Complicated Cotingas: Can we resolve any phylogeny by just adding more data?

A recent genetic study tried to resolve the phylogeny of two bird genera by generating more data.

Time for a trip down memory lane. In 2012, I started my PhD at the Wageningen University in the Netherlands. The topic of my research project: unraveling the evolutionary history of the True Geese (genera Anser and Branta). To my surprise, there was no resolved phylogeny at the time. Several researchers had tried to determine the phylogenetic relationships between the different goose species, but they all ran into polytomies and branches with low bootstrap support. How could we ever solve this conundrum? My solution was quite straightforward: just use more data! So, I sequenced the whole genomes of all goose species and released several phylogenomic tools on the terabytes data. A few years later, I proudly published a resolved phylogenetic tree for the True Geese (you can find the paper here). A recent study in the journal Molecular Phylogenetics and Evolution applied a similar approach to determine the phylogeny of two tropical bird genera.

Tijuca_condita_Gray-winged_Cotinga

Gray-winged cotinga (Tijuca condita) © Joao Quental | Flickr

 

Cotingidae

Deep within the bird family Cotingidae, you can find the genera Lipaugus (7 species) and Tijuca (2 species). Most of these species are restricted to montane habitats, where they occur along narrow elevational ranges, whereas two species reside in the lowlands. Previous genetic work on the Cotingidae family revealed that these genera are closely related. Interestingly, one Tijuca species – the black-and-gold cotinga (T. atra) – was embedded with the other genus. The reliability of this finding was uncertain, because the relationship had low statistical support. The study only used six genetic markers, so perhaps more data could provide some clarity.

Amie Settlecowski and her colleagues revisited this situation with more data. First, they repeated the previous analysis with the six markers (but including more species). This exercise confirmed the relationships uncovered before, but again with low statistical support. In addition, three nodes in the tree could not be resolved. Next, the researchers generated a large dataset of more than 1,000 ultraconserved elements (UCEs). These conserved sequences are shared among divergent animal genomes and are probably involved in controlling gene expression. Analyses of these elements resulted in a completely resolved phylogeny with high statistical support for all nodes. It turned out that the two Tujica species are indeed embedded with the genus Lipaugus. Moreover, they are not even sister species!

tree_cotingidae

A few genetic markers generated with Sanger sequencing could not resolve the phylogeny. Adding more data with ultraconserved elements revealed that the Tujica species are embedded within the genus Lipaugus. From: Settlecowski et al. (2020) Molecular Phylogenetics and Evolution

 

Problem solved?

What can we learn from my goose story and this study: If you cannot solve a phylogenetic tree, just add more data? Not necessarily. More data can help to resolve some contentious relationships, but it is not a guarantee for success. Take the attempts to reconstruct the complete avian phylogeny, for example. Erich Jarvis and his colleagues used whole genome sequences from 48 species and could not confidently determine the branching order at the base of the tree. Clearly, more data is not always the answer.

If we cannot fix a phylogenetic problem with more data, we run into a heated debate. Some scientists will argue that we will be able to resolve the issue in the future (with even more data or with better methods), while others will say that the problem cannot be fixed (the uncertainty reflects reality). In the latter case, the situation cannot be captured in a simple bifurcating tree. A network approach might then be more suitable to depict complex dynamics, such as high levels of hybridization. It is important to keep in mind that each phylogenetic solution – whether it is a tree or a network – is just a provisional hypothesis. And hypotheses can be rejected with new data…

Lipaugus vociferans

Screaming piha (Lipaugus vociferans) © Hector Bottai | Wikimedia Commons

 

References

Settlecowski, A. E., Cuervo, A. M., Tello, J. G., Harvey, M. G., Brumfield, R. T., & Derryberry, E. P. (2020). Investigating the utility of traditional and genomic multi-locus datasets to resolve relationships in Lipaugus and Tijuca (Cotingidae). Molecular Phylogenetics and Evolution, 106779.

Loss of migration leads to speciation in the Fork-Tailed Flycatcher

The establishment of sedentary populations has several consequences for genetics, morphology and behavior.

Numerous bird species migrate. Occasionally, a migrating population “decides” to stop their annual trips and become sedentary. These migratory drop-offs have been documented in several taxa and often result in morphological and physiological changes. But can they also drive speciation? Theoretically, it is certainly possible that differences in morphology and genetics start to accumulate between migratory and sedentary populations, ultimately resulting reproductive isolation and the origin of new species. A recent study in the journal Current Biology tested this idea in the Fork-Tailed Flycatcher (Tyrannus savana).

Tyrannus savana

A Fork-Tailed Flycatcher © Charles J. Sharp | Wikimedia Commons

 

Four Subspecies

The Fork-Tailed Flycatcher contains four subspecies. One subspecies (savanna) is a long-distance migrant that breeds from central Brazil to Argentina and spends the non-breeding season in northern South America. The other three subspecies (monachus, sanctaemartae, and circumdatus) are sedentary in Central and South America. This system provides the ideal circumstances to test the idea that loss of migration can result in speciation. If this idea holds true, you would expect clear differences in genetics, morphology and behavior between the migratory and sedentary subspecies. And that is exactly what Valentina Gómez-Bahamón and her colleagues found. Time for a quick overview!

