A mitochondrial mystery involving two Monarch Flycatchers

Why are there two mitochondrial haplotypes in the Spectacled Monarch?

When researchers took a closer look at the mitochondrial DNA of the Spectacled Monarch (Symposiachrus trivirgatus), they were in for a surprise. This species contained two distinct haplotypes that were not even closely related. One of these haplotypes clustered with a non-sister species: the Spot-winged Monarch (S. guttala). What is going on here? A recent study in the journal Molecular Ecology tried to solve this mitochondrial mystery by testing several hypotheses:

  1. Cryptic speciation: the Spectacled Monarch is actually comprised of two species.
  2. Neutral gene flow: the mtDNA introgressed from the Spot-winged into the Spectacled Monarch by neutral processes (e.g., genetic drift).
  3. Adaptive introgression: the mitochondrial variant confers an adaptive advantage to the Spectacled Monarch.

To discriminate between these explanations, Michael Andersen and his colleagues sampled birds across the range of both species (i.e. Australia and New Guinea) and analyzed thousands of genetic markers. Let’s see if they could figure out what happened with these Monarch Flycatchers…

Cryptic Species?

First, the cryptic speciation hypothesis: could it be that the Spectacled Monarch is not one, but two species? If so, we would expect to find similar patterns of genetic divergence in the nuclear genome. This was, however, not the case. Genetic analyses of the nuclear markers clearly separated the Spot-winged and the Spectacled Monarch into two distinct groups. No sign of hidden species in nuclear genome of the Spectacled Monarch. Hence, we can already cross out cryptic speciation from our list.

The presence of mtDNA from the Spot-winged Monarch in some Spectacled Monarch individuals clearly suggests that introgression occurred. And indeed, demographic analyses pointed to ancient introgression events. The exact timing of these events was more difficult to determine, because these species probably established secondary contact multiple times when lower sea levels allowed exchange between Australia and New Guinea. But the main question is: was the introgression of mtDNA adaptive or not?

The mitochondrial phylogeny (figure b) reveals two distinct haplotypes in the Spectacled Monarch (blue and orange groups). These birds cluster together in the nuclear phylogeny (figure a), rejecting the hypothesis of cryptic speciation. From: Andersen et al. (2021) Molecular Ecology.

Positive Selection

To examine the possibility of adaptive introgression, the researchers performed several tests of selection on the genetic data (including the McDonald-Kreitman test). These analyses provided “little to no evidence for positive selection acting on the mitochondria since the capture event.” These results are thus consistent with neutral processes. It seems that genetic drift alone might be sufficient to explain the mitochondrial mystery in these birds. Genetic drift is especially prevalent in small populations. It is easy to imagine that the population size of the Spectacled Monarch diminished when sea levels rose and these birds became isolated again. However, more detailed demographic analyses are needed to test this scenario.

Finally, there is one explanation that the researchers did not explicitly consider: ghost introgression (as was probably the case in other species, such as Phylloscopus warblers and the Red-billed Chough, Pyrrhocorax pyrrhocorax). Perhaps the mtDNA did not introgress from the Spot-winged Monarch, but rather from an extinct species. Although this scenario does not provide an answer to the neutral vs. adaptive debate, it raises an interesting hypothesis that remains to be explored (see my review for possible analyses). As if the situation was not complicated enough.

References

Andersen, M. J., McCullough, J. M., Gyllenhaal, E. F., Mapel, X. M., Haryoko, T., Jønsson, K. A., & Joseph, L. (2021). Complex histories of gene flow and a mitochondrial capture event in a nonsister pair of birds. Molecular Ecology30(9), 2087-2103.

Featured image: Spectacled Monarch (Symposiachrus trivirgatus) © J.J. Harrison | Wikimedia Commons