It takes two: The evolution of duets in New World warblers

Ornithologists uncover relationship between duets and migration.

Everybody knows that birds sing. But did you know that some species sing duets? Males and females sometimes combine their songs into a harmonious melody. The Carolina Wrens (Thryothorus ludovicianus), for example, produce a primitive duet. The male sings a song that sounds like tea-kettle, tea-kettle, tea-kettle, and from time to time the female jumps in with a buzzy sound. You can listen to such a duet in the video below.


Pair Bonds

Ornithologists think that birds mainly sing these duets to defend their territories. In addition, duets might also play a role in strengthening pair bonds. The more time birds spend together, the more likely they will evolve the ability to produce duets. The duration of a pair bond can be limited by migration during which partners go their separate ways. So, you would expect that duets are negatively associated with migration. A recent study in the journal The Auk tested this prediction for the bird family Parulidae (the New World warblers).


A singing Common Yellowthroat (Geothlypis trichas). However, this species does not duet. © Wolfgang Wander | Wikimedia



Liam Mitchell and his colleagues investigated 107 species of warblers and found evidence for duets in 19 species. When they correlated this behavior with migratory strategies, they uncovered a significant relationship. In line with the prediction outlined above, birds that produce duets tend to be sedentary. The researchers also reconstructed the evolutionary history of duets, revealing that this behavior evolved several times (concentrated in particular genera, such as Myioborus and Myiothlypis). The ancestor of these birds probably did not sing duets.


The evolutionary history of duets and migration in the New World warblers. Birds that sing duets (red dots on the left) tend to be sendentary (blue dots in the right). From: Mitchell et al. (2019) The Auk


A role for hybridization?

One big assumption in this macro-evolutionary study is that the traits under investigation (here, duets and migration) follow the species tree. But this does not have to be the case (see this commentary in Evolution). If traits have a genetic basis, they could be exchanged between species by hybridization. On the evolutionary tree, it might seem like an independent origin, while in reality the trait was transferred during a hybridization event.

I don’t know whether this scenario applies to the duet behavior in New World warblers. These birds are known to hybridize extensively (see here for an overview), but the genetic basis of duets is – to my knowledge – still a mystery. It would be interesting to pinpoint the genes underlying this behavior and reconstruct their evolutionary history. Will they follow the species tree?



A duetting species from Costa Rica, the Collared Whitestart (Myioborus torquatus) © Cephas | Wikimedia Commons



Hahn, M. W., & Nakhleh, L. (2016). Irrational exuberance for resolved species trees. Evolution, 70(1), 7-17.

Mitchell, L. R., Benedict, L., Cavar, J., Najar, N., & Logue, D. M. (2019). The evolution of vocal duets and migration in New World warblers (Parulidae). The Auk: Ornithological Advances, 136(2), ukz003.



A philosopher claims species do not exist. He is wrong.

What is a species?

Philosophers think a lot. Sometimes they think so much that they get entangled in their own thoughts and do not see the flaws in their reasoning (theology is the perfect example of this). Henry Taylor – a philosopher from the University of Birmingham – wrote an article on The Conservation in which he claims that species do not exist. He argues that we should scrap the idea of a species and “think of life as one immense interconnected web.” His article has already been criticized by evolutionary biologist Jerry Coyne. I recently published a book chapter on avian species concept, so this is a nice opportunity to summarize this chapter and correct the sloppy reasoning of this philosopher.


There are about 10,000 bird species. And they do exist. From:


We know what a species is…in theory

After a general introduction about taxonomy, Taylor writes the following sentence: “So, what even is a species? The truth is, we don’t really have any idea.” Actually, we do have an idea. But to understand the solution to this species problem, we need to make a distinction between the theoretical question of what species are (i.e. species concepts) and the ways in which species can be delimited in practice (i.e. species criteria). From a theoretical point of view, we know what species are. This part of the species problem was independently solved by Richard Mayden and Kevin De Quieroz.

Richard Mayden examined 22 distinct species concepts and proposed a hierarchy of species concepts, with a primary theoretical species concept and several secondary operational species concepts. He argued that only one concept is suitable as primary concept, namely the Evolutionary Species Concept: “A species is an entity composed of organisms which maintains its identity from other such entities through time and over space, and which has its own independent evolutionary fate and historical tendencies”. The remaining, secondary concepts function as guidelines that are essential for the study of species in practice. So, they are actually species criteria instead of concepts.

Similarly, Kevin De Queiroz reviewed several existing species concepts and argued that all existing species concepts are variants of a single general concept, which he dubbed the General Lineage Concept. Species are considered separately evolving metapopulation lineages. A lineage indicates an ancestor-descendant series, and metapopulation refers to an inclusive population made up of connected subpopulations.


The hierarchy of species concepts with an overarching primary concept (i.e. the Evolutionary Species Concept) and several secondary concepts that are used as criteria. From: Mayden (1997) Species: The units of diversity.


A Life History Approach

So far, so good. From a theoretical point of view, we can define species according to the Evolutionary Species Concept and the General Lineage Concept. But what about species delimitation in practice? Which secondary concepts should we use? That choice will depend on the evolutionary history of the species in question. Here, a “life history approach” is warranted, in which different species concepts correspond to different stages in the life history (i.e. speciation process) of a species.

