Gray or white cygnets? Juvenile plumage of Mute Swans matters more than you might think

Plumage morph influences survival probability.

Every year, a pair of Mute Swans (Cygnus olor) breeds on the campus of Wageningen University (the Netherlands). This year, they produced eight little swans (or cygnets). When strolling from my office to one of the education buildings, I regularly run into the local pair of campus-swans and their young. I noticed that two cygnets have white plumage whereas the other six are gray. Diving into the scientific literature, I found some interesting information about the genetic basis of this trait and the impact on individual survival. These juvenile plumage morphs matter more than I imagined.

The campus-swans foraging in a ditch. You can clearly see the difference between the white and gray cygnets. © Jente Ottenburghs

A Single Sex-linked Gene

The genetic basis of the gray/white plumage morph has already been unraveled in 1968. Three ornithologists – Munro, Smith and Kupa – observed the distribution of these two morphs in 53 nests. The resulting patterns suggest that this trait is determined by a single gene that follows the Mendelian rules (see the table below). As you might remember from high school, one version of a gene (or an allele) can be dominant whereas the other version is recessive. In the case of Mute Swans, the gray allele is dominant and the white one is recessive.

Moreover, the researchers noticed that most white cygnets were female. This observation indicates that the gene is probably located on one of the sex-chromosomes. In birds, sex is determined by a ZW-system. Males have two Z-chromosomes whereas females have one Z-chromosome and one W-chromosome. Because the plumage-gene resides on Z-chromosome, females with a recessive allele will always be white. In contrast to males, females don’t have a second Z-chromosome that could carry a dominant allele.

In summary, the gray/white plumage morph is determined by a single gene on the Z-chromosome with the gray allele being dominant over the white allele.

The distribution of plumage phenotypes points to one gene with a dominant and a recessive allele. From: Munro et al. (1968).

Aggressive Experiments

Now we know the genetic basis of this trait. But does it really matter whether a cygnet is gray or white? Apparently, it does. In a study in the journal Behaviour, Douglas Norman wrote that “It appears that white cygnets are subjected to far more parental aggression than their brown coloured siblings [gray cygnets molt into brown subadult plumage].” This statement was largely based on personal observations by other ornithologists. So, Norman put this idea to the test with an experiment.

He presented brown or white swan models to adult Mute Swans in their territories. The white models were attacked more vigorously than the brown ones, supporting the idea that white cygnets experience more parental aggression. However, Norman noted that “the brown model might be less visible to the swans due to the lack of contrast between it and the marsh grass (predominately Spartina alterniflora) background.”

Therefore, he devised a second experiment in which both models were presented to the Mute Swans at the same time. Now, the adults consistently attacked the white model, even when they had to pass the brown model to reach it. Norman concluded that “this unequivocally demonstrates that the “whiteness” has the effect of eliciting aggression and attacks from these swans.”

In the second experiment – with brown and white models presented simultaneously – only the white models were attacked by the Mute Swans. From: Norman (1977).

Survival Rates

Now we have experimental evidence that parents are more aggressive towards white cygnets. But does this also influence the survival probability of these young birds? To answer this question, Michael Conover and his colleagues followed the fate of Mute Swans on the Chesapeake Bay in 1972–1980 and on Long Island Sound in 1982–1989. Their results – published in The American Naturalist – revealed that gray cygnets had higher survival rates from hatching to fledging than white ones. Moreover, when the white cygnets began to molt into their adult-like white plumage, their parents often attacked and drove them off. It seems that the parents regarded their white offspring as intruding adults. The gray cygnets – which molt into brown subadult plumage – from the same brood were allowed to remain on their territories for several more months. The gray plumage morph clearly has several benefits, but also one important downside.

Benefits include being allowed to remain longer on their parents’ territory and enjoying a greater tolerance from older conspecifics during their first 2 yr of life. The liability is that they must wait longer before they can reproduce.

However, breeding at an early age is not always an advantage. Less experienced parents might have a higher chance of brood failure. But this aspect remains to be studied in more detail. Perhaps we can follow the lives of the eight cygnets that are currently exploring the campus?

White cygnets (AP) show lower survival rates compared to gray cygnets (SAP). From: Conover et al. (2000).

References

Conover, M. R., Reese, J. G., & Brown, A. D. (2000). Costs and benefits of subadult plumage in mute swans: testing hypotheses for the evolution of delayed plumage maturation. The American Naturalist, 156(2), 193-200.

Munro, R. E., Smith, L. T., & Kupa, J. J. (1968). The genetic basis of color differences observed in the Mute Swan (Cygnus olor). The Auk, 85(3), 504-505.

