The largest sex-chromosome found in birds consists of parts from several other chromosomes.
Let’s talk about sex. To be more specific, let’s talk about sex chromosomes. Most people are familiar with the human system of sex-determination: if you have two X-chromosomes, you are female; and if you have an X and a Y-chromosome, you are male. In birds, the situation is slightly different. Males have two Z-chromosomes, whereas females have a Z and a W chromosome. However, a recent study on larks in the Proceedings of the Royal Society B shows that things are not always that straightforward.
Evolution of sex-chromosomes
The sex-determining locus
Before we delve into the findings of that study, we first need to understand the evolution of sex-chromosomes. Who are they? Where do they come from? What drives them? It mostly starts with one genetic locus: the sex-determining locus. Most mammals carry the gene SRY (sex-determining region Y) on the Y-chromosome which is responsible for the start of male sex-determination. In birds, the gene DMRT1 (Doublesex and mab-3 related transcription factor 1) seems to be an important player. Sex chromosomes initially arise when a standard chromosome (i.e. an autosome) acquires a sex-determining gene.
Suppression of recombination
Next, recombination is suppressed around this gene. Recombination occurs during meiosis when homologous chromosomes line up and exchange sections of themselves. This genetic exchange results in new combinations of genetic variants that evolution can work with. The suppression of recombination between a pair of chromosomes allows them the become different from each other. This explains why the X and Y chromosome look so distinct.
Why did recombination become suppressed? The main hypothesis calls upon sexually antagonistic alleles: genetic variants that are under different selection pressures in males and females. For example, a particular variant might be beneficial in males but detrimental in females. By residing close to the sex-determining locus, these genes end up on different chromosomes and eventually spend most of their time in the sex they benefit.
As more and more sexually antagonistic alleles accumulate around the sex-determining locus, larger sections of the chromosome stop recombining. This recurring process gives rise to “evolutionary strata” on the sex-chromosome that started diverging at different time points.
Degeneration of sex chromosomes
Finally, the sex chromosomes stop recombining altogether, mostly leading to rapid degeneration of one chromosome. In humans, this happened to the Y-chromosome, while in birds, the W-chromosome is degenerating. Eventually, these chromosomes can disappear completely. The figure below gives a nice overview of the evolution of sex chromosomes that I just described.
Back to the larks! Previous studies already indicated that something fishy is going on with the sex-chromosomes of these birds. A cytogenetic study of Bimaculated Lark (Melanocorypha bimaculata) and Horned Lark (Eremophila alpestris) revealed extremely large sex-chromosomes. And a genetic study of the Razo Lark (Alauda razae) indicated sex-specific inheritance of markers on chromosomes 3 and 5. This prompted Hanna Sigeman and her colleagues to have a closer look at these species.
Genomic analyses of four species – Bimaculated Lark, Raso Lark, Eurasian Skylark (Alauda arvensis) and Bearded Reedling (Panurus biarmicus) – uncovered some interesting patterns. The researchers found sex-specific signatures on the entire Z-chromosome (what you would expect), but also on chromosomes 3, 4A and 5. The strength of these signatures varied between the species, suggesting that different parts of these chromosomes have been added to the Z-chromosome at different times.
Using the phylogenetic relationships between the species, the researchers could estimate when different chromosome-sections (or strata) were added to the sex-chromosomes. The first strata is the Z-chromosome itself, which arose about 140 million years ago in an ancestor of birds. The second oldest stratum – coming from chromosome 4A – formed when the suborder Sylvioidea split from all other songbirds, roughly 21-19 million years ago. About 19-17 million years ago, chromosome 3 contributed its first share to the sex-chromosome. A few million years later, between 17 and 14 million years ago (when the Larks and the Bearded Reedling parted ways), chromosome 3 made its second contribution. Finally, chromosome 3 (again!) and 5 were added to the mix between 14 and 6 million years ago. The final result is the largest avian sex-chromosome known to date: 195,300,000 DNA-letters long!
Sigeman, H., Ponnikas, S., Chauhan, P., Dierckx, E., Brooke, M. L. & Hansson, B. (2019) Repeated sex chromosome evolution in vertebrates supported by expanded avian sex chromosomes. Proceedings of the Royal Society B.
Vicoso, B. (2019). Molecular and evolutionary dynamics of animal sex-chromosome turnover. Nature Ecology & Evolution, 1-10.