It is important to keep in mind that the order in which species concepts arise is contingent upon the speciation process. In some cases, morphological differentiation might evolve first, followed by reproductive isolation. In other cases, it might be the other way around. And in yet other cases, some species concepts will not apply.

Moreover, during the speciation process, there will be a grey zone in which different species criteria come into conflict. For example, several putative species of Redpoll Finches (genus Acanthis) are morphologically different despite largely undifferentiated genomes. There is a conflict between a morphological and a genetic species concept. What should taxonomists do now? The answer is integrative taxonomy.


This simplified diagram represents a single lineage splitting into two independently evolving lineages (or species). The horizontal lines represent the times at which the lineages acquire different properties (e.g. they become phenetically distinguishable, reproductively isolated, reciprocally monophyletic, etc.). This set of properties (SC species concept) coincides with a grey zone in which alternative species concepts come into conflict. On either side of the grey zone, there is agreement on the number of species. Adapted from De Queiroz (2007) Systematic Biology.


Integrative Taxonomy

The rationale behind integrative taxonomy is quite straightforward: different taxonomic concepts and methods are integrated in the delimitation and description of species. A recent paper on taxonomic bird studies found that nearly half (46.5%) applied multiple criteria in species delimitation. Within this context, two general frameworks have been advocated: integration by congruence and integration by cumulation.

The congruence approach to species delimitation entails that different data sets, such as molecular and morphological characters, support the decision to recognize certain taxa as valid and distinct species. For example, Per Alström and his colleagues used congruence between plumage, biometrics, egg coloration, song, mitochondrial DNA and distribution to draw species limits in the Bradypterus thoracicus complex. The main advantage of this approach is that most taxonomists will agree on the validity of a species supported by several independent data sets, leading to taxonomic stability.

The alternative framework, integration by cumulation, is based on the assumption that any of the data sets can be used as evidence for the delimitation of species. Congruence is desired but not necessary. In practice, evidence from different data sets is cumulated, 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. An advantage of this approach is that species delimitation is not restricted by one particular biological property.


Species limits in the Bradypterus thoracicus complex were determined using an integrative approach based on several criteria. From:


An Interconnected Web

I hope that the explanations above have convinced you that species do exist and that we can define them in practice (although drawing species limits is not always straightforward). What about the statement by Henry Taylor that “we should think of life as one immense interconnected web.” I agree with this statement but it does not lead to the conclusion that species do not exist.

Hybridization is a common phenomenon (as this website clearly shows for birds). Numerous species are known to exchange genetic material through hybridization. But does that invalidate their rank as distinct species? No, despite the occasional genetic contribution of other taxa, species tend to maintain their own identity with their own independent evolutionary fate and historical tendencies (as stated by the Evolutionary Species Concept).

In the end, Taylor writes that “there is no such thing as ‘the human species’ at all.” He does not explain the exact reasoning behind this bold statement, but I assume he refers to the interbreeding between humans, Neanderthals and Denisovans. Does gene flow between these members of the genus Homo result in the disappearance of the species Homo sapiens? Of course not! The genes that we obtained from Neanderthals and Denisovans have certainly influenced our consequent evolution but overall the human species has maintained its own identity with its own independent evolutionary fate and historical tendencies (sorry to repeat this concept, but I really want to drive the point home here).


The complex evolutionary history of humans with multiple events of interbreeding with Neanderthals and Denisovans. From: Callaway (2016) Nature


Avian Species Concepts in the Light of Genomics

I will end my discussion of the species problem here. To summarize, the species problem can be partly resolved by theoretical monism (the evolutionary species concept or general lineage concept) in combination with practical pluralism, in which different species criteria correspond to different stages during the speciation process.

In my book chapter on species concept, I focused on the role of genomics in this debate. If you are interested in this question, feel free to contact me for a PDF of the chapter. I will paste the main points from the abstract below:

In this chapter, I argue that genomics provides another line of evidence in this pluralistic approach to species classification. Indeed, genomic data can be combined with classical species criteria, such as diagnosability, phylogeny and reproductive isolation. First, genomic data can provide an extra diagnostic feature in species delimitation. Compared to ‘old-school’ genetic markers, the use of genome-wide markers leads to a significant rise in statistical power. Second, phylogenomic analyses can resolve the evolutionary relationships within rapidly diverging or hybridizing groups of species while taking into account gene tree discordance. Third, genomic data can be used to pinpoint the genetic basis of reproductive isolation and provide a detailed description of the speciation process. All in all, the genomic era will supply avian taxonomists with a new tool box that can be applied to old concepts, leading to better informed decisions in cataloguing biodiversity.



Ottenburghs, J. (2019). Avian species concepts in the light of genomics. In Avian Genomics in Ecology and Evolution (pp. 211-235). Springer, Cham.


Can Mandarin Ducks hybridize with other duck species?

Send me your pictures of Mandarin Duck hybrids!

