Mitochondrial capture in the Chestnut Quail-thrush: Neutral or adaptive introgression?

Genetic study tries to solve this mitochondrial mystery.

Evolution is the change of populations of time. On a molecular level, evolutionary biologists quantify this change in allele frequencies (i.e. different versions of the same gene). Imagine sampling a population and measuring genetic diversity at a particular mitochondrial gene. It turns out that 20 percent of the individuals have variant A, while the remaining 80 percent carry variant B. A few years later, we return to this population and again measure genetic diversity. This time, the majority of the population (about 90 percent) have gene-variant A. This significant change is allele frequency – from 20 to 90 percent – indicates that the population evolved. But what evolutionary processes underlie these changes?

According to the Neutral Theory of Molecular Evolution, “mutations are either sufficiently deleterious in their effects on fitness that they have little chance of becoming fixed in the population, or are under such weak selection that they may become fixed as a result of genetic drift” (see Jensen et al. 2018). In our example, the increase of variant A might thus be the outcome of genetic drift. Alternatively, variant A provided an advantage for the individuals that carried it. They might have survived better and produced more offspring compared to their conspecifics with variant B. Hence, variant A was under strong natural selection and increased in frequency due to its adaptive advantage (see Kern & Hahn 2018). The importance of neutral vs. adaptive processes in molecular evolution is currently a hot topic in population genetics (the two papers mentioned here nicely summarize both sides of the debate). And this discussion can be applied to the main focus of this blog: introgressive hybridization in birds.

A Chestnut Quail-thrush in Australia © Kevin1243 | Wikimedia Commons

 

Disagreeing DNA

In a recent Ecology and Evolution paper, Kerensa McElroy and her colleagues investigated the genetic population structure of the Copperback Quail-thrush (Cinclosoma clarum) and the Chestnut Quail-thrush (C. castanotum). Two species that can be found in the arid and semi‐arid zones of southern Australia. The genetic analyses clearly separated both species and revealed a striking discordance between nuclear and mitochondrial DNA within the Copperback Quail-thrush. This species can be divided into two populations (referred to as East and West in the study). But the nuclear and mitochondrial DNA do not agree on the assignment of individuals to these populations (clearly visible in the figure below). What is going on here?

Discordance between mitochondrial and nuclear DNA is a relatively common phenomenon and can be the result of several processes (reviewed by Toews & Brelsford 2012). The researchers think that the Quail-thrush case can be explained by introgression of mtDNA. Phenotypic data and the nuclear DNA in this study suggests that there is a hybrid zone between the populations where the mitochondrial genome of the western population is being replaced by the eastern (so gene flow from the eastern into the western population).

Genetic analyses show a clear separation between Chestnut Quail‐thrush (purple) and Copperback Quail‐thrush (blue and green). Nuclear and mitochondrial DNA disagree about the population assignment within the Chestnut Quail‐thrush. From McElroy et al. (2020) Ecology and Evolution

 

Mitochondrial Capture

Which brings us to the topic at the start of this blog post: Is this mitochondrial capture neutral or adaptive? This question is currently difficult to answer because the mitochondrial capture is ongoing (not all individuals have the same color in the figure above). However, the researchers argue that the process is probably neutral, based on a demographic model of population invasion. First, the expanding species is outnumbered and is thus more likely to hybridize with members from the local population. As the expansion proceeds, the resident species and previously produced hybrids are engulfed by the expanding species, thereby overturning the numerical imbalance. Consequently, hybrids have a higher chance of backcrossing into members of the expanding species, resulting in gene flow from the resident into the expanding species. In the Quail-thrush case, the western population expanded and genes should thus flow from the resident eastern into the invading western population. And that is exactly what we observe.

Of course, we cannot completely rule out the adaptive explanation. Perhaps the eastern mtDNA does fare better in southern Australia, but this will require more detailed genomic analyses and perhaps some experimental lab work. For example, David Toews and his colleagues measured mitochondrial respiration in flight muscles of Yellow-rumped Warblers (Setophaga coronata) to determine which variant was best suited for long-distance migration. There is still much to learn about the “powerhouses of the cell”.

 

References

McElroy, K., Black, A., Dolman, G., Horton, P., Pedler, L., Campbell, C. D., Drew, A. & Joseph, L. (2020) Robbery in progress: Historical museum collections bring to light a mitochondrial capture within a bird species widespread across southern Australia, the Copperback Quail‐thrush Cinclosoma clarum. Ecology and Evolution, 10(13): 6785-6793.

Featured image: A Chestnut Quail-thrush © Peter Jacobs | Wikimedia Commons

 

This paper was added to the Cinclosomatidae page.

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