Demographic analyses using genomic data indicated that the migratory and sedentary populations diverged about 1.08 million years ago. There was no sign of gene flow between these populations after the initial split, suggesting that the loss of migration happened only once. This finding is supported by a phylogenetic analyses that shows the sedentary populations nested within the migratory subspecies. The researchers conclude that “[the genomic] patterns are consistent with the hypothesis that migratory and sedentary fork-tailed flycatchers are on separate evolutionary trajectories.”

flycatcher_genetics

The genetic data indicated that the sedentary populations are nested within the migratory subspecies (Figure A), suggesting a single loss of migration. Moreover, there were no signs of gene flow between the sedentary and migratory subspecies, as shown by the clear separation in the admixture plots (Figure B). From: Gómez-Bahamón et al. (2020) Current Biology

 

More Differences

The genetic patterns are corroborated by morphological and behavioral data from the field. The researchers reported morphometric divergence between migratory and sedentary birds in traits associated with flight performance, such as the shape of the wings and tails. In line with previous studies, migratory birds had longer, more pointed wings for powered flight, while sedentary birds had shorter and more rounded wings to enhance maneuverability. The populations also exhibited differences in the timing of breeding (see figure below), contributing to reproductive isolation.

Taken together, these findings indicate that “migratory and tropical sedentary fork-tailed flycatchers are reproductively isolated due to spatial and temporal separation in breeding activities as a result of changes in migratory behavior leading to alternative strategies.”

flycatchers_breeding

The migratory (blue) and sedentary (yellow) subspecies breed at different times, contributing to their reproductive isolation. From: Gómez-Bahamón et al. (2020) Current Biology

 

Genetic Assimilation

The genetic data show that a small section of the migrating population became sedentary: both the demographic modelling and several measure of genetic diversity (e.g., heterozygosity and Tajima’s D) point to a reduction in effective population size. In a sense, this event can be seen as a founder event speciation. But how did this event happen? Migration is a complex trait that is influenced by numerous genes. A single genetic mutation cannot simply overturn migratory behavior and lead to sedentary individuals.

The researchers speculate that the change in migration strategy was due to behavioral plasticity. Some individuals switched to a sedentary lifestyle and were exposed to new selection pressures, leading to the accumulation of genetic differences between the sedentary and the migratory populations. Later on, the plasticity was lost when the new sedentary behavior was “assimilated” into the genome. An interesting hypothesis that needs further investigation.

Regardless of the mechanism behind the establishment of sedentary populations. It seems that loss of migration might be a common road to speciation. A macroevolutionary analysis of the family Tyrannidae shows that several species have lost the ability to migrate. Interestingly, speciation rates were higher for migratory and partially migratory lineages than those of sedentary lineages. Migration is thus an important factor to take into account if we want to understand the origin of bird species.

macro

A macroevolutionary analysis of the Tyrannidae showed that migration has been lost in several species (migration = blue, partial migration = green, sedentary = yellow). The dynamic nature of migratory behavior is an important factor in avian speciation. Gómez-Bahamón et al. (2020) Current Biology

 

References

Gómez-Bahamón, V., Márquez, R., Jahn, A. E., Miyaki, C. Y., Tuero, D. T., Laverde-R, O., Restrepo, S. & Cadena, C. D. (2020). Speciation associated with shifts in migratory behavior in an avian radiation. Current Biology.

Do plumage patterns support the eleven subspecies of the Velazquez’s Woodpecker?

Recent study maps the geographic phenotypic variation in a highly variable woodpecker.

Biologists try to classify the living world into neat little boxes (which is not always possible). Some get carried away and grasp any opportunity to draw lines between supposed species or subspecies. A few feathers with a slightly different color can be used to define a new subspecies. Devising a realistic and biologically relevant classification for variable species can be tricky. The Velazquez’s Woodpecker (Centurus santacruzi), for example, exhibits striking variation in plumage and size across its range, which runs from northeastern Mexico to Nicaragua. Subdividing this diversity has resulted in at least 11 recognized subspecies. But how meaningful is this taxonomic arrangement? A recent study in the Journal of Ornithology took a closer look.