This week, Jan Harteman (from Harteman Wildfowl) asked me if Mandarin Ducks (Aix galericulata) hybridize with other duck species. Someone once told him that this duck species cannot interbreed with other ducks because of a difference in chromosome number. My overview of duck hybrids on the Anseriformes page lists six captive crosses with Mandarin duck:

  • Wood Duck (Aix sponsa)
  • Laysan Duck (Anas laysanensis)
  • Mallard (Anas platyrhynchos)
  • Gadwall (Anas strepera)
  • Redhead (Aythya americana)
  • Long-tailed Duck (Clangula hyemalis)

The colorful Mandarin Duck © Alexandra Sora | Wikimedia Commons


Reliable Sources?

These hybrid records are based on the Serge Dumont Bird Hybrid Database, which provides references for all the listed hybrids. Most of the reported hybrids can be traced back to the Hybrid Ducks inventory of Eric and Barry Gillham. A few hybrids are supported by older articles in the Avicultural Magazine, namely “On Mandarin Duck Hybrids” by Prestwich (1960) and “Reference to possible Mandarin x Wood (Carolina) Duck and Wood Duck x Mandarin Hybrids Bred at Tracy Aviaries, Salt Lake City” by Anon (1965). Unfortunately, I cannot access these articles and judge their reliability.

There is, however, a paper by Paul Johnsgard on these putative hybrids. He provides good evidence for the Mandarin Duck x Laysan Duck hybrid but casts some doubt on the crosses with Long-tailed Duck and Redhead. In addition, he described some possible hybrids between Mandarin Duck and Wood Duck. It seems that these two species can interbreed.


A putative hybrid between Mandarin Duck and Wood Duck © Quartl | Wikimedia Commons



The idea that Mandarin Ducks cannot hybridize with other species due to a chromosomal difference has a long history. Johnsgard writes the following.

Prestwich (1960) and Gray (1958) have concluded, mirroring Delacour and Mayr (1945) and Seth-Smith (1922), that the Mandarin Duck is unable to hybridize, even with its nearest living relative the Wood Duck. The explanation usually advanced for this seemingly unique situation is a reportedly an aberrant chromosomal condition of the Mandarin Duck (Yamashima 1952).

I could not access the paper by Yamashima, but I did find the karyotype for the Mandarin duck in another study. This duck has 84 chrosomosomes whereas other ducks have 80. This difference could prevent the production of hybrids. However, horses (with 64 chromosomes) and donkeys (with 62) can interbreed and the resulting offspring, mules and hinnies, have 63 chromosomes. Perhaps other chromosomal rearrangements might have occurred in the Mandarin Duck genome? Indeed, in the book “The Cell Nucleus“, I found that all the chromosomes of the Mandarin Duck are acrocentric, meaning that one chromosomal arm is much shorter than the other. In other duck species, the chromosomes can also be submetacentric (i.e. one chromosome arm is somewhat shorter than the other). This different chromosomal shape could explain the difficulty of producing hybrids with this species.


The different types of chromosomes. Mandarin Ducks only have acrocentric chromosomes (highlighted with black box). From:



Anon (1965) Reference to possible Mandarin x Wood (Carolina) Duck and Wood Duck x Mandarin Hybrids Bred at Tracy Aviaries, Salt Lake City. Avicultural Magazine, 71(3), 96-97.

Johnsgard, P. A. (1968). Some putative Mandarin Duck hybrids. Bulletin of the British Ornithologists Club, 88, 140-148.

Prestwich A. A. (1960) On Mandarin Duck Hybrids. Avicultural Magazine, 66(1), 5-8.

Shields, G. F. (1982). Comparative avian cytogenetics: a review. The Condor, 84(1), 45-58.


Thanks to Jan Harteman for bringing this mystery to my attention. If you have any burning questions about avian hybrids, feel free to contact me.

The social lives of quails: Why do California and Gambel’s quail hybridize?

Social network analyses might provide the answer to this question.

Why do some birds choose a partner from a different species? Couldn’t they find a member of their own species? Did they want to try something new? Or did they just make a mistake? These questions come to mind when you observe a hybrid individual in the wild. A recent study, published in The American Naturalist, tries to solve this conundrum for a pair of quail species (genus Callipepla).


Hybrid Zone

California Quail (C. californica) and Gambel’s (C. gambelii) Quail are sister species that hybridize along a contact zone in Southern California. Previous work showed that these species can discriminate between each other in captivity. In the wild, however, mating seems random, resulting in mixed pairs and consequently hybrids. These patterns raise the question how quails choose a partner.


A California Quail © Alan Schmierer | Flickr


Social Interactions

To investigate the mating patterns of these quails, David Zonana and his colleagues turned to social network analyses. They equipped several birds with automated radio-frequency identification tags that generate detailed data on which individuals interact with one another. These interactions can be visualized in social networks in which the individuals represent dots and the connecting lines (or edges) indicate the strength of interaction. The figure below shows the social network for the quails.

Analyses of these social networks can tell us more about the way quails select their partner. Surprisingly, they do not use species-specific plumage during mate choice. These plumage patterns did not correlate with the structure and strength of the associations in the network. Instead, the birds focus on two other characteristics: body mass and monomorphic plumage (i.e. the same in both sexes).


