structure. This finding could be explained by (1) recent divergence with gene flow or (2) lack of statistical power of these studies.

araripe manakin.jpg

The white Araripe manakin (Antilophia bokermanni) – from: http://www.hbw.com/


Conservative Measures

To differentiate between these two possibilities, Fabio Raposo do Amaral and his colleagues focused on another molecular marker: ultraconserved elements (UCEs). Analyses of these genomic regions revealed clear differentiation between Araripe and helmeted manakin. It thus seems that the statistical power of the previous studies was just too low to pick up any signal of population structure. In addition, demographic modelling indicated that there has been no (or very little) gene flow between these two species.

helmeted manakin.jpg

The black helmeted manakin (Antilophia galeata) – from: http://www.hbw.com/


Male Plumage

Araripe and helmeted manakin are genetically distinct, but how did the males of these species evolve different plumage patterns? Perhaps these colors have been under strong sexual selection, with Araripe females preferring white and helmeted females preferring black males. Or maybe the white plumage of Araripe males simply increased in frequency due to genetic drift in a small isolated population.

To answer these questions, a genomic approach might be warranted. Indeed, the authors write that “resequencing of their complete genomes will offer exciting opportunities to identify functionally important regions evolving under selection, which may include candidate genes related to the plumage differences between those two species.”



Amaral, F.A., Coelho, M.M., Aleixo, A., Luna, L.W., Rego, P.S., Araripe, J., Souza, T.O., Silva, W.A.G. & Thom, G. (2018) Recent chapters of Neotropical history overlooked in phylogeography: shallow divergence explains phenotype and genotype uncoupling in Antilophia manakins. Molecular Ecology.