Golden-fronted Woodpecker

A Velazquez’s Woodpecker in Mexico © Becky Matsubara | Wikimedia Commons

 

Morphs

Pilar Benites and her colleagues collected specimens from all 11 subspecies (for interested readers: grateloupensis, veraecrucis, dubius, polygrammus, santacruzi, huglandi, pauper, leei, insulanus, canescens, and turneffensis). Based on extensive analyses of morphometrics and plumage patterns, the researchers uncovered three basic morphs:

  1. red nape/red belly with higher barring frequency and lower barring ratio
  2. red nape/yellow belly with intermediate barring frequency and intermediate barring ratio
  3. yellow nape/yellow belly with lower barring frequency and higher barring ratio

A closer look at the distribution of the 11 subspecies shows that they do not reflect the variation in morphology and plumage patterns. A taxonomic revision might thus be warranted here.

woodpecker_distr

The geographical distribution of subspecies (left) does not match the three morphs uncovered in this study. Adapted from: Benites et al. (2020) Journal of Ornithology

 

Local Adaptation

The patterns uncovered by this study raise an additional question: What environmental factors underlie this morphological variation? The researchers reported a significant correlation between plumage patterns and precipitation seasonality. However, because precipitation co-varies with numerous other environmental variables (e.g., habitat type) it is difficult to pinpoint the exact driver of this phenotypic diversity. Despite this uncertainty, it seems plausible that the plumage patterns are caused by local adaptation.

Genetic work on the Velazquez’s Woodpecker reported weak population structure, indicating that “divergence in the phenotypic traits probably evolved faster than neutral genetic markers.” Most likely, the plumage patterns in these birds are encoded by a few genes, similar to other woodpecker species. For instance, the genetic differences between three Sphyrapicus woodpeckers are due to 19 small genomic regions, one of which contains a candidate gene for plumage variation. Will a genomic analysis of the Velazquez’s Woodpecker reveal comparable patterns?

 

References

Benites, P., Eaton, M. D., García-Trejo, E. A., & Navarro-Sigüenza, A. G. (2020). Environment influences the geographic phenotypic variation in Velazquez’s Woodpecker (Centurus santacruzi). Journal of Ornithology, 1-14.

Ready, set, speciate: The role of sex chromosomes in the divergence of Reunion grey white-eye morphs

Genomic analyses find evidence for sex-linked diversification of island populations.

Sex chromosomes can drive speciation. From a genetic point of view, the origin of new species can be seen as the slow accumulation of genetic mismatches – so-called Bateson-Dobzhansky-Muller incompatibilities – between populations. These genetic mismatches often arise on sex chromosomes for several reasons (reviewed by Darren Irwin in this excellent paper). For example, important reproductive isolation mechanisms, such as male sterility, male plumage traits, and assortative mating, have all been linked to sex chromosomes. If these chromosomes are involved in the build-up of reproductive isolation, you expect genomic regions on the sex chromosomes to be more divergent compared to other chromosomes (i.e. the autosomes). A recent study in the journal Molecular Ecology tested this idea for the Reunion grey white-eye (Zosterops borbonicus).

Zosterops borbonicus

The Reunion grey white-eye © David Monniaux | Wikimedia Commons

 

Color Morphs

I have written about the Reunion grey white-eye before (see this blog post from 2017). On the small island of Reunion, this small passerine occurs in several populations with distinct plumage patterns. In the lower parts of the island, you can find a brown-headed brown (BHB), a grey-headed brown (GHB), and a brown-naped brown form (BNB). A fourth form is restricted to the highlands (between 1,400 and 3,000 m) and comprises two very distinct color morphs. Previous genetic work uncovered narrow hybrid zones between several populations and suggested that these color morphs are separated by a few genomic regions. Unfortunately, the resolution of genetic markers (microsatellites) was too weak to pinpoint the exact genomic regions that might be involved in reproductive isolation. Recently, Yann Bourgeois and his colleagues used genomic data to fill this gap in our knowledge on the Reunion grey white-eye.

reunion_map

A map of Reunion showing the different Zosterops populations. From: Bourgeois et al. (2020) Molecular Ecology

 

Sex-linked Genes

The results were in line with an important role for sex chromosomes in the early stages of speciation on Reunion. First, the autosomal markers could only discriminate between lowland and highland populations, whereas the sex-linked markers uncovered more fine-grained population structure within the lowland morphs. Second, the researchers contrasted demographic models with autosomal and sex-linked markers. The models with sex-linked markers pointed to lower levels of gene flow between the different populations compared to models based on autosomal markers. This suggests that some genomic regions on the sex chromosomes are not being exchanged between the populations and might harbor genes involved in reproductive isolation.

To identify candidate genes for reproductive isolation, the researchers searched the genomes for divergent regions. These analyses uncovered several promising genomic locations, including a clear outlier on chromosome 4A. Wait a minute, you might say, chromosome 4A is not a sex chromosome! Well, recent studies reported the existence of special sex chromomes in the Sylvioidea superfamily, to which the Reunion grey white-eye belongs. Several genomic locations – including part of chromosome 4A – have fused with fused with the existing sex chromosomes, giving rise to neo-sex chromosomes (you can read the entire story in this blog post).

genomic_landscape

Scanning the genomes of the white-eyes for divergent regions uncovered a clear peak on chromosome 4A, which has fused with the traditional sex chromosome. From: Bourgeois et al. (2020) Molecular Ecology

 

Plumage Patterns

Additional analyses revealed two interesting candidate genes that are involved in plumage coloration: TYRP1 and WNT5A. Interestingly, WNT5A is known to regulate the expression of TYRP1. These findings “suggests that a large part of plumage colour variation between the geographical forms of the Reunion grey white-eye may be controlled by a set of a few loci of major effect. More detailed studies of hybrid zones between the different lowland forms may help to characterize the exact association of alleles that produce a given plumage color phenotype.” Other studies have already taken advantage of hybrid zones to pinpoint specific plumage genes, such crows and warblers. Hopefully, the Reunion grey white-eye can be a new addition to this list.