A social network for the California Quail and Gambel’s Quail. The dots represent individuals (blue = male, orange = female) and the lines indication interactions. The thicker the lines, the stronger the association. From: Zonana et al. (2019) The American Naturalist


Body Mass and Shared Plumage Patterns

Pairing up by body mass is consistent with a previous study on Gambel’s Quail. This study found that larger males are more likely to win competitions with other males. Consequently, these males have first pick with the females and they settle down with large females that are more experienced. This choice increases the chances of a successful brood.

The second cue for mate choice is monomorphic plumage. Given that quails can discriminate between species in captivity, it is surprising that they pair up with individuals that look similar to them. This pattern suggests that quails are sexually imprinted in particular plumage traits that are shared by males and females. Which specific traits are used by the quails remains to be determined.


Mate Choice in the Contact Zone

These finding can explain the occurrence of hybridization in the contact zone. Quails pair up with individuals that share particular plumage patterns with them. Outside the contact zone, this strategy works perfectly because they only encounter members of their own species. In the contact zone, however, they run into quails from another species. But instead of focusing in the species-specific differences, they keep using the shared plumage traits to pick their partner. And voila, hybrids!



A Gambell’s Quail © Alan D. Wilson | NaturesPicsOnline



Gee, J. M. (2003). How a hybrid zone is maintained: behavioral mechanisms of interbreeding between California and Gambel’s quail (Callipepla californica and C. gambelii). Evolution, 57(10), 2407-2415.

Hagelin, J. C. (2003). A field study of ornaments, body size, and mating behavior of the Gambel’s Quail. The Wilson Bulletin, 246-257.

Zonana, D. M., Gee, J. M., Bridge, E. S., Breed, M. D., & Doak, D. F. (2019). Assessing Behavioral Associations in a Hybrid Zone through Social Network Analysis: Complex Assortative Behaviors Structure Associations in a Hybrid Quail Population. The American Naturalist193(6), 852-865.


This paper has been added to the Galliformes page.

What’s for dinner? Rapid evolution of non-native frugivores on O’ahu

Four introduced bird species show significant changes in size and beak morphology after a few decades on the island.

On the Hawaiian island of O’ahu you can find mostly non-native bird species. The native seed-dispersing birds have been replaced by many fruit-eating birds through introductions. These birds not only facilitate the invasion of exotic plants, they may also be the only dispersers of native plants. The non-native species have become integrated into the native ecosystem (see this Science paper for more details). But have these introduced bird species changed since they took over the island? A recent study in the journal Evolution tried to answer this question by studying four species that were introduced since the 1920s.


The Japanese White-eye © Laitche | Wikimedia Commons


Museum Specimens

Jason Gleditsch and Jinelle Sperry focused on the following species: the Japanese White-eye (Zosterops japonicus), the Red-billed Leiothrix (Leiothrix lutea), the Red-wiskered Bulbul (Pycnonotus jocosus) and the Red-vented Bulbul (P. cafer). They compared museum specimens from these species’ native ranges with the living birds on O’ahu.

These comparisons revealed significant changes since the birds arrived on O’ahu. In general, the birds became shorter with more robust beaks. The changes in beak morphology are probably related to a more generalized diet, including many types of fruit.


The morphological changes in the four species (from left to right: Japanese White-eye, the Red-billed Leiothrix, Red-wiskered Bulbul and Red-vented Bulbul) since they arrived on O’ahu. Body measurements (blue) tend to decrease while beak measurements (brown) mostly increase. Significant changes are indicated with stars (*) From: Gleditsch & Sperry (2019) Evolution


Natural Selection?

These clear changes took place in just a few decades, showing that under particular circumstances evolution can proceed rapidly. It does, however, raise the question of whether these changes are due to natural selection or non-adaptive processes. The researchers used Lande’s F statistic, a measure from quantitative genetics to determine the role of genetic drift (i.e. a non-adaptive process) in evolutionary changes. The analyses suggested that the observed patterns are due to a mixture of adaptive and non-adaptive processes.


The Red-billed Leiothrix © Shrikant Rao | Wikimedia Commons


Founder Effects

However, the test does not address the role of founder effects or population bottlenecks, when a population is reduced to a small number of individuals . These events can have profound effects on the consequent evolutionary trajectory of a species. For example, the Red-billed Leiothrix went to a population bottleneck due to competition with another introduced species, the White-rumped Shama (Copsychus malabaricus). This event probably selected for certain traits that provided the starting point for further evolutionary change.

The morphological changes in these non-native frugivores have important implications for the future of this ecosystem. The authors conclude that “because all of the native frugivores have been extirpated from O’ahu, the ability of the nonnative community of frugivores to effectively disperse fruiting plants is crucial for the long‐term stability and functioning of the novel forest ecosystems on the island.”


The Red-wiskered Bulbul © | Wikimedia Commons



Gleditsch, J. M., & Sperry, J. H. (2019). Rapid morphological change of nonnative frugivores on the Hawaiian island of O’ahu. Evolution.

Genetic study of the Mallard complex reveals extensive hybridization with little recent gene flow

The genetic similarity between members of this complex is mainly due to ancestral variation and ancient gene flow.