Norman, D. O. (1977). A role for plumage color in Mute Swan (Cygnus olor) parent-offspring interactions. Behaviour, 62(3-4), 314-320.

Featured image: The campus-swans with their cygnets © Bingxin Wang

How highland hummingbirds adapt to life in the Andes

Similar signatures of natural selection despite demographic differences.

From a population genetic point of view, the Violet-throated Starfrontlet (Coeligena violifer) and the Sparkling Violetear (Colibri coruscans) could not be more different. The Violet-throated Starfrontlet comprises three distinct genetic clusters that are connected by occasional gene flow, whereas the Sparkling Violetear does not show any population subdivision (i.e. a panmictic population, similar to the Red-backed Shrike in this blog post). Despite these differences, however, researchers found similar signatures of natural selection across the genomes of these highland hummingbirds.

Local Adaptation

In a recent Journal of Heredity study, Marisa Lim and her colleagues analyzed the genomes of 62 Violet-throated Starfrontlets and 101 Sparkling Violetear across an elevation gradient in the Peruvian Andes. In both species, numerous genetic variants were associated with particular elevational regions. Close inspection of these genetic variants revealed candidate genes involved in dealing with low oxygen conditions and energy metabolism, pointing to local adaptation.

An overview of the different candidate genes in both hummingbird species, classified according to function. From: Lim et al. (2021).

A Striking Contrast

As explained above, these hummingbird species show different demographic patterns. Hence, the underlying dynamics of natural selection are probably quite different. The researchers nicely describe this contrast in the discussion of their paper. With regard to the Violet-throated Starfrontlet, they write the following.

Given their genetic structure and reduced levels of gene flow, clinal variation in Coe. violifer populations could have arisen from the addition of new genetic material via small amounts of gene flow between populations.

The situation in the Sparkling Violetear, however, is very different.

The widespread distribution and lack of population subdivision in Col. coruscans suggests the observed locus-specific clinal variation is maintained by selection strong enough to supersede the homogenizing effect of gene flow.

These hummingbirds show that natural selection can produce similar patterns in different demographic settings. However, it remains important to consider other evolutionary forces – such as gene flow and genetic drift – to understand the genetic basis of local adaptation.

References

Lim, M. C., Bi, K., Witt, C. C., Graham, C. H., & Dávalos, L. M. (2021). Pervasive genomic signatures of local adaptation to altitude across highland specialist Andean hummingbird populations. Journal of Heredity, 112(3), 229-240.

Featured image: Sparkling Violetear (Colibri coruscans) © Félix Uribe | Wikimedia Commons

Is the Red-backed Shrike a panmictic population?

Genomic analyses fail to find population genetic structure.

“Population genomics uses technology to increase the number of genetic markers by orders of magnitude, thereby offering the potential for fine-scale resolution of population structure and determination of population boundaries and population membership.” This statement comes from a book chapter that I wrote with several colleagues a few years ago. At first sight, we seem to suggest that genomic data will mostly be able to detect subtle genetic population structure. Just add more data and you are bound to find some differences. This is, however, not always the case. In the book chapter, we mentioned some genomic studies that failed to reveal population structure, even for species with broad geographic distributions, such as the European Turtle Dove (Streptopelia turtur) or the Mountain Chickadee (Poecile gambeli).

This lack of genetic population structure is known as panmixia. And a recent study in the journal Diversity adds another example to this list of panmictic bird species: the Red-backed Shrike (Lanius collurio).

mtDNA and Genomics

In 2019, Liviu Pârâu and his colleagues analyzed the mitochondrial DNA (mtDNA) of 132 breeding Red-backed Shrikes across their entire breeding range. They found two distinct groups with no clear geographical pattern, pointing to a panmictic population. But perhaps the mtDNA does not tell the complete story? That is why the researchers recently revisited this species with genomic data. They sequenced the whole genomes of 88 Red-backed Shrikes from 11 countries. The genetic analyses showed … the same patterns as the mtDNA. No sign of genetic population structure. The Red-backed Shrike does seem to be a panmictic bird species.

The Principal Component Analyses (PCA) does not reveal any population structure in the Red-backed Shrike. From: Pârâu et al. (2022) Diversity.

An Ice Age Legacy

But what evolutionary processes resulted in this panmictic population? The researchers argue that this panmixia is a “genetic legacy of the widespread and continuous distribution of the species, high locomotion capacities, and, most importantly, the numerous ice ages from the past few million years, which forced various populations to retract to refugia and expand their ranges several times, and to interbreed both in the glacial refugia and during warm periods in Eurasia.”