 

References

Bourgeois, Y. X., Bertrand, J. A., Delahaie, B., Holota, H., Thébaud, C., & Milá, B. (2020). Differential divergence in autosomes and sex chromosomes is associated with intra‐island diversification at a very small spatial scale in a songbird lineage. Molecular Ecology29(6), 1137-1153.

 

This paper has been added to the Zosteropidae page.

Crossbills show there is more to evolution than natural selection

What explains the fit between beak morphology and pine seeds in a Spanish population?

A common misunderstanding about evolutionary theory is equating evolution to natural selection. However, evolution is much more than natural selection. Evolution refers to the change of populations over time (often phrased in terms of allele frequencies), while natural selection is just one mechanism underlying these changes. The idea behind natural selection is simple, but very powerful. It is the logical conclusion of these three premises:

  1. Individuals vary in certain traits
  2. These traits are heritable (they are passed on from parent to offspring)
  3. Variation in these traits leads to differences in survival and reproduction

And that’s it. A quick hypothetical example illustrates the workings of natural selection. Imagine a population of birds with different beak sizes. These birds feed on a tree species that produces seeds hidden inside small cones. Birds with a certain beak size can open these cones and access the seeds inside. These birds will be most successful in surviving (they have plenty of food) and producing offspring (they can feed their young). Because beak morphology is heritable, the young birds inherit beak size from their parents. Each generation, the variation in beak size will be determined by the surviving birds and their offspring from the previous generation. Over time, the average beak size of the population will converge upon the optimal size for cracking the cones.

Loxia curvirostra

A Common Crossbill in Austria © Frank Vassen | Wikimedia Commons

 

Capture-recapture

A recent study in the Journal of Avian Biology studied this scenario in common crossbills (Loxia curvirostra) from Spain. These birds show variation in beak size and forage on mountain pines (Pinus uncinata). Using a capture–recapture dataset spanning 27 years, the researchers investigated whether natural selection is driving beak morphology to an optimum size to feed on mountain pines. Between 1988 and 2014, birds were ringed and recaptured. How did beak morphology change over this period?

Statistical models indicated that the population optimum beak width is 11.43 mm. Apparent survival decreased when beak width deviated from this value. I write “apparent survival” because the capture-recapture data only suggest that a bird did not survive. When a bird is not caught again, it could be dead or it could have moved to another location.

jav12638-fig-0002-m

For different age classes (juveniles, yearling and adults), apparent survival shows a peak around a beak width of ca. 11 mm. From: Gómez‐Blanco et al. (2019) Journal of Avian Biology

 

Selecting Environments

This results suggests that natural selection is keeping the population stable around a beak width of 11.43 mm. As I explained above, individual birds with smaller or bigger beaks don’t survive and are thus removed from the population. The reality, however, is not that straightforward. An alternative explanation is that maladapted birds do survive but fly to other locations where they have better access to food. Instead of the environment selection for particular individuals (i.e. natural selection), the individuals are selecting a certain environment.

This phenomenon could partly explain the result in this study. The authors write that “our estimate would be a rather unusually strong measure of stabilizing natural selection. Said otherwise, an unusual number of selective deaths would have to occur because of a phenotypic trait. Therefore, it appears probable that selective dispersal of locally maladapted individuals out of the study area has also contributed in order to produce this high value.” More widespread sampling of neighboring populations is needed to confirm this idea.

jav12638-fig-0003-m

The estimated selection gradients from the present study (blue) versus a literature review (grey) indicates from strong selection on crossbills. Perhaps too strong? Gómez‐Blanco et al. (2019) Journal of Avian Biology

 

Alternative Explanations

This study illustrates that a match between a certain trait and the environment is not always the outcome of only natural selection. There are several alternative explanations that need to tested, such as individuals selecting certain environments. Other possibilities are phenotypic plasticity and adjustment of the environment. Phenotypic plasticity concerns the situation where a trait can vary in different environments (think of a tree growing higher in fertile soil compared to bare soil). Adjustment of the environment is self-explanatory: a population changes the environment to fit its needs, such as beavers building a dam to flood an area.

These alternative explanations highlight that we should be careful in attributing adaptations solely to natural selection and telling unfounded just-so stories (such as my hypothetical example above). Explore all possibilities before your draw conclusions.

 

References

Gómez‐Blanco, D., Santoro, S., Borrás, A., Cabrera, J., Senar, J. C., & Edelaar, P. (2019). Beak morphology predicts apparent survival of crossbills: due to selective survival or selective dispersal?. Journal of Avian Biology50(12).

Solving the seabird paradox: How does genetic differentiation arise in highly mobile species?

An extensive review paper attempts to answer this intriguing question.