The Mallard (Anas platyrhynchos) is the king of hybrids. This duck species has hybridized with at least 40 different species. Specifically, it regularly interbreeds with its closely related monochromatic (i.e. males and females have the same color) cousins, such the Mottled Duck (A. fulvigula), the Black Duck (A. rubripes) and the Spot-billed Duck (A. zonorhyncha). This extensive hybridization has raised conservationists warning flags. Is the Mallard driving these species to extinction by hybridization? A recent study in the journal Molecular Ecology explored the Mallard complex to answer this question.


The Mallard hybridizes with numerous other duck species. © Richard Bartz | Wikimedia Commons


The Mallard Complex

Philip Lavrestsky and his colleagues sequenced the DNA of five members from the Mallard complex that occur in North America: the Mallard (obviously), the American Black Duck, the Mexican Duck (A. diazi), the Florida Mottled Duck and the West Gulf Coast Mottled Duck (for more information about population structure in the Mottled Duck you can read this blog post). Although these species are morphologically clearly distinct, it has been proven difficult – if not impossible – to distinguish between them genetically.

The genetic similarity of these duck species could be due to two processes: extensive gene flow through hybridization or retention of ancestral genetic variation (the technical term is incomplete lineage sorting). My money would be on the first possibility, but I am biased when it comes to avian hybrids…

Mallard Complex.jpg

The monochromatic members of the Mallard complex: the Mexican Duck (topleft, © Gary L. Clark), the Mottled Duck (topright, © Dick Daniels) and the American Black Duck (bottom, © Dick Daniels)


Patterns of Gene Flow

Using a large genetic data set (with over 3000 loci), the researchers were able to assign individuals to their respective taxonomic groups. They also inferred gene flow between particular species, but the results varied depending on which genetic variants were analyzed. In general, they found the following patterns of gene flow (I added information about the variants that supported the findings, see also figure below):

  • From Mexican Ducks into West Gulf Coast Mottled Ducks (all variants)
  • From Black Ducks into Mottled Ducks (all variants)
  • From Mallard into Black Ducks (autosomal, non-outlier variants)
  • From Mallard into Mexican Ducks (Z-linked variants)
  • From West Gulf Coast Mottled Ducks (Z-linked, non-outlier variants)

However, the amount of gene flow was less than expected. The authors write that “although hybridization is known to occur between mallards and each of the monochromatic species, our results suggest that contemporary gene flow and introgression may be lower than assumed.” It seems that the genetic similarity between these species is mainly due to ancestral variation and ancient gene flow. However, it is good news for conservationists. The monochromatic species are not threatened by extinction due to hybridization with the Mallard.


Patterns of gene flow (indicated by arrows) between the different duck species for particular genetic variants. From: Lavretsky et al. (2019) Molecular Ecology


Unexpected Results

Honestly, I am a bit disappointed with the results of this study. As loyal readers might know, I just published a review on “Multispecies Hybridization in Birds.” In that paper, I constructed a hybrid network for the Anseriformes. The Mallard was connected to numerous other species and I envisioned this species as a “genetic distribution center”, picking up genetic material from one species and siphoning it to another one. Whether this idea fits with reality remains to be determined, but this study questions it by showing that recent gene flow is lower than expected. As so often, more research is needed to figure this out.


A hybridization network for the Anseriformes. The Mallard is the blue dot with many connections. Whether it functions as a genetic distribution center remains to be investigated. From: Ottenburghs (2019) Avian Research



Lavretsky, P., DaCosta, J.M., Sorenson, M.D., McCracken, K.G., & Peters, J.L. (2019). ddRAD‐seq data reveal significant genome‐wide population structure and divergent genomic regions that distinguish the mallard and close relatives in North America. Molecular ecology.


This paper has been added to the Anseriformes page.


A Brazilian Brain-teaser: How did the hybrid zone between Rufous-capped and Bahia Spinetail form?

Did it arise in situ or due to secondary contact? And did rivers play a role in the process?

There is more than one way to get a hybrid zone. Over the years, several models have been put forward to explain the formation of hybrid zones. The easiest model to envision is the origin of a secondary hybrid zone: two populations diverge in separate regions (i.e. allopatry) and establish secondary contact at some point. I have written about such hybrid zones (see for example here and here), which seem to be the most common type.

Hybrid zones can also arise in situ in response to environmental gradients. Imagine a population distributed across a landscape that changes from very wet to very dry . Over time, some individuals adapt to the wet areas whereas others learn to cope with dry conditions. The middle of the range contains a mixture of wet-adapted and dry-adapted individuals. This would be a primary hybrid zone. A possible example of this scenario is the Little Greenbul (Andropadus virens). You can read the whole story here.


The Rufous-capped Spinetail © Dario Sanches | Wikimedia Commons


Atlantic Forest Spinetails

In a recent Heredity paper, Henrique Batalha-Filho and his colleagues set out to test whether a hybrid zone between two Atlantic Forest spinetail species (Synallaxis) is of primary or secondary origin. The two species – the Rufous-capped Spinetail (S. ruficapilla) and the Bahia Spinetail (S. cinerea) – hybridize in a contact zone along the Doce and Jequitinhonha Rivers in Brazil. The location of this hybrid zone suggests that the rivers might play a role.

