The estimation of genetic diversity is extra complicated due to some special sex chromosomes.
Birds have two sex chromosomes: Z and W. A bird with one of each (ZW) will be female and a bird with two Z-chromosomes will be male. Simple, right? But biology wouldn’t be biology if there weren’t any exceptions. Members of the avian superfamily Sylvioidea have weird sex chromosomes. Some sections of other chromosomes – namely 4A, 3 and 5 – have fused with the traditional sex chromosomes, giving rise to enlarged neo-sex chromosomes (you can read the details in this blog post). A recent study in the journal Biology Letters added another chromosomes to the mix: in the zitting cisticola (Cisticola juncidis) part of chromosome 4 is now part of a sex chromosome.
Apart from making the evolution of avian sex chromosomes more complicated (and more interesting), these findings also have implications for population genomic studies. For example, if you want to calculate the genetic diversity of a population, these neo-sex chromosomes can wreak havoc. Female birds have only one member of a sex chromosome pair instead of the usual two (i.e. they are hemizygous). The same goes for the sections on other chromosomes that fused with the sex chromosomes. If you don’t know that these chromosome-sections are now also hemizygous and you treat them as “normal” autosomes (i.e. the non-sex chromosomes), you will make errors in calculating genetic diversity.
In a recent paper in Proceedings of the Royal Society B, Elisa Dierickx and her colleagues illustrated the dangers of these neo-sex chromosomes using the Raso Lark (Alauda razae). This species is endemic to the small uninhabited island of Raso in Cape Verde. Latest estimates suggest that the population has been fluctuating between about 50 and 1,500 individuals. The researchers estimated the genetic diversity of this island population. When they accounted for the neo-sex chromosomes, genetic diversity (calculated as average nucleotide diversity, π) was 0.001. This means that there is, on average, one difference in DNA sequence every 1000 base pairs when comparing two individuals. When neo-sex chromosomes are included in the calculations, this estimate almost doubles to 0.0019. That is a huge change, given that these sections only represent 12% of the genome.
Island species tend to have lower population sizes than mainland species, resulting in lower levels of genetic diversity. And indeed, the genetic diversity of the Raso Lark is lower compared to a mainland species, such as the Eurasian skylark (Alauda arvensis) with π equal to 0.0114. However, when we transform the genetic diversity of the Raso Lark to an effective population size, we end up with an intriguing result. Effective population size (Ne) is a quite abstract concept in population genetics. For now, just envision it as a measure for the historical population size. Doing the calculation, we find an effective population size of 50,000. That is much higher than the census population size of maximum 1,500 individuals. What is going on here?
To understand this fascinating finding, the researchers ran several demographic analyses. It turns out that the population size of the Raso Lark was much larger in the past, after an expansion about 110,000 years ago. Recently, the population experienced a dramatic decrease in population size that seems to coincide with the settlement of Cape Verde by humans in 1462. This recent population bottleneck failed to eliminate the high genetic diversity of the large population. The following analogy explains the process. Imagine you have a jar with 50,000 colorful marbles, representing 10,000 distinct colors. If you now sample 1,500 marbles randomly, you will still end up with a very diverse set of marbles because there are so many distinct colors. The Raso lark might not be a very flamboyant bird, but its evolutionary history is definitely quite colorful.
Dierickx, E. G., Sin, S. Y. W., van Veelen, H. P. J., Brooke, M. D. L., Liu, Y., Edwards, S. V., & Martin, S. H. (2020). Genetic diversity, demographic history and neo-sex chromosomes in the Critically Endangered Raso lark. Proceedings of the Royal Society B, 287(1922), 20192613.