Seabirds travel thousands of kilometres to find foraging and breeding areas. Gliding over the largely homogeneous oceans, there seem to be no obvious barriers for these birds. You would expect that this high vagility is reflected in the genetics of the populations, namely no genetic structure. Interestingly, many studies report clear genetic differentiation between different seabird colonies. For example, a recent genetic study of the white-chinned petrel (Procellaria aequinoctialis), which breeds on New Zealand and islands in the Indian and Atlantic Ocean, uncovered clear population boundaries using genomic data. What factors could be responsible for the origin of genetic differentiation in highly mobile species, such as seabirds? A paper in the journal Biological Reviews tried to solve this conundrum.

Procellaria_aequinoctialis

A white-chinned petrel © JJ Harrison | Wikimedia Commons

 

Literature Review

Anicee Lombal and her colleagues dove into the scientific literature and collected as many studies on the population genetics of seabirds as they could find. For each study, they extracted the genetic data and noted down biological factors that could explain genetic differentiation between colonies. Let’s have a look at the most important factors on this list.

Seabirds are often philopatric, consistently returning to the same breeding area. This behavior might lead to isolation between colonies and consequently genetic differences. Spatial segregation can also occur outside of the breeding season. Birds from distinct colonies might use different foraging areas and are thus less likely to mix at sea. Eventually, they will return to different colonies. There can also be morphological or phenological differences between colonies that affect mate choice and culminate in genetic differentiation.

imperial shag

An imperial shag (Phalacrocorax atriceps) from the Falkland Islands © Samual Blanc | Wikimedia Commons

 

Summary Statistics

The biological factors above – philopatry, spatial segregation and morphological or phenological differences –  make intuitive sense. However, the analyses found no consistent support these factors driving genetic differentiation in seabirds. Indeed, one section in the paper is entitled “Biotic factors do not predict genetic differentiation among seabird populations.” So, what factors are responsible for the observed genetic differences?

Perhaps the genetic patterns we quantify now are the outcome of past events? To test this idea, the researchers performed additional genetic analyses on the collected data. They calculated several population genetic statistics to quantify past changes in population size, including Tajima’s D, Fu and Li’s F* and Fu’s Fs statistic. The combination of these statistics can be used to deduce demographic events. For example, when Fs is significant and D and F* are not, there was probably a range expansion.

rockhopper

Northern rockhopper penguin (Eudyptes moseleyi) on Inaccessible island © Brian Gratwicke | Flickr

 

Ice Ages

The genetic analyses revealed the strong genetic legacies of past demographic changes. However, the underlying events were slightly different for particular geographic regions. Northern temperate species were clearly influenced by the glacial cycles of the Pleistocene when populations retreated to different refugia, such as the southern edge of the Bering Land Bridge, the Newfoundland Bank and the Spitsbergen Bank, where they accumulated genetic differences. Species on the southern hemisphere, on the other hand, expanded their ranges after the Last Glacial Maximum (ca. 20,000 year ago) and colonized areas that became free of ice. This expansion resulted in geographic isolation and consequently genetic differentiation.

In summary, the seabird paradox can be partly resolved by the genetic legacy of past demographic changes. Additional biological factors might strengthen these patterns over time, but they are mostly species-specific.

 

References

Lombal, A. J., O’dwyer, J. E., Friesen, V., Woehler, E. J., & Burridge, C. P. (2020). Identifying mechanisms of genetic differentiation among populations in vagile species: historical factors dominate genetic differentiation in seabirds. Biological Reviews95(3), 625-651.

Splitting scimitar babblers: Genetics and morphology point to two distinct species

The study also uncovered some evidence for hybridization.

Morphology matters. Most species descriptions are based on careful morphological analyses. But morphology cannot always be trusted when drawing taxonomic lines between species. Take the redpoll finch complex, for example. This group of songbirds currently contains three species: common redpoll (Acanthis flammea), hoary redpoll (Acanthis hornemanni) and lesser redpoll (Acanthis cabaret). Despite obvious morphological differences – as any birdwatcher can tell you – these species have largely undifferentiated genomes. From a genetic point of view, these three species could thus be lumped together. Similar results have been reported for bean geese, warblers and crows. Alternatively, species might be morphologically indistinguishable, but drastically different on a genetic level. These cryptic species can thus only be identified with genetic techniques. The yellow-browed warbler (Phylloscopus inornatus), for instance, turned out to be composed of three cryptic species.

These examples clearly indicate that there is more to life than morphology. It is advisable to test classifications based on morphological data with genetic analyses. A recent study in the journal Zoologica Scripta performed this exercise for two East Asian scimitar babblers.

Pomatorhinus gravivox

A black-streaked scimitar babbler (Pomatorhinus gravivox) © Carrie Ma | Oriental Bird Images

 

Morphology and Genetics

In 2006, two races within the rusty-cheeked scimitar babbler (Pomatorhinus erythrogenys) were elevated to species level. From that moment onward, you could check the black-streaked scimitar babbler (P. gravivox) and the grey-sided scimitar babbler (P. swinhoei) on your Asian birding list. This taxonomic decision was based on meticulous morphological analyses. The most conspicuous features were the coloration of the ventral and dorsal feathers.  The black-streaked scimitar babbler has olive-gray dorsal feathers and orange-tawny ventral feathers, while gray-sided scimitar babbler can be recognized by its foxy-rufous and grayish coloration. But are the distinct plumage patterns also reflected in the genetic make-up of these species?

