A gene within a supergene: An estrogen receptor shapes the behavior of White-throated Sparrow morphs

Expression levels of the estrogen receptor determine aggressive behavior in these songbirds.

White-throated sparrows (Zonotrichia albicollis) come in two distinct morphs: the white-striped (WS) and the tan-striped morph (TS). These morphs do not only differ in their plumage patterns, but also in behavior, such as the degree of parental care that they provide (which I discussed in this blog post). The differences between these morphs have a solid genetic basis. Already in 1966, Thorneycroft identified a chromosomal rearrangement that explains the occurrence of the two white-throated sparrow morphs. Recent molecular work showed that this rearrangement is an inversion (i.e. a flipped section of DNA, more on inversions in this blog post), giving rise to a so-called supergene which links numerous genes that influence the morphology and behavior of these birds. Tan morphs have the same version of the supergene (i.e. they are homozygous) whereas white-striped morphs have two different versions (i.e. they are heterozygous).

Knowing that a supergene underlies the different morphs is only the first step. Now, we can zoom in on the contents of this supergene and determine how these linked genes work together in shaping the plumage and behavior of white-throated sparrows. A recent study in the journal PNAS performed some clever experiments to understand the role of one particular gene.

The different morphs of the White-throated Sparrow (A and B) prefer to mate with the opposite morph (see percentages in C). The differences between the morphs can be traced back to a super-gene (D). From: Campagna (2016) Current Biology.

Estrogen Receptor

As mentioned above, the white-striped and the tan-striped morphs behave differently. Studies in wild populations found that WS birds are more aggressive compared to TS birds when defending their territories. Given that territorial aggression in songbirds has been linked to steroid hormones, it makes sense to search for genes that are involved in the production or processing of these hormones. Interestingly, one of the genes (ESR1) in the supergene codes for an estrogen-receptor. Moreover, this gene comes in two different versions (ZAL2 and ZAL2m) that follow the genetic patterns underlying the two morphs. Tan morphs have the same version of gene (two times ZAL2) whereas white-striped morphs have two different versions (ZAL2 and ZAL2m). Sounds like the perfect candidate gene!

The researchers quantified the level of aggression of different birds in several behavioral trials. Next, they measured the expression levels of the different ESR1-versions in certain brain areas. They summarized their findings as follows: “the degree to which a bird engaged in territorial aggression, which was markedly higher in the WS birds than in the TS birds, was predicted by the relative expression of the ZAL2m allele.” In another experiment, the researchers knocked down the expression of the ESR1-gene in certain brain areas and assessed the aggression of the birds. This experiment revealed that the more aggressive birds became less aggressive when the ESR1-gene was turned off.

One allele (ZAL2m, in red) was more highly expressed in white-striped morphs, and correlated with aggressive behavior (measures as the number of songs per 10 minutes). These results support a central role for the estrogen receptor in shaping the behavior of the morphs. From: Merritt et al. (2020) PNAS.

Gene Network

These findings provides direct evidence that the estrogen-receptor plays a crucial role in determining the behavior of these morphs. However, it remains to be determined how it actually works. This receptor is a transcription factor that interactions with a large number of other proteins as well as with numerous regulatory elements. A previous study reported that ESR1 lies within an interconnected module of 157 genes that are differentially expressed between the morphs. Of these 157 genes, 115 are located in the supergene. More experimental work is needed to disentangle this complex web. Slowly but steadily we are getting closer to the genetic underpinnings of these intriguing morphs.

References

Merritt, J. R., Grogan, K. E., Zinzow-Kramer, W. M., Sun, D., Ortlund, E. A., Soojin, V. Y., & Maney, D. L. (2020). A supergene-linked estrogen receptor drives alternative phenotypes in a polymorphic songbird. Proceedings of the National Academy of Sciences117(35), 21673-21680.

Featured image: White-throated sparrows (Zonotrichia albicollis) © Cephas | Wikimedia Commons

Admixture in Amazonia: Reconstructing the evolutionary history of the Pectoral Sparrow

Genomic data tell the story of how this passerine spread across South America.

