From the Amazon to the Atlantic Forest: the evolutionary story of the Blue-backed Manakin

What geological and ecological processes explain the distribution of this species?

At the moment, I am enjoying a well-deserved holiday with my family in Belgium. Apart from writing blog posts for the Avian Hybrids Project, I fill my free time with reading books and watching some Netflix-series (for those interested: I am currently watching The Walking Dead and Titans). Nothing more relaxing than immersing yourself in good story. But you don’t need to switch in your television or dive into the writings of Stephen King or George R. R. Martin to find these stories. Nature is full of amazing stories on a huge variety of species. For example, a recent study in the Journal of Ornithology used genetic analyses and ancestral area reconstructions to tell the evolutionary story of the Blue-backed Manakin (Chiroxiphia pareola) across South America. Sit back, relax and enjoy this epic journey from the Amazon to the Atlantic Forest.

Changing Rivers

Our story starts about 3 million years ago in the Amazon region where an ancestral population of the Blue-backed Manakin resides. At the end of the Pliocene (ca. 2.8 million years ago), massive erosion events changed the river dynamics in this area and split the ancestral population in two. Later on, the resulting western population gave rise to the subspecies regina and napensis, which became isolated on opposite sides of the Marañon River and Ucayali River. The eastern population, on the other hand, moved into the Guiana Shield (a mountain range in the northeast of South America), evolving into the subspecies pareola. These events nicely show how different processes – vicariance and dispersal – come into play during the evolutionary history of a bird species.

Fast forward to about 0.5 million years ago and we can see that the eastern population has colonized the Atlantic Forest. In previous blog posts – on the Variable Antshrike (Thamnophilus caerulescens) and Buff-browed Foliage Gleaner (Syndactyla rufosuperciliata) – I described several routes into the Atlantic Forest. But how did the Blue-backed Manakin get there? Based on ecological niche modelling, the authors argue that this species followed “a scenario in which a connection between the Amazonian and northeastern Atlantic Forest occurred in the early/middle Pleistocene via routes that extended through the interior of the Brazilian northeast.” This connection is supported by studies on other bird species and analyses of plant fossils.

Ancestral area reconstruction and diversification history of the Blue-backed Manakin. From: do Nascimento et al. (2021) Journal of Ornithology.

Taxonomy

And there you have it, the evolutionary story of the Blue-backed Manakin. Currently, this species is classified into four subspecies: napensis, regina, atlantica and pareola. However, the genetic analyses in this study uncovered five distinct lineages, not four. It seems that the subspecies atlantica and pareola are composed of more genetic groups than currently thought. A taxonomic revision might thus be warranted. And if these changes in classification are published, you can read the entire taxonomic story at the Avian Hybrids Project.

References

do Nascimento, N. F. F., Agne, C. E. Q., Batalha-Filho, H., & de Araujo, H. F. P. (2021). Population history of the Blue-backed Manakin (Chiroxiphia pareola) supports Plio-Pleistocene diversification in the Amazon and shows a recent connection with the Atlantic Forest. Journal of Ornithology, 162(2), 549-563.

Featured image: Blue-backed Manakin (Chiroxiphia pareola) © Steve Garvie | Wikimedia Commons

Unraveling the evolutionary history of the Manakins

Different methods largely converge on the same species tree.

Constructing a phylogeny from genomic data is a challenging exercise. Some researchers have proposed a concatenation approach where you combine all genes into one long sequence and analyze them as one huge gene. This straightforward strategy has the major limitation that it assumes all genes share the same evolutionary history. This is mostly not the case: different genes tend to tell different evolutionary stories. So, how can you extract the “true” phylogeny from this forest of discordant gene trees. Here, the multispecies coalescent (MSC) can be useful. This statistical framework uses a set of discordant gene trees to estimate the species tree, while taking into account their diverse evolutionary trajectories (often caused by incomplete lineage sorting). Although there has been intense debate on this method, it does seem to be a reliable way to reconstruct species trees. A good strategy is to apply multiple methods and try to understand any incongruent results that pop up. In my own research on the evolution of geese, for example, I applied both concatenation and multispecies coalescent approaches. Both methods converged on the same species tree, suggesting that it reflects the main evolutionary history of these birds. Recently, a study in the journal Molecular Phylogenetics and Evolution used a variety of methods to unravel the phylogenetic relationships of manakins (family Pipridae). Let’s see if they succeeded.