Chuanyin Dai, Feng Dong and Xiaojun Yang took a closer look at one mitochondrial and four nuclear loci to see whether morphology and genetics were congruent. Analyses of the nuclear markers pointed to two genetic clusters that corresponded to the morphologically described species. These findings were recapitulated by the haplotype networks which showed a clear separation between the taxa (see figure below). The researchers concluded that “the concordance of divergence between morphological, mitochondrial locus and nuclear DNA analyses should be viewed as the most convincing evidence supporting P. gravivox and P. swinhoei as distinct species.”

zsc12411-fig-0003-m

Haplotype networks for each nuclear locus. Green and red circles denote Pomatorhinus gravivox and P. swinhoei , respectively. From: Dai et al. (2020) Zoologica Scripta

 

Acoustic Isolation?

The genetic and morphological data were also confirmed by differences in vocalizations. The researchers did not test this feature explicitly, but describe an interesting incident during their fieldwork.

Besides, it is worth mentioning that in one case a pair of P. swinhoei showed no reaction to the playback of P. gravivox vocalizations during the period of sample collection in the field. When we collected samples in a location far from the contact zone (Jixi county), where the collected birds were P. swinhoei, we had mistakenly played the songs and calls of P. gravivox to attract a pair of targeted birds observed in a shrub. We noted that the birds nearby neglected this disturbance and did not exhibit any reaction at all. Approximately 15 min later, we checked the player and recognized this mistake and then played the songs and calls of P. swinhoei. The two birds came out the shrub immediately, and the male bird was caught by the mist net!

This suggests that there is some acoustic isolation between the two species, but more research is needed to confirm this observation.

 

A Mitochondrial Mismatch

All these lines of evidence point to two distinct species. The ultimate test would be to check whether these birds can produce viable offspring. If they are unable to hybridize, there will be no debate on this separate species status. However, it seems that reproductive isolation between the black-streaked and the grey-sided scimitar babbler is not complete yet. Analyses of the mitochondrial gene revealed one grey-sided scimitar babbler that falls right in the middle of the black-streaked scimitar babbler group. Most likely, this individual received this mitochondrial variant through hybridization. Whether we can find hybrids in the wild remains to be seen…

zsc12411-fig-0002-m

Analyses of the mitochondrial gene showed one individual P. swinhoei that clusters with all the P. gravivox specimens. From: Dai et al. (2020) Zoologica Scripta

 

References

Dai, C., Dong, F., & Yang, X. (2020). Morphotypes or distinct species? A multilocus assessment of two East Asian scimitar babblers (Aves, Timaliidae). Zoologica Scripta49(3), 265-279.

This paper has been added to the Timaliidae page.

Do rivers promote avian speciation in the subtropics?

A recent genetic study tested the riverine barrier hypothesis in the Paraná–Paraguay River system.

How would you explain allopatric speciation to a layperson? Most biologists would roughly follow the definition you can find on Wikipedia: “A mode of speciation that occurs when biological populations become geographically isolated from each other to an extent that prevents or interferes with gene flow.” And perhaps they would add an example of a geographical barrier, such as a river. Studies on the Amazon river and its tributaries have indeed found support for this so-called riverine barrier hypothesis. But what about rivers in non-tropical regions? Subtropical bird species tend to show higher dispersal rates compared to their tropical cousins (see for example here). Hence, a river might not be such a formidable barrier for some subtropical species. A recent study in the journal Molecular Ecology put this idea to the test.

Cyclarhis gujanensis

A rufous-browed peppershrike in Brazil © Dario Sanches | Wikimedia Commons

 

Seven Species

Cecilia Kopuchian and her colleagues studied the population genetics of seven pairs of subspecies that can be found around the subtropical Paraná–Paraguay River system. It concerns the following bird species:

  • Green‐barred woodpecker (Colaptes melanochloros)
  • Narrow‐billed woodcreeper (Lepidocolaptes angustirostris)
  • Variable antshrike (Thamnophilus caerulescens)
  • Rufous‐browed peppershrike (Cyclarhis gujanensis)
  • Sayaca tanager (Thraupis sayaca)
  • Red‐crested finch (Coryphospingus cucullatus)
  • Ultramarine grosbeak (Cyanocompsa brissonii)

If the riverine hypothesis holds true in the subtropics, we would expect to find a clear genetic break between populations east and west of the rivers. Moreover, the timing of divergence between these pairs of populations should be similar across the seven bird species.

