The role of positive selection during the genomic evolution of Flycatchers

Comparing four species of Ficedula flycatchers to unravel their genomic landscape of differentiation.

One of the most interesting debates in speciation research revolves around the genomic landscape of differentiation. Scan across the genomes of two closely related species and calculate the level of genetic differentiation as you go along. This exercise will probably reveal a heterogenous picture with some genomic regions that show little genetic differences, and other regions that are highly divergent. With some imagination, you can recognize a hilly landscape with valleys and peaks. Most research efforts have focused on the origin of the peaks in this landscape, so-called “genomic islands of differentiation”. What evolutionary processes underlie the formation of these differentiated regions?

Reproductive Isolation and Selection

The earliest studies interpreted these patterns in the context of speciation-with-gene-flow, suggesting that these genomic islands contain loci that contribute to reproductive isolation. When two species interbreed, these barrier loci are expected to be immune to introgression. Hence, they will diverge while the remainder of the genome is homogenized by introgression. This explanation might apply to some study systems, such as bean geese.

Alternatively, selection events might be responsible for origin of genomic islands. This can either be negative selection against recurring deleterious alleles (also known as background selection) or positive selection for beneficial alleles. Because peaks in genetic differentiation are often shared between species, some authors have argued that positive selection is not a reasonable explanation. The rationale is that positive selection is unlikely to occur in the same genomic regions over long evolutionary periods. Instead, background selection is presented as the dominant force shaping genomic landscapes. Because the genomes of birds are relatively stable – in terms of recombination rate and gene density – the targets of background selection will remain the same over millions of years.

Four Flycatchers

To discriminate between background selection and positive selection, it would make sense to choose on a study system where introgression plays a minor role. That is why Madeline Chase and her colleagues focused on two independent species pairs of Ficedula flycatchers: the Pied Flycatcher (F. hypoleuca) and the Collared Flycatcher (F. albicollis), and the Red-breasted Flycatcher (F. parva) and the Taiga Flycatcher (F. albicilla). First, they constructed the genomic landscapes of these species pairs and identified the location of numerous genomic islands of differentiation (based on the summary statistic FST). Next, the researchers performed several tests for positive selection, namely Fay and Wu’s H and the composite likelihood test (CLR). The analyses revealed that most selective sweeps coincided with the previously identified peaks in FST. These findings suggest that positive selection plays an important role in shaping the genomic landscape of these flycatchers (similar to patterns uncovered in Sporophila Seedeaters using a different method).

Overview of the genomic landscape of differentiation for four flycatcher species. Different circles indicate a variety of summary statistics. The most relevant ones for this blog post are FST and DXY. From: Chase et al. (2021).

Recurrent Selection

Now that we know that positive selection is involved, we can go one step further: when did these selective sweeps happen? Are these genetic signatures the result of repeated selection in these species and their ancestral population (i.e. recurrent selection model) or do they represent species-specific selection after speciation occurred (i.e. selection in allopatry model). Some researchers proposed that you can discriminate between these models by looking at three different summary statistics: FST, DXY and π (see this blog post for a detailed explanation). The rationale behind this approach was nicely described in the paper:

Because DXY is unaffected by current levels of diversity, under the selection in allopatry scenario, DXY is expected to be similar both within and outside of FST peaks. However, when selection has recurrently impacted a region from the common ancestor of two species, ancestral diversity will have also been reduced, leading to a reduction in DXY in FST peaks.

Calculating DXY across the species pairs indicated that this summary statistic was consistently lower in the FST peaks for Pied and Collared Flycatcher. A pattern that is consistent with recurrent selection. In the Red-breasted and Taiga Flycatcher comparison, however, this was not the case: DXY was higher in the FST peaks. What is going on here? The researchers think that as species differentiation proceeds, substitutions become fixed in certain genomic regions – perhaps due to positive selection – resulting in a higher DXY value. Because Red-breasted and Taiga Flycatcher diverged before Pied and Collared Flycatcher, they have had more time to accumulate substitutions and inflate their DXY. The shared FST peaks might thus still be the outcome of recurrent selection. Hence, the timescale of species divergence is important to keep in mind when interpreting these summary statistics.

Finally, the researchers also uncovered several lineage-specific signatures of selection that seemed to coincide with changes in local recombination rates. All in all, the patterns uncovered in this study highlight the interplay of positive selection and recombination in the evolution of genomic landscapes of differentiation.

References

Chase, M. A., Ellegren, H., & Mugal, C. F. (2021). Positive selection plays a major role in shaping signatures of differentiation across the genomic landscape of two independent Ficedula flycatcher species pairs. Evolution75(9), 2179-2196.

Featured image: Red-breasted Flycatcher (Ficedula parva) © Nppgrandmeadow | Wikimedia Commons

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