The researchers collected samples from more than 100 birds and sequenced a handful of molecular markers. The genetic analyses confirmed the location of the hybrid zone and indicated gene flow mainly from the Bahia Spinetail into the Rufous-capped Spinetail. Moreover, these species diverged about one million years ago.


The Bahia Spinetail © Hector Bottai | Wikimedia Commons


Forest Fragmentation

But is the hybrid zone primary or secondary? Ecological niche modelling provided some clues. This technique predicts the distribution of a species across geographic space and time using environmental data. The analysis indicated that both species were geographically isolated in the past and established secondary contact at some point. This suggestion is further supported by the genetic data, which showed signatures of population expansion.

This observation leads to another question: did the rivers play a role? The answer seems to be no. The researchers found genetic material of the two species on both sides of the river. If the river was a barrier, the species would be restricted to separate banks. Moreover, the ecological niche modelling indicated range fragmentation in the past, unrelated to the rivers. So, they conclude that “isolation and divergence due to forest fragmentation during the last ca. 2 mya is the most likely scenario explaining the evolution of S. ruficapilla and S. cinerea in the Atlantic Forest.”



Batalha-Filho, H., Maldonado-Coelho, M., & Miyaki, C.Y. (2019). Historical climate changes and hybridization shaped the evolution of Atlantic Forest spinetails (Aves: Furnariidae). Heredity, 1.


This paper has been added to the Furnariidae page.



Introducing another hybrid bird species: the Salvin’s Prion

Its intermediate beak morphology might result in a broader range of prey species.

Scientific progress does not stand still. A few months ago, I published a review paper on hybrid bird species (check the blog post here) in which I assessed the evidence for seven putative hybrid species. In addition, I proposed a scheme to classify these cases into two types: type I where reproductive isolation is a direct consequence of hybridization and type II where reproductive isolation is the by‐product of other processes, such as geographical isolation. Recently, a study in the journal Molecular Biology and Evolution added another case to the list: the Salvin’s Prion (Pachyptila salvini). Let’s have a look at the evidence and see if we are dealing with a type I or type II hybrid species.


Salvin’s Prion, another hybrid bird species? © Duncan | Wikimedia Commons



The prions (genera Pachyptila and Halobaena) are a group of small petrels. Their name comes from the Greek word for saw, referring to the serrated edges of their bills. Prions have a fringe of thin plate-like structures (so-called palate lamellae) in their beaks. In some species, such as the Broad-billed Prion (P. vittata), these lamellae are quite big and can be used for filter feeding, resulting in an exclusive diet of copepods. That is why they are sometimes called whale-birds. In other species, such as the Thin-billed Prion (P. belcheri), the lamellae are vestigial and not suitable for filter feeding. These species focus on other prey items, including small squids and fish.


A prion bill showing the lamellae. © Colin Miskelly | Museum of New Zealand


Genetic and Morphological Evidence

An international team of researchers sequenced the DNA of six prion species. When they compared these species, they discovered that Salvin’s Prion was a genetic mixture of Antarctic Prion (P. desolata) and Broad-billed Prion. Further analyses indicated that an evolutionary model in which Salvin’s Prion was a hybrid between these two species was the most likely scenario.

The genetic analyses were complemented with morphological measurements. These showed that, in terms of beak morphology, Salvin’s Prion was intermediate between both parental species. This could potentially allow it to feed on a broad range of prey species by combining the filter feeding and non-filter feeding strategies described above.


The beak morphology of Salvin’s Prion (grey) is intermediate between its parental species, the Antarctic Prion (green) and the Broad-billed Prion (orange). From: Masello et al. (2019) Molecular Biology and Evolution.


Breeding Times

There is clear genetic and morphological evidence for hybridization. But what about reproductive isolation? The authors suggest that Salvin’s Prion has an intermediate breeding schedule compared to the other two species. Antarctic Prions start laying eggs at the end of August, whereas Broad-billed Prion does this in December. Salvin’s Prion falls somewhere in the middle (early to mid-November). Because egg-laying correlates strongly with mating time, this pattern suggests that Salvin’s Prion is isolated from both parental species. However, this hypothesis remains to be tested.

This intermediate breeding schedule suggests a genetic basis of this behavior (similar to the intermediate beak morphology). If so, reproductive isolation is a direct consequence of hybridization. That would mean Salvin’s Prion is a type I hybrid species.


One of the parental species, the Antarctic Prion. © Trevor Lancaster | Wikimedia Commons



Masello, J. F., Quillfeldt, P., Sandoval-Castellanos, E., Alderman, R., Calderón, L., Cherel, Y., Cole, T.L., Cuthbert, R.J., Marin, M., Massaro, M., Navarro, J., Phillips, R.A., Ryan, P.G., Shepherd, L.D., Suazo, C.G., Weimerkirch, H. & Moodley, Y. (2019). Additive traits lead to feeding advantage and reproductive isolation, promoting homoploid hybrid speciation. Molecular Biology and Evolution. msz090.