However, these ice ages might have left some subtle genetic signatures in the genomes of these birds. Particular genomic regions might reveal in which refugia the ancestors of present-day birds survived. Finding these genomic regions – if they even exist – will require more detailed genomic analyses (see for example this study on bean geese). The genetic population structure in the Red-backed Shrike might be hidden deep within its genome.

References

Pârâu, L. G., Wang, E., & Wink, M. (2022). Red-Backed Shrike Lanius collurio Whole-Genome Sequencing Reveals Population Genetic Admixture. Diversity, 14(3), 216.

Featured image: Red-Backed Shrike (Lanius collurio) © Antonios Tsaknakis | Wikimedia Commons

Complicated patterns of gene flow in the Green-winged Teal complex

What processes underlie mito-nuclear discordance in these ducks?

Different genes tell different stories. Throughout my blog posts on the Avian Hybrids website, I have repeated this statement numerous times (see for example here). A recent study on the Green-winged Teal (Anas crecca) complex provides another example of this mantra. The taxonomy of this species complex is still a matter of debate, so I will follow the authors of the paper and stick with three subspecies: the Eurasian Teal (A. c. crecca), the Aleutian Teal (A. c. nimia), and the American Teal (Anas c. carolinensis). The fourth relevant member of this species complex is the Yellow-billed Teal (Anas flavirostris) from South America.

Analyses of mitochondrial DNA reveal two groups in the species complex: the Eurasian Teal and the Aleutian Teal in one group and the American teal and the Yellow-billed Teal in the other group. But when you look at the nuclear DNA a different arrangement emerges: the three subspecies cluster together, separate from the Yellow-billed Teal. What is going on here?

Different genes tell different stories. The mtDNA clusters the American Teal (yellow) with the Yellow-billed Teal (red), whereas the nuclear DNA groups the three subspecies together. From: Spaulding et al. (2023).

Gene Flow

Previous studies already reported these conflicting phylogenetic patterns. In the recent study, Fern Spaulding and her colleagues confirmed the discordance between mitochondrial and nuclear DNA with ultraconserved markers (UCEs). Moreover, they found signatures of gene flow in several pairwise comparisons (see figure below). All three subspecies have exchanged genes at some point in their evolutionary history. And there has even been gene flow between the American Teal and the Yellow-billed Teal, despite breeding on different continents. These patterns of genetic exchange can help us to understand the conflict between mitochondrial and nuclear DNA.

Demographic models with different taxa showed signs of gene flow. The evolutionary scenarios are slightly different but all involve some level of gene flow. From: Spaulding et al. (2023).

Two Scenarios

Based on the available information, we can explore two possible scenarios for the mito-nuclear discordance in the Green-winged Teal complex: (1) sex-biased gene flow, and (2) mtDNA capture.

The first scenario (sex-biased gene flow) takes into account the ecology of these ducks. Males are known to disperse whereas females are philopatric (i.e. they return to the same breeding areas). It is thus possible that the mtDNA – which is inherited through the female line – depicts the “true” evolutionary history of the Green-winged Teal complex. And this history is consequently muddled in the nuclear DNA by dispersing males that connect the different taxa through gene flow. In my own research, I found a similar pattern in the Bean Goose complex where extensive hybridization between the Taiga and the Tundra Bean Goose erased the phylogenetic branching pattern between these taxa and the Pink-footed Goose.

The second scenario involves mtDNA capture (see this blog post for another example of this phenomenon). The mitochondrial phylogeny unites the American Teal and the Yellow-billed Teal even though they breed on different continents. However, American Teals are known to winter in the north of South America (e.g., Venezuela, Colombia and Ecuador). The authors note that “it is plausible that wintering A. c. carolinensis males occasionally pair bond with A. flavirostris females and remain there to reproduce rather than return to northern breeding grounds.” The offspring of these adventurous males will carry mtDNA from the Yellow-billed Teal which they could consequently introduce into the North American breeding populations. Perhaps this exchange occurred several times in the distant past.

Both scenarios are possible. So, more research is needed to unravel the exact evolutionary history of the Green-winged Teal complex. One thing is certain though: it’s complicated.

References

Spaulding, F., McLaughlin, J. F., Cheek, R. G., McCracken, K. G., Glenn, T. C., & Winker, K. (2023). Population genomics indicate three different modes of divergence and speciation with gene flow in the green-winged teal duck complex. Molecular Phylogenetics and Evolution, 182, 107733.

Featured image: Eurasian Teal (A. crecca) © Koshy Koshy | Wikimedia Commons