Many Methods

Rafael Leite and his colleagues sequenced two types of molecular markers for several manakin species: ultraconserved elements (UCEs) and exons. UCEs are genomic sequences that are highly conserved across vertebrates and can thus be easily sequenced across a wide range of species. Their flanking regions are more variable and can be used for phylogenetic analyses (see for example this study on honeyeaters). Exons are the expressed sections of gene sequences and can be obtained with specific target capture methods. These two types of molecular markers were subsequently analyzed with both concatenation and multispecies coalescent approaches.

The researchers used the UCE data to create two datasets: one with at least 75% of the species sampled (75% UCE) and one with at least 95% of the species sampled (95% UCE). Next, they performed the following phylogenetic analyses: concatenated analyses on three datasets (75% UCE, 95% UCE and exons) and multispecies coalescent on two datasets (75% UCE and 95% UCE). For the latter analyses, they relied on two approaches: ASTRAL (which uses the gene trees as input) and SVDquartets (which uses the sequence data as input).

Phylogenetic tree of the manakins (family Pipridae) based on Maximum Likelihood analyses of the UCE concatenated datasets. The numbers in the boxes indicate support values for the 75% UCE and 95% UCE datasets. From: Leite et al. (2021) Molecular Phylogenetics and Evolution.

Non-monophyletic Clades

I will not bother you with a detailed description of all the resulting phylogenies. The researchers noted that their results “were largely congruent across analyses, and led to a robust hypothesis about the phylogenetic relationships of manakins.” In line with previous molecular studies, the analyses pointed to an early split between the sexually monomorphic genera Neopelma and Tyranneutus (group A, subfamily Neopelminae), and the dichromatic “core” manakins (group B, subfamily Piprinae). In addition, the results suggest sub-clades B1 (Ilicura, Masius, Corapipo, Chiroxiphia and Antilophia) and B2 (Xenopipo, Chloropipo, Cryptopipo, Lepidothrix, Heterocercus, Manacus, Pipra, Machaeropterus, Pseudopipra and Ceratopipra) within the Piprinae.

Most genera turned out to be monophyletic, but there are some notable exceptions. First, several species of the genus Tyranneutus – namely the Tiny Tyrant-manakin (T. virescens) and the Dwarf Tyrant-manakin (T. stolzmanni) – are nested with the genus Neopelma. Second, the analyses indicated that two species of the genus Antilophia – the Helmeted Manakin (A. galeata) and the Araripe Manakin (A. bokermanni) – cluster within the genus Chiroxiphia. Moreover, different methods pointed to different phylogenetic relationships between the members of these genera (although Antilophia was always nested within Chiroxiphia). More work is needed here to sort out the details, but a taxonomic revision seems warranted.

Different methods resulted in different topologies for the genera Antilophia and Chiroxiphia. From: Leite et al. (2021) Molecular Phylogenetics and Evolution.

Future Work

Despite some phylogenetic conflicts between the methods and a few clades with low statistical support, this study generated a reliable backbone for the manakin phylogeny. This phylogenetic framework can now be applied to macroevolutionary questions to better understand the evolution of the unique behaviors and morphological variation of these beautiful birds.

References

Leite, R. N., Kimball, R. T., Braun, E. L., Derryberry, E. P., Hosner, P. A., Derryberry, G. E., Anciaes, M., McKay, J. S., Aleixo, A., Ribas, C. C., Brumfield, R. T. & Cracraft, J. (2021). Phylogenomics of manakins (Aves: Pipridae) using alternative locus filtering strategies based on informativeness. Molecular Phylogenetics and Evolution, 155, 107013.

