A supergene determines morphological variation in redpolls

But are these redpolls different species or not?

“Thus, redpolls appear to function as a single species harboring ecotypic variation, rather than three distinct species.” This statement caught my attention while I was reading a recent Nature Communications paper by Erik Funk and his colleagues. Using genomic data from 73 individuals, they managed to pinpoint the genetic basis of three redpoll taxa that are currently described as separate species: the Hoary Redpoll (Acanthis hornemanni), the Common Redpoll (A. flammea), and the Lesser Redpoll (A. cabaret). The morphological variation between these three taxa could be traced back to a big inversion – about 55 million DNA-letters long – on chromosome one (see this blog post for more information on inversions). This genomic region contains almost 500 genes, several of which are involved in plumage pigmentation and beak morphology. As all these genes are tightly linked and inherited together, the researchers describe it as a “supergene”.

The taxonomically-orientated reader might now be confused by the first sentence of this blog post. These redpolls are morphologically distinct and we now know the genetic basis of these differences. Why refer to them as ecotypes, and not species? Let’s find out.

Morphological differences between the three redpolls species – or ecotypes – in the study. From: Funk et al. (2021).

Three Genotypes

Detailed analyses of the inversion revealed three clusters that do not completely correspond to the three redpoll taxa. Two clusters contain multiple species, namely Lesser Redpolls with Common Redpolls, and Hoary Redpolls with Common Redpolls. The third cluster consists almost entirely of Hoary Redpolls. The researchers assigned these clusters to three inversion genotypes: AA, AB and BB. Interestingly, these genotypes seem to align with plumage patterns:

Transitioning from the AA, to AB, to BB genotype also broadly mirrors a transition in phenotype from dark to light plumage coloration, where the AA genotype is associated with dark plumage, BB is associated with light plumage, and AB is intermediate.

Moreover, the geographical distribution of the three genotypes follows a latitudinal gradient with AA-birds at low latitudes and BB-birds at high latitudes. The heterozygotes (AB) occupy an intermediate position. These patterns suggest that the inversion might play a role in local adaptation. Indeed, bird species with white plumage and small beaks, such as the BB-redpolls, tend to occur in high-altitude regions.

The three inversion genotypes do not correspond to the three redpolls species (left figure), but do show a relationship with latitude (right figure). From: Funk et al. (2021).

Reproductive Isolation

The observation of heterozygotes (AB-birds) indicates that no combination of the supergene is lethal. This situation is different from other cases where certain combinations are often sterile or unviable due to genetic incompatibility. In Ruffs (Philomachus pugnax), for example, homozygotes with an inverted region are unviable and heterozygotes show low survival rates. The lack of lethal combinations in redpolls suggests that the inversion does not play an important role in reproductive isolation between the taxa. In fact, intermediate individuals and mixed pairs have been observed in the wild. Moreover, the genetic analyses in the current study indicated significant levels of gene flow between the redpoll taxa.

With this additional information about local adaptation and reproductive isolation, we can return to the statement about ecotypes versus species that kicked off this blog post. Here is the complete quote from the paper.

In light of the link between the redpoll supergene and phenotype and differences in breeding distribution between ecotypes, the supergene may impart local adaptation to the environment. However, given the detection of inversion heterozygotes and the presence of gene flow, the inversion likely does not influence reproductive isolation. Thus, redpolls appear to function as a single species harboring ecotypic variation, rather than as three distinct species.

It is clear that the authors are referring to “biological species” where a certain level of reproductive isolation is required. However, some ornithologists might focus on the morphological and genetic differences between the taxa, and downplay the relevance of reproductive isolation. I will not get involved in this debate and will leave the final decision with taxonomists. Honestly, I do not care whether these redpolls are classified as species, subspecies or ecotypes. I prefer to focus on the ecological and evolutionary impact of their supergene, which is obviously super-interesting.

References

Funk, E. R., Mason, N. A., Pálsson, S., Albrecht, T., Johnson, J. A., & Taylor, S. A. (2021). A supergene underlies linked variation in color and morphology in a Holarctic songbird. Nature communications12(1), 1-11.

Featured image: Common Redpoll (Acanthis flammea) © Jyrki Salmi | Wikimedia Commons

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