Decoupling of genetic and phenotypic evolution in the Tawny-Crowned Greenlet

Study finds deep genomic divergence despite little morphological changes.

South America houses high levels of cryptic bird diversity. Although some populations look morphologically similar, they often exhibit drastic genetic differences. Because the taxonomy of Neotropical birds is largely based on the study of museum specimens, we are probably missing a lot of species.

A notable example concerns the Tawny-Crowned Greenlet (Tunchiornis ochraceiceps). This small songbird can be found from the lowlands of Central America to the Amazon region. Based on subtle differences in plumage and morphometrics, ornithologists have recognized 10 subspecies. Genetic data, however, paint a drastically different picture. Analyses of mitochondrial DNA showed that some of these subspecies diverged ca. 10 million years ago. That would be a distinct species in anyone’s book.

A recent study in the journal Molecular Phylogenetics and Evolution undertook a more detailed analysis of the Tawny-Crowned Greenlet, combining plumage coloration, morphometrics, vocalizations and genomic data. How many cryptic species are hiding in the tropical rainforests?

Six Lineages

Let’s start with the genomic patterns. Based on more than 2000 ultraconserved elements (UCEs), the researchers could delineate six separate lineages (of which two showed signs of substructure). The main split in the phylogenetic tree – dated to about 9 million years ago – differentiates between the western and the eastern lineages. The western group falls apart into populations on both sides of the Andes, whereas the eastern group is subdivided by different Amazonian rivers. The figure below provides a nice overview of the complex geographical distribution of these genetic lineages.

Genomic analyses suggested six distinct lineages across Central and South America. From: Buainain et al. (2021).

Phenotypic Boundaries

But can we also discriminate between these lineages with phenotypic data or vocalizations? When it comes to morphometrics and song, the answer is no. The authors indicate that “no clear spatial separation between samples belonging to the two [genetic] clusters can be seen in the [morphological] classification graph” and “the quantitative analysis shows no diagnostic vocal characters for any of the populations of T. ochraceiceps.”

In terms of plumage coloration, the situation is slightly better. One plumage character – the coloration of the forehead and crown – can be used to distinguish between three groups, namely populations in the west, northeast of the Amazon and southeast of the Amazon. Other plumage traits were not diagnostic for different populations, but did show variation across the distribution of the Tawny-Crowned Greenlet. In most cases, the geographic extremes were clearly different with a large area of intermediate phenotypes in between. Drawing clear phenotypic boundaries between populations is difficult, at best.

Some examples of plumage traits that distinguished some populations of the Tawny-Crowned Greenlet. In general, however, it was difficult to determine clear phenotypic boundaries. From: Buainain et al. (2021).

A Conservative Species

These analyses reveal an interesting evolutionary pattern: the decoupling of genetic and phenotypic evolution. Although the Tawny-Crowned Greenlet is composed of genetically distinct populations, this differentiation is not reflected in the phenotypic variation. Why is the phenotype of this (group of) species so conserved? The researchers offer several explanations that require further investigation:

• Stabilizing selection: there is no selective pressure – social or ecological – to develop morphological or vocal differences.
• Habitat specialist: the Tawny-Crowned Greenlet follows a specific habitat type which does not require it to adapt morphologically.

Finally, the authors propose a taxonomic arrangement for the six genetic lineages. They divide them into four distinct species, of which two species are further separated into two subspecies: T. o. ochraceiceps, T. o. bulunensis, T. ferrugineifrons, T. luteifrons, T. r. rubrifrons and T. r. lutescens. This classification might change in the future. Stay tuned.

Geographical distribution of the six taxa (species and subspecies) in the Tawny-Crowned Greenlet. From: Buainain et al. (2021).

References

Buainain, N., Maximiano, M. F., Ferreira, M., Aleixo, A., Faircloth, B. C., Brumfield, R. T., … & Ribas, C. C. (2021). Multiple species and deep genomic divergences despite little phenotypic differentiation in an ancient Neotropical songbird, Tunchiornis ochraceiceps (Sclater, 1860)(Aves: Vireonidae). Molecular Phylogenetics and Evolution, 162, 107206.

Milá, B., Tavares, E. S., Munoz Saldana, A., Karubian, J., Smith, T. B., & Baker, A. J. (2012). A trans-Amazonian screening of mtDNA reveals deep intraspecific divergence in forest birds and suggests a vast underestimation of species diversity. PLoS One, 7(7), e40541.

Featured image: Tawny-Crowned Greenlet (Tunchiornis ochraceiceps) © Dominic Sherony | Wikimedia Commons