Genetic study reveals how four different sparrow species adapted to life in the salt marshes

If you put butter and salt on it, it tastes like salty butter.”

– Terry Pratchett (Moving Pictures)

Salt marshes are a relatively new feature in the North American landscape. The expansion of these habitats occurred only a few thousand years ago. In this short time span, several bird species have quickly adapted to living in these salty conditions. Adaptations include a larger bill to facilitate heat exchange in these open environments and an altered kidney structure to cope with the salty drinking water. Members of the bird family Passerellidae seem to have an inordinate fondness for salt marshes, four lineages have independently colonized this habitat. A recent study in the journal Evolution Letters investigated whether these birds used the same genetic tricks to thrive in this new environment.

Passerculus_sandwichensis_crop.jpg

A singing Savannah Sparrow © Cephas | Wikimedia Commons

 

Parallel Evolution

Jennifer Walsh and her colleagues compared the genomes of four salt marsh specialists with their upland cousins (see list below). They wanted to know whether the salt-adapted subspecies survive in the salt marshes due to parallel evolution, which they define as “shared [genomic] regions of elevated differentiation between multiple upland-salt marsh pairs.” Alternatively, differentiated regions that are only found in one subspecies pairs are an example of lineage-specific evolution.

  • Savannah Sparrows (Passerculus sandwichensis nevadensis and Passerculus sandwichensis beldingi)
  • Nelson’s sparrows (Ammospiza nelsoni nelsoni and Ammospiza nelsoni subvirgatus)
  • Song Sparrows (Melospiza melodia gouldii and Melospiza melodia pusillula)
  • Swamp Sparrows (Melospiza georgiana georgiana and Melospiza georgiana nigrescens).

The researchers found no regions of elevated differentiation that were shared by all four subspecies pairs. However, some differentiated regions were shared among two or three pairs. In total, the analyses yielded 33 candidate regions that contained 16 genes with a putative role in adaptation to salt marshes.

Nelson's_Sparrow_(10301730173).jpg

A Nelson’s Sparrow © Andy Reago & Chrissy McClarren | Wikimedia Commons

 

Osmoregulation

Most of the candidate genes were involved in osmoregulation (i.e. maintaining the fluid balance and the concentration of salts to keep the body fluids from becoming too diluted or concentrated). This makes sense because salty environments can disturb the osmotic balance of cells. Interestingly, different osmoregulation genes were under selection in different subspecies pairs.

In Savannah Sparrows, the researchers found WNK2 under selection. This gene plays an important role in regulating cell volume in response to osmotic stress. In Nelson’s Sparrows, MMP17 showed signs of selection. This gene has been linked to drinking behavior and kidney function in mice. In Song Sparrows, yet another gene popped up: MYOF, which is differentially expressed when fish are transferred from fresh to salt water. And in Swamp Sparrows, SLC9A3 has been under selection, a gene that is involved in sodium transport across the cell membrane.

These examples suggest that “these [osmoregulation] pathways are common targets of selection, but the specific genic targets of selection within the pathways differ among species.”

Melospiza-melodia-001.jpg

A Song Sparrow © Mdf | Wikimedia Commons

 

Gene Flow

The researchers also reconstructed the demographic histories of all subspecies pairs. They did this to rule out any demographic factors that might influence their search for differentiated regions. These analyses revealed continuous gene flow between each pair of subspecies. This observation raises the question whether introgression of beneficial alleles might have facilitated adaptation to salt marshes. Indeed, a previous study on Nelson’s Sparrows identified several candidate genes for adaptive introgression. Whether this also occurred in the other lineages remains to be determined.

Melospiza_georgiana_MN2.jpg

A Swamp Sparrow © Cephas | Wikimedia Commons

 

References

Walsh, J., Benham, P. M., Deane‐Coe, P. E., Arcese, P., Butcher, B. G., Chan, Y. L., … & Shriver, W. G. (2019). Genomics of rapid ecological divergence and parallel adaptation in four tidal marsh sparrows. Evolution Letters.

 

This paper has been added to the Passerillidae page.

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