Ottenburghs (2018) Exploring the hybrid speciation continuum in birds. Ecology and Evolution. 8(24): 13027-13034.


This paper has been added to the Procellariiformes page.

Spooky introgression in the African jungle: Bonobos hybridized with a “ghost” ape

Genetic study finds traces of ancient introgression in bonobo genomes.

Gene flow between distinct species is a common phenomenon. Scientists often observe hybrids in the wild and find evidence for genetic exchange when they look into the genomes of the interbreeding species. But what about ancient hybridization with extinct species? It seems sensible to expect traces of ancient introgression from unknown species in the genomes of extant species. In fact, more and more studies are reporting genetic material from these so-called “ghost lineages” in present-day genomes. A recent paper in the journal Nature Ecology & Evolution found traces of a “ghost” ape in bonobos. Spooky!


A bonobo contemplating the traces of ancient introgression in its genome… © Pierre Fidenci | Wikimedia Commons


S* statistic

Martin Kuhlwilm and his colleagues compared 69 genomes of chimpanzees and bonobos to explore patterns of ancient introgression. Chimpanzees have been split into several subspecies based on their distribution, namely the central, western, eastern and Nigeria-Cameroon populations. The map below gives an overview of these subspecies.

The researchers used the S* statistic to find signatures of old gene flow events (for more information about this statistic, you can check this review by Fernando Racimo and others). The analyses revealed an unexpected sharing of genetic variation between central chimpanzees and bonobos, which confirms previous findings.

Distribution of chimpanzee subspecies – western (verus, blue), Nigeria-Cameroon (ellioti, red),
central (troglodytes, green), eastern (schweinfurthii, orange) – and bonobo (pink). Adapted from: de Manuel et al. (2016) Science


Ghost Ape

Some genomic regions in the bonobo genomes could not be assigned to any of the chimpanzee populations. Detailed analyses indicated that bonobos received 0.9 to 4.2 percent from an unknown extinct population. The haplotype network below nicely illustrates this finding. The bonobos (red) and chimpanzees (yellow, green, blue and purple) form clearly defined clusters. However, one bonobo haplotype (indicated with the black arrow) is very different from the rest and probably came from a ghost lineage. Inspection of these spooky genomic regions revealed genes involved in immune response and diet, but further research is needed to validate any functional consequences of ancient hybridization.


The haplotype network shows that bonobos (red) and chimpanzees (yellow, green, blue and purple) form clearly defined clusters. However, one bonobo haplotype (indicated with the black arrow) is very different from the rest and probably came from a ghost lineage. Adapted from: Kuhlwilm et al. (2019) Nature Ecology & Evolution


Multispecies Introgression

This study shows that the evolutionary history of chimpanzees and bonobos was heavily influenced by introgressive hybridization. Not only did they interbreed among each other, bonobos even received genetic material from an extinct species. I would not be surprised if traces of ancient introgression are also present in the chimpanzee populations. It also illustrates that hybridization is not always restricted to two species, multiple species might be hybridizing. The ecological and evolutionary consequences of multispecies hybridization remain to be investigated. I just published a paper advocating a multispecies perspective on avian hybridization (see blog post here and paper here). Clearly, this perspective is not restricted to birds…


The evolutionary history of chimpanzees and bonobos has been shaped by introgressive hybridization. From: Kuhlwilm et al. (2019) Nature Ecology & Evolution



de Manuel, M. et al. (2016). Chimpanzee genomic diversity reveals ancient admixture with bonobos. Science, 354(6311), 477-481.

Kuhlwilm, M., Han, S., Sousa, V. C., Excoffier, L., & Marques-Bonet, T. (2019). Ancient admixture from an extinct ape lineage into bonobos. Nature Ecology & Evolution, 3(6), 957.

Ottenburghs, J. (2019). Multispecies hybridization in birds. Avian Research, 10(1), 20.

Racimo, F., Sankararaman, S., Nielsen, R., & Huerta-Sánchez, E. (2015). Evidence for archaic adaptive introgression in humans. Nature Reviews Genetics, 16(6), 359.

The more the merrier? My review on multispecies hybridization in birds

A summary of my recent paper in Avian Research.

Traditionally, hybridization has been studied by comparing species pairs. But what happens when multiple species are interbreeding? This question led me to write a review on multispecies hybridization in birds, which was recently published in the journal Avian Research. In this blog post, I will walk you through the review and highlight some interesting results and discussion points. But I encourage you to read the whole paper.


How Common Is It?

First of all, how common is multispecies hybridization? To quantify this phenomenon, I used records from the Serge Dumont Bird Hybrid Database for six bird orders with the highest incidence of hybridization: Anseriformes (waterfowl), Galliformes (wildfowl), Charadriiformes (waders, gulls and auks), Piciformes (woodpeckers), Apodiformes (hummingbirds and swifts) and Passeriformes (songbirds). This analysis revealed that most species hybridize with only one other species, but multispecies hybridization does occur frequently. In some bird orders, there are clear outliers (i.e. species that hybridize with many other species) such as Mallard (Anas platyrhynchos) Anseriformes, Common Pheasant (Phasianus colchicus) and European Herring Gull (Larus argentatus). These outliers have a large distribution range, providing ample opportunity to interact and potentially interbreed with several other species.