Apart from managing the Avian Hybrids Project, I regularly contribute to the blog of the British Ornithologists’ Union (the BOUblog, you can find an overview of my blog posts here). A few weeks ago, I published my 50th story for the BOUblog, which focused on the phylogenetics of the Pectoral Sparrow (Arremon taciturnus). A recent study used mitochondrial DNA to unravel the evolutionary history of this neotropical species. The researchers uncovered six distinct lineages and speculated about the factors responsible for their origins. Here is my summary:

Could it be that the origin of these rivers drove the diversification of the Pectoral Sparrow? Not exactly, because these rivers started crisscrossing the South American landscape between 9 and 2.5 million years ago. The rivers certainly prevent neighboring populations from mixing extensively, but they are not the main cause for the origin of these lineages. Rather, the researchers suspect that ‘past ecological barriers must have played a role in accounting for the observed phylogeographical structure.’ During the glacial cycles of the Pleistocene, forests contracted and expanded. The Pectoral Sparrows became isolated in forest fragments during contraction phases and followed the spreading forests during the expansions. At rivers, however, the birds could not disperse further, giving rise to the geographical boundaries between the six lineages. Amazing what you can deduce from a string of A, T, G and Cs.

Although this scenario seems plausible, it remains largely speculative. Indeed, the authors indicated the uncertainties in their proposed model and wrote that “alternative scenarios could be tested with more powerful genomic datasets.” Luckily, another recent paper did just that. Using genomic data, Nelson Buainain and his colleagues provided a more fine-grained picture of the evolution of the Pectoral Sparrow.

Analyses of mitochondrial DNA indicated six distinct lineages within the Pectoral Sparrow. From: Carneiro de Melo Moura et al. (2020) Ibis.

Genotypes and Phenotypes

In contrast to the six mitochondrial lineages, the genomic data suggested four main genetic clusters. The genetic make-up of these four groups reveals an interesting pattern. Individuals from the Guyana Shield (region A in the figure above), southwestern Amazonia (region F) and the Atlantic Forest (region D) generally have “pure” genotypes. In other words, they do not share genetic variation with other regions. In central Amazonia (regions B, C and E), however, individuals have admixed genotypes.

The genetic patterns are mirrored in the plumage of the birds. In the genetically “pure” populations, pectoral band patterns are mostly homogenous, whereas the admixed populations show a variety of shapes and sizes in the pectoral bands. The most likely scenario is that populations became isolated in different forest patches across central Amazonia and established secondary contact, giving rise to the genetic and morphological variety we see today. This interpretation was further supported by ecological niche modelling.

Genetic and morphological variation across the range of the Pectoral Sparrow. Notice the admixed nature of the populations in central Amazonia. From: Buainain et al. (2020) Molecular Ecology.

North to South

The genetic analyses indicated that the populations north and south of the Amazon separated about 160,000 to 380,000 years ago. The higher genetic diversity in the northern populations of the Guyana Shield suggest that the Pectoral Sparrow started its journey across South America here. As birds spread to the south, they separated into distinct populations, settling in the patches of suitable habitat. These populations were probably separated in at least three regions south of the Amazon River, namely southwestern Amazonia and south‐central Amazonia and the Atlantic Forest. These regions functioned as refugia during harsh climatic periods when forest fragments were isolated. Occasionally, climatic changes would cause these forests to expand, resulting in the secondary contact that I described above. This scenario nicely builds upon the patterns that arose from the mitochondrial study. Step by step, we are unraveling the complex evolutionary history of South American birds.

References

Buainain, N., Canton, R., Zuquim, G., Tuomisto, H., Hrbek, T., Sato, H., & Ribas, C. C. (2020). Paleoclimatic evolution as the main driver of current genomic diversity in the widespread and polymorphic Neotropical songbird Arremon taciturnus. Molecular Ecology29(15), 2922-2939.

Featured image: Pectoral Sparrow (Arremon taciturnus) © Caio Brito | eBird