Coryphospingus cucullatus

A red‐crested finch (also known as  red pileated finch) © Dario Sanches | Wikimedia Commons

 

Discordant Patterns

The genetic analyses revealed some surprising patterns. Only one species – the variable antshrike – followed the expected distribution with a clear genetic intergradation zone across the river (see panel a in figure below). In four other species, the genetic break between eastern and western populations was located between 150 and 300 kilometres east of the river (panels b-e), while in one species this break could be found on the western side of the rivers (panel f). Finally, the seventh species – the red‐crested finch – showed no relationship with the rivers whatsoever.

In addition to these discordant geographical patterns, the timing of divergence was widely different for the seven species. The authors report that “substantial variation in the number of generations since the split between individuals belonging to different genetic populations, ranging from 0.59 million generations in Coryphospingus cucullatus [red‐crested finch] to 2.25 million generations in Cyclarhis gujanensis [rufous‐browed peppershrike].” It is not looking good for the riverine barrier hypothesis here…

mec15384-fig-0002-m

The seven bird species show distinct genetic patterns along the araná–Paraguay River system. From: Kopuchian et al. (2020) Molecular Ecology

 

Geology and Ecotones

What can explain these discordant patterns? The researchers offer several possibilities. First, the geological history of the Paraná–Paraguay River system might provide a clue. The Paraná river has not always been in its current location. Geological studies revealed that this river has changed its course several times during the last few million years. Perhaps the genetic breaks uncovered in this study coincide with previous locations of the Paraná river.

Second, the location of the genetic breaks might be due to local ecological conditions, specifically the transition between different ecoregions (i.e. ecotones). Indeed, other studies have indicated that ecological gradients can drive genetic differentiation (interested readers can check these blog posts on saltmarsh sparrows or little greenbuls). In this case, it concerns the transition between the Chaco and Espinal ecoregions. Denser sampling of these regions is needed to confirm this possibility.

Taking into account the geological history and ecology of the area might still indicate that the genetic patterns are partly driven by rivers. The riverine barrier hypothesis is not dead yet in the subtropics.

Colaptes melanochloros

A green‐barred woodpecker © Claudney Neves | Wikimedia Commons

 

References

Kopuchian, C., Campagna, L., Lijtmaer, D. A., Cabanne, G. S., García, N. C., Lavinia, P. D., … & Di Giacomo, A. S. (2020). A test of the riverine barrier hypothesis in the largest subtropical river basin in the Neotropics. Molecular Ecology.

 

Captive-bred ducks are genetically swamping wild Mallard populations in eastern North America

Feral and wild mallards might be collapsing into a hybrid swarm.

More than a year ago, I wrote a blog post about hybridization between mallards (Anas platyrhynchos) and American Black Ducks (A. rubripes). A study in the journal Ecology and Evolution found low levels of gene flow between these species, but also uncovered some interesting patterns within the mallards populations. The researchers could discriminate between two main mallard populations, which they referred to as western and non-western mallards. Interestingly, the non-western birds, which occur mainly east of the Mississippi River, carry the mitochondrial haplotype A. This genetic variant originates from the Old World and could have reached North America in a number of ways. I ended the blog post with one possibility.

The most likely source for this haplotype is feral ducks, which have been (and are still being) released in North America. The game-farm birds are originally from Eurasia and thus carry haplotype A. Based on these patterns, the researchers propose the following scenario: hybrids tend to backcross with mallards and these backcrosses consequently interbreed with feral ducks. But samples from game-farm birds are needed to confirm this hypothesis. There will definitely be more studies on this system. So keep an eye on the Avian Hybrids Project.

Recently, my prediction came true. Philip Lavretsky and his colleagues sampled feral mallards and compared their genetic make-up with the wild populations. Their findings appeared in the journal Molecular Ecology.

feral_mallard

A feral mallard in Canada. © Ryan Hodnett | Wikimedia Commons

 

Hybrid Swarm

I will not keep you in suspense. The new study confirmed the suspicion that wild mallards acquired haplotype A from feral birds. A haplotype network – which shows the relationships between different mitochondrial variants – clearly shows several wild mallards cluster with the game-farm mallards. More detailed analyses, based on genomic data, corroborated these patterns.

The researchers state that this is “compelling evidence that the presence of the predominant OW [Old World] A mtDNA haplotypes in North America is instead largely the result of a century of game-farm stocking practices.” Indeed, game managers have yearly released more than 500,000 captive-bred ducks on the eastern coast since the 1920s. The numbers have decreased in recent years, but there are still about 210,000 feral mallards being released annually. Moreover, the conversion of boreal forests into open, prairie-like habitat, has allowed mallards to naturally expand eastward since the 1950s. Together, these processes have brought wild and feral mallards into contact, resulting in high levels of hybridization and potentially the formation of a hybrid swarm.

haplotype_network

The haplotype network shows that many wild mallards contain haplotype A and thus cluster with feral mallards. From: Lavretsky et al. (2020) Molecular Ecology

 

Increased genetic divergence

The hybrid dynamics between wild and feral mallards have important implications for understanding the genetic differences between mallards and black ducks. Although there is frequent hybridization between mallards and black ducks, this does not seem to result in high levels of gene flow. Which reproductive isolation mechanisms are preventing gene flow between these species remains to be determined, but it does lead to increased genetic divergence between mallards and black ducks. This genetic differentiation might be accelerated by hybridization between wild and feral mallards.

