How low can you go? Exploring sex-linked genetic diversity in Barn Swallows

What evolutionary processes determine levels of genetic diversity on the Z-chromosome?

“Theory and empirical patterns suggest a disproportionate role for sex chromosomes in evolution and speciation.” This opening sentence from Darren Irwin’s excellent review on sex chromosomes perfectly illustrates why evolutionary biologists are so interested in these chromosomes. They often show peculiar patterns of genetic change, allowing researchers to formulate precise theoretical predictions which can consequently be tested with actual data. Take, for example, genetic diversity on the Z-chromosome. In birds, males have two Z-chromosomes, whereas females have one Z-chromosome and one W-chromosome. Hence, the Z-chromosome will be present in a population at a frequency of 3/4 compared to “normal” chromosomes (or autosomes). Similarly, the W-chromosome will be found at a frequency of 1/4 relative to autosomes. These lower frequencies mean that sex chromosomes will harbor less genetic diversity than autosomes.

If no other ecological or evolutionary processes are at play, we can expect the level of genetic diversity on the Z-chromosome to be 3/4 of the autosomes. But Z-linked genetic diversity can be reduced even more when the mating success of males is highly skewed. If a few males account for the majority of the offspring, there will be a significant reduction in genetic diversity on the Z-chromosome. To visualize this process, imagine a population of colorful candies (red, blue, green, yellow, orange, purple). If only red candies are allowed to “reproduce” and make it to the next generation, you will end up with a very low level of diversity. Brian Charlesworth calculated that this mating effect can push the level of genetic diversity to a minimum of 0.56 (compared to 0.75 under standard conditions). A recent study in the journal Molecular Ecology explored patterns of genetic diversity on the Z-chromosomes of Barn Swallows (Hirundo rustica). Do these birds conform to theoretical expectations?

Bottlenecks and Linked Selection

Drew Schield and his colleagues analyzed the levels of genetic diversity for 160 individuals, representing six subspecies of the Barn Swallow. For each subspecies (and several hybrid zones), they calculated the ratio between genetic diversity on the Z-chromosome and the autosomes. As explained above, theoretical work suggests that this ratio should be 0.75 under neutral conditions and can drop to 0.56 in cases of extreme skews in mating success. In Barn Swallows, the average ratio was even lower: 0.48. In fact, most subspecies were well below the theoretical minimum of 0.56. These patterns suggest that other evolutionary forces are at play here. The researchers point to “recent demographic history, linked selection and divergence hitchhiking” as possible explanations (see this paper for a short explanation of linked selection).

Previous work indicated that Barn Swallows have experienced recent population bottlenecks. These demographic changes are expected to affect the Z-chromosome more relative to autosomes, contributing to further reductions in genetic diversity on this sex chromosome. In addition, the Z-chromosome exhibits lower recombination rates compared to autosomes. Because less genetic reshuffling occurs on the Z-chromosome, larger genomic sections will be impacted by selection. If one genetic variant is under strong selection, all neighboring variants that are linked to it will hitchhike along. Large regions might thus lose genetic diversity.

Comparisons of genetic diversity on autosomes and Z-chromosomes for six subspecies and several hybrid zones (figure a) revealed that the ratio between these chromosomes is will below the theoretical minimum of 0.56 (orange region in figures b and c). From: Schield et al. (2021).

Genomic Islands

In addition to the low genetic diversity on the Z-chromosome, the researchers also noted increased genetic differentiation between the subspecies on this sex chromosome. Indeed, the Z-chromosome clearly stands out in the genomic landscape of differentiation (see this blog post for more details on this concept). The exact mechanism underlying these peaks in genetic differentiation remain to be determined. The main contenders are linked selection (as explained above) or reduced introgression on the Z-chromosome. The latter explanation entails that the Z-chromosome harbors genomic regions that contribute to reproductive isolation. If these regions are immune to introgression, they will diverge over time. Disentangling the relative contribution of these processes will require a more detailed exploration of the genes on the Z-chromosome. Clearly, sex chromosomes still hold many secrets.

Exploring the genomic landscape of differentiation (using the Population Branch Statistic) in the six subspecies revealed highly differentiated regions on the Z-chromosome (in green). From: Schield et al. (2021).

References

Schield, D. R., Scordato, E. S., Smith, C. C., Carter, J. K., Cherkaoui, S. I., Gombobaatar, S., … & Safran, R. J. (2021). Sex‐linked genetic diversity and differentiation in a globally distributed avian species complex. Molecular Ecology30(10), 2313-2332.

Featured image: Barn Swallow (Hirundo rustica) © Stefan Berndtsson | Wikimedia Commons

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