Featured image: Graphical abstract from the study.

The phylogeographic story of a Manakin and a Bamboo Tyrant

Ecology explains the genetic differences in two Atlantic Forest species.

One of my favorite science stories is the discovery of the neutrino by the Austrian physicist Wolfgang Pauli. During an experiment, he found that energy appeared not to have been conserved. Reluctant to give up the universal idea of conservation of energy, Pauli developed an explanation. He speculated that the missing energy was carried off by a new particle. Next, he developed a mathematical model to predict certain properties of this new particle, so that its existence could be verified. Twenty-five years later this new particle was found and is now a well-established member of particle physics, even if still hard to detect. This story illustrates the power of formulating explanations and hypotheses which can consequently be tested with new experiments and observations.

A recent study in the journal Molecular Phylogenetics and Evolution took a similar approach when examining the genetic population structure of of two species in the Montane Atlantic Forest: the blue manakin (Chiroxiphia caudata) and the drab-breasted bamboo tyrant (Hemitriccus diops). What explanations could account for the similarities and differences in population structure between these species?

Last Glacial Maximum

Reconstructing the past distributions of these species revealed that they responded similarly to the climatic conditions during the Last Glacial Maximum (about 20,000 years ago). At this time, the Montane Atlantic Forest covered a larger area of South America, allowing both species to expand their range. This finding was also supported by the genetic analyses where several statistics (Fu’s Fs and R2) indicated population expansion in both species.

Despite these similarities, additional genetic analyses of the mitochondrial ND2 gene revealed some striking differences. The blue manakin did not display a clear phylogeographic structure, whereas the drab-breasted bamboo tyrant showed a phylogeographic break near the Doce River. What could explain these differences?

The blue manakin did not show any phylogeographic study, while the drab-breasted bamboo tyrant showed a clear phylogeographic break. From: da Silva Ribeiro et al. (2020) Molecular Phylogenetics and Evolution.

Ecological Differences

The researchers discuss several explanations for this phylogeographic incongruence. A first possibility is that there has been more gene flow between several blue manakin populations, preventing the build-up of genetic differences. This higher exchange of individuals (and genes) between populations could relate to the diet and mating system of this species. The blue manakin is a frugivore. Given that fruit is a more ephemeral resource in time and space, frugivorous species are expected to travel large distances to find food. In addition, the blue manakin exhibits lekking behavior in which females visit several locations where multiple males display (see video below). Again, lekking species are expected to disperse over larger distances during their visits. The drab-breasted bamboo tyrant, on the other hand, is a insectivore (plenty of those around) and has a territorial mating system (no need to travel far). These characteristics might lead to less gene flow between populations and the accumulation of genetic differentiation.

A second explanation concerns the different generation times of both species. Female manakins start breeding when they are 2–3 years old and have a generation time of 4.9 years. This is roughly three times larger than the average generation time of non-lekking passerine birds (ca. 1.7 years). Hence, the authors suggest that “the shorter generation time of H. diops could have favored the accumulation of differences between geographically isolated populations.”

The complex courtship ritual at a manakin lekking spot.

More Research

Similar to Pauli postulating the existence of a new particle, the formulation of all these explanations is just the first step in this scientific endeavor. Now, the researchers will need to dig deeper and test these explanations with other analytical tools and new datasets. Indeed, they mention that “the incongruent population structure pattern shown in our comparative study indicates that life history and ecological traits can be important in diversification processes. Further investigations of these traits are needed to clarify their micro-evolutionary role.” Whether you are a physicist or a biologist, further investigations are the way forward.

References

da Silva Ribeiro, T., Batalha-Filho, H., Silveira, L. F., Miyaki, C. Y., & Maldonado-Coelho, M. (2020). Life history and ecology might explain incongruent population structure in two co-distributed montane bird species of the Atlantic Forest. Molecular Phylogenetics and Evolution, 153, 106925.

Featured image: Blue Manakin (Chiroxiphia caudata) © Dave Curtis | Flickr