In a recent review paper on multispecies hybridization in birds, I wrote that “introgression between certain species might contribute to increased divergence and reproductive isolation between those species and other related species.” The three duck populations in the current study might be a nice example of this idea. Gene flow from feral into wild mallards changes the genetic make-up of the wild populations, resulting in increased genetic differentiation between wild mallards and black ducks.

mec15343-fig-0007-m

A summary of the hybridization dynamics between black ducks and mallards. From: Lavretsky et al. (2020) Molecular Ecology

 

References

Lavretsky, P., McInerney, N. R., Mohl, J. E., Brown, J. I., James, H. F., McCracken, K. G., & Fleischer, R. C. (2020). Assessing changes in genomic divergence following a century of human‐mediated secondary contact among wild and captive‐bred ducks. Molecular Ecology29(3), 578-595.

This paper has been added to the Anseriformes page.

A suite of subfamilies: How to classify the estrildid finches?

A recent genetic study proposes six subfamilies.

Ornithologists are often arguing about the species status of particular birds: are they distinct species or just subspecies?! The discussions about other taxonomic levels, such as genera or subfamilies, are often less heated. There is no clear consensus among taxonomists on how to determine whether a group of species should be classified in the same genus or subfamily. However, these higher-level classifications can be important to understand the evolutionary history of a particular lineage and should thus reflect some underlying characteristics in terms of genetic divergence or morphology. A recent study in the journal Molecular Phylogenetics and Evolution applied this reasoning to the bird family Estrildidae: the estrildid finches.

Red_browed_finch02

A red-browed finch (Neochmia temporalis) © Fir0002/Flagstaffotos | Wikimedia Commons

 

Subfamilies

The taxonomic limits within the Estrildidae are still controversial. Several studies have resolved certain sections within this family, but no complete species-level phylogeny has been published yet. The most comprehensive classification of the estrildid finches can be found in the Handbook of Birds of the World, but is based on unpublished data. Currently, the Estrildidae family is divided into three subfamilies: Estrildinae (mainly African waxbills), Lonchurinae (grassfinches, mannikins and munias), and Erythrurinae (parrotfinches).

That is why Urban Olsson and Per Alström decided to sample as many species as possible and reconstruct their evolutionary history. Genetic analyses uncovered six distinct groups within this family. The authors propose to consider these six groups as subfamilies, because “the relatively similar age of the six clades is a strong argument for treating them at the same taxonomic level.” Indeed, the molecular dating analyses revealed that these groups originated about 10 million years ago. The names for these subfamilies would be Amandavinae, Erythrurinae, Estrildinae, Lagonostictinae, Lonchurinae and Poephilinae.

tree_finches

The resulting evolutionary tree of the estrildid finches shows six distinct clades that could be considered subfamilies. From: Olsson & Alström (2020) Molecular Phylogenetics and Evolution

 

One or Two Genera?

There are some interesting patterns within the newly recognized subfamilies. Take the genus Coccopygia, for example. This small group of waxbills is sometimes classified within the genus Estrilda. This study, however, shows that both genera are actually very different on a genetic level. Moreover, grouping them together would render the genus Estrilda polyphyletic (while taxonomists aim for monophyletic groups). So, better to keep them separate.

waxbill

A swee waxbill (Coccopygia melanotis) © Alandmanson | Wikimedia Commons

 

Morphology vs. Genes

In the subfamily Lagonostictinae, we find four Pytilia species. These have traditionally been divided into two morphologically similar pairs: red-billed pytilia (P. lineata) with red-winged pytilia (P. phoenicoptera) and orange-winged pytilia (P. afra) with red-faced pytilia (P. hypogrammica). Surprisingly , this arrangement is not reflected in the genetic data. It turns out that the morphologically different red-winged pytilia and red-faced pytilia are closely related. Possibly, there has been (or still is) gene flow among these two species that live side by side in western Africa.

Rotmaskenastrild_(Pytilia_hypogrammica)

A pair of red-faced pytilias (P. hypogrammica) © Edward Cwik | Wikimedia Commons

 

Hybrids

There might thus be hybrids between Pytilia species to be discovered. A genus where hybridization is definitely quite common is Lonchura. A recent genomic study reported high levels of gene flow between certain species, indicating that “they represented a very recent radiation that had not yet developed reproductive isolating barriers.” This conclusion was corroborated by the current study that reported very short branch lengths for these species in the phylogeny.

We might have resolved the main relationships within the Estrildidae family, but there remains much to be unraveled on a lower taxonomic level.

Tricoloured munia (Lonchura malacca)

A tricoloured munia (Lonchura malacca) © Nrik Kiran | Wikimedia Commons

 

References

Olsson, U., & Alström, P. (2020). A comprehensive phylogeny and taxonomic evaluation of the waxbills (Aves: Estrildidae). Molecular Phylogenetics and Evolution146, 106757.