The incidence of multispecies hybridization in six bird orders.



I have been advocating the use of phylogenetic networks for some time (see for example this paper in The Auk). In the current review paper, I introduce networks as a way to visualize patterns of hybridization. In its simplest form, you just connect all the species that are known to have produced hybrid offspring. Next, you could adjust the width or color of the connections based on other parameters, such as frequency, fertility, gene flow, … These hybrid networks are an important starting point for further exploration of multispecies hybridization.


A hybrid network for the Anseriformes. Dots represent species (colored according to different genera) while connections indicate that hybrid offspring have been observed.


Multispecies Introgression

Hybridization does not necessarily result in introgression (i.e. the exchange of genetic material from one (sub)species into the gene pool of another by means of hybridization and backcrossing). Although most statistical methods have been developed to quantify introgression between two hybridizing species, some approaches can be transferred to a multispecies setting. I will not cover all these methods here, but I will highlight a few interesting studies.


Clustering Methods

Model-based clustering methods, such as STRUCTURE and ADMIXTURE , are often used to visualize the genetic ancestry of individuals. This approach can be used to pinpoint individuals whose genomes show signs of ancestry from multiple sources. For example, Thies et al. (2018) uncovered a putative hybrid zone between three subspecies of the Common Ringed Plover (Charadrius hiaticula) based on STRUCTURE analyses. However, the output from these model-based clustering methods should not be taken at face value. Other processes can produce similar ancestry plots. That is why it is important to present the results of other analyses alongside these plots.


A STRUCTURE plot for the Common Ringed Plover. Three locations (in red box) point to a hybrid zone between three subspecies. Adapted from: Thies et al. (2018) Ardea.


The D-statistic and Phylogenetic Networks

The D-statistic was originally developed to infer gene flow between humans and Neanderthals. This approach was hidden deep in the supplementary material of a Science paper, but emerged as one of the most often used statistics to infer introgression. There are several bird studies that have applied the D-statistic in a multispecies setting. For instance, I used this method in my goose work to show that there is a lot of genetic exchange between several species, as exemplified by the phylogenetic network below. Did I mention that I like networks?


A phylogenetic network of the True Geese. From: Ottenburghs et al. (2017) BMC Evolutionary Biology


Modelling Introgression

There are numerous ways of modelling the demographic history of a species pair, ranging from Approximate Bayesian Computation (ABC) to diffusion-based models (e.g., DADI). Most of these models have not been applied in a multispecies setting yet. One notable exception concerns Isolation-with-Migration models that have been used to infer gene flow between three Acrocephalus warblers and between three Icterus orioles. New methods are being developed (as I witnessed at a recent Speciation Genomics workshop), but each of these approaches comes with its own assumptions (e.g., selective neutrality or small changes in allele frequency) and one should be aware of these when inferring patterns of gene flow.


An Isolation-with-migration model for three oriole species. The circles indicate effective population sizes and the arrows show the amount of gene flow. Adapted from: Jacobsen & Omland (2012) Ecology and Evolution


Adaptive Introgression

In his book on introgressive hybridization, Edgar Anderson (1949) already stated that “raw material brought in by introgression must greatly exceed the new genes produced directly by mutation.” Indeed, adaptive introgression has been documented in several bird groups, such as Darwin’s finches and sparrows (see this blog post for more details). When multiple lineages are interbreeding, the adaptive alleles can flow in from multiple sources. This is nicely illustrated by a recent study on the diversification and domestication of the bovine genus Bos. Comparing the genomes of members of this genus – which includes taurine cattle, zebu, gayal, gaur, banteng, yak, wisent and bison – revealed complex patterns of introgression between several species. Interestingly, both gayal and bali cattle received genes from zebu cattle through introgressive hybridization. In both cases, the introgressed genes were related to a decrease in anxiety-related behaviour and could have played a role in the domestication of these animals. You can read the whole story on cow introgression here.


The complex evolutionary history of cows with multiple introgression events. From Wu et al. (2018) Nature Ecology & Evolution



To end this blog post, I will copy the conclusions of my review paper below. I hope more people will adopt this multispecies perspective on hybridization.

Hybridization is generally studied in the context of species pairs, although multiple species might be interbreeding. Hence, a multispecies perspective on hybridization is warranted. In birds, an animal group prone to hybridization, multispecies hybridization is common. However, hybridization does not necessarily result in introgression. A broad range of tools are available to infer interspecific gene flow. The majority of these tools can be transferred to a multispecies setting. Specifically, model-based approaches and phylogenetic networks are promising in the detection and characterization of multispecies introgression. At the moment, we know that introgression is relatively common across the avian Tree of Life, but we do not have an estimate of how often introgression is adaptive. In addition, when multiple species are interbreeding, the impact on the build-up of reproductive isolation, adaptation to novel environments and the architecture of genomic landscapes remains elusive. Studying hybridization between multiple species and applying new network approaches will lead to important insights into the history of life on this planet.



Ottenburghs, J. (2019) Multispecies Hybridization in Birds. Avian Research, 10:20.