Rampant introgression across the evolutionary tree of suboscine birds

An extensive genomic study detects numerous cases of interspecific gene flow.

Introgression – the exchange of genetic material through hybridization and backcrossing – seems to be an integral part of avian evolution. In 2017, I published a review paper on this phenomenon, trying to provide an overview of the known cases and the methods to detect introgression. At the time, my search uncovered 165 genetic studies that were published between 1987 and 2017. Most of these papers focused on members of the Passeriformes (songbirds), Galliformes (gamefowl), Anseriformes (waterfowl) and Charadriiformes (gulls, waders and auks), bird orders that display high levels of hybridization. However, I did not attempt to quantify the incidence of introgression, because this would probably be a gross underestimate. Numerous bird species have not been studied with genetic tools yet. Such as quantification would involve a large genomic data set, comprising many species. And that is exactly the approach of a study that recently appeared in the journal Evolution Letters.

D-statistics

Sonal Singhal and her colleagues focused on the suboscines, a clade of passerine birds that comprises more than 1000 species, most of which can be found in South America. Using a genomic dataset of 2389 loci (consisting of ultraconserved elements and exons) for 1306 species, the researchers looked for signatures of introgression. They relied on one of my favorite methods: the D-statistic (also known as the ABBA-BABA test). I have explained this approach so many times that I regularly dream about it (and no, the dream does not involve ABBA-songs). Here is the short explanation from my review:

The D-statistic considers ancestral (‘A’) and derived (‘B’) alleles across the genomes of four taxa. Under the scenario of incomplete lineage sorting without gene flow, two particular allelic patterns ‘ABBA’ and ‘BABA’ should occur equally frequent. An excess of either ABBA or BABA, resulting in a D-statistic that is significantly different from zero, is indicative of gene flow between two taxa.

The researchers calculated this statistic for numerous trios of species. They found that 49 out of 130 trios (38%) had a significant D-statistic. The highest five D-statistics were detected in Dendrocolaptes woodcreepers, Smithornis broadbills, Neopelma manakins, Grallaria antpittas, and Phlegopsis antbirds. I have described hybridization in some of these taxa on their family pages at Avian Hybrids Project (you can click the links if you want to learn more).

An example of the ABBA-BABA test for a trio of species (plus an outgroup). From: Singhal et al. (2021) Evolution Letters.

An Underestimate?

To understand the mechanisms underlying the introgression patterns, the researchers correlated the D-statistics with several environmental variables. These analyses revealed some expected relationships. For example, introgression was most common between species that were geographically close and that experienced higher rates of climate change (which moves species around and might lead to secondary contact). In addition, introgression occurred more between species at lower latitudes. It could be that tropical regions provide more opportunities for introgressive hybridization due to the higher species richness in these areas. It would be interesting to repeat these analyses with more species-specific traits to better understand the drivers of introgression in suboscine birds.

Although an introgression incidence of 38% seems quite high, I think it is probably even an underestimate. The analyses only included trios of closely related species and might thus have missed introgression between more distantly related species. Moreover, the D-statistic does detect gene flow between sister species. It only reports only gene flow between the third species and one of the first two in the phylogenetic tree. The researchers did also not take ghost introgression into account: the exchange of genetic material with unsampled or extinct lineages (see my recent review on this topic for more details). And finally, the analyses involved only a subset of the genome. Who knows how many introgressed regions are hiding in the rest of the genome?

An overview of significant D-statistics (highlighted in orange) across the phylogeny of the suboscines. From: Singhal et al. (2021) Evolution Letters.

References

Singhal, S., Derryberry, G. E., Bravo, G. A., Derryberry, E. P., Brumfield, R. T., & Harvey, M. G. (2021). The dynamics of introgression across an avian radiation. Evolution letters5(6), 568-581.

Featured image: Green-and-black Fruiteater (Pipreola riefferii) © Francesco Veronesi | Wikimedia Commons

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