Flipping DNA: The role of inversions in avian evolution

A short overview of chromosomal inversions and their effect on the ecology and evolution of birds.

The mating system of the Ruff (Calidris pugnax) is peculiar. Males come in three types: aggressive independents, submissive satellites and female-mimicing faeders. The independents, recognizable by their black or chestnut ruffs, hold territories where they hope to attract as many females as possible. The white-ruffed satellites don’t have their own territory, but sneak into the independents’ ranges, trying to mate with the visiting females. The faeders, finally, blend in with the females and copulate secretely. This complicated system is determined by a chromosomal inversion.

ruffs.jpg

The three ruff morphs: (left to right) faeder, satellite & territorial (from: https://www.flickr.com/photos/sfupamr/22674449779/in/photostream/)

 

Flipping DNA

What is an inversion? In essence, it is just a region in the DNA that has been flipped around. Compare it to reading part of a sentence from right to left:

SOME TEXT – THIS IS AN INVERSION – SOME MORE TEXT

SOME TEXT – NOISREVNI NA SI SIHT – SOME MORE TEXT

These inversions were discovered by Alfred Sturtevant in the 1920s when he was studying several Drosophila species. It was thought that most inversions are small. But recent genomic studies revealed that inversions can be huge, ranging from 130 kilobases (130 000 DNA letters) to 100 megabases (100 000 000 DNA letters). A recent paper by Maren Wellenreuther and Louis Bernatchez provides a nice overview of the ecological and evolutionary consequences of these big inversions. In this blog post, I will focus on the avian examples in that paper.

 

Mating Systems

In a 2016 Nature Genetics paper, Clemens Küpper and his colleages described the inversion that controls the mating system in the Ruff. It concerns a chunk of about 4.5 Mb, containing 125 genes, on chromosome 11. If a male carries two copies the ancestral (i.e. not inverted) genomic region, he will develop into an independent. One copy of the inversion results in a satellite or faeder male, depending on the genetic variants within the inversion. An individual with two copies of the inversion will die because of issues in cell division (for those interested in the details, one inversion breakpoint disrupts the CENP-N gene which is essential for mitotic centromere assembly).

A similar situation was described for the White-throated Sparrow (Zonotrichia albicollis). Here, a 100 Mb inversion with 1137 genes is associated with two plumage phenotypes, white-striped and tan-striped birds, that differ in territorial and parental behavior.  Interestingly, the white-striped birds almost exclusively mate with tan-striped birds, giving rise to four “sexes”.

white-throated-sparrows

An inversion in the White-throated Sparrow genome results in two morphs: white-striped and tan-striped (from: https://www.northcountrypublicradio.org/).

 

Sperm speed

The inversions in the Ruff and the White-throated Sparrow result in clear phenotypes. Other avian cases are not so obvious. For example, in the Zebra Finch (Taeniopygia guttata) an inversion on the sex chromosome is related to sperm morphology. Birds with an ancestral and an inverted copy (i.e. heterozygotes) have the fastest sperm. Since it pays off to be heterozygous, selection preserves a balance between the ancestral and the inverted variant in the population. This finding was published in Nature Ecology & Evolution.

zebra finch.jpg

In Zebra Finches, an inversion explains variation in sperm speed (from: http://www.efinch.com/)

 

Migratory Inversions

Some time ago, I wrote about a study into the migratory behavior of the Willow Warbler (Phylloscopus trochilus) in Europe. One subspecies (P. t. trochilus) migrates to the southwest to wintering areas in West Africa, whereas the other subspecies (P. t. acredula) migrates in a southeastern direction to winter in Eastern and Southern Africa. Genomic analyses of these disparate migration strategies suggested that three genomic regions – on chromosomes 1, 3 and 5 – were involved. These regions are probably inversions.

willow warbler

A Willow Warbler (from http://www.naturespot.org.uk)

 

Speciation and Hybridization

The genetic characteristics of inversions suggest that they can play an important role in speciation. The flipping of DNA captures a host of genes that consequently behave as a kind of “supergene”. Divergent selection on such supergenes can result a barrier against hybridization. In hybrids, the ancestral and the inverted region might become incompatible, resulting hybrid sterility or inviability. Based on this scenario, you expect that species that live in the same area harbour more inversions than geographically isolated species, because the inversions “protect” the species against maladaptive hybridization. This prediction was recently confirmed by Daniel Hooper and Trevor Price.  Clearly, inversions are a crucial component in avian evolution. Something to keep an eye on.

 

References

Campagna, L. (2016) Supergenes: The Genomic Architecture of a Bird with Four Sexes. Current Biology, 16(3):R105-R107.

Hooper, D.M. & Price, T.D. (2017) Chromosomal inversion differences correlate with range overlap in passerine birds. Nature Ecology & Evolution, 1:1526–1534.

Kim, K.-W. (2017) A sex-linked supergene controls sperm morphology and swimming speed in a songbird. Nature Ecology & Evolution, 1:1168–1176.

Küpper, C. et al. (2016) A supergene determines highly divergent male reproductive morphs in the ruff. Nature Genetics, 48:79-83.

Lundberg, M. et al. (2017) Genetic differences between willow warbler migratory phenotypes are few and cluster in large haplotype blocks. Evolution Letters 1: 155-168.

Wellenreuther, M. & Bernatchez, L. (2018) Eco-Evolutionary Genomics of Chromosomal Inversions. Trends in Ecology & Evolution, 33(6):427-440.

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