Genetic mismatches in the Long-tailed Finch

Exploring the interactions between mitochondria, sex chromosomes and beak color.

Hybrids are often sterile or unviable. These developmental issues can mostly be traced back to genetic incompatibilities: mismatches between certain genetic variants. During the 1930 and 1940s, Theodosius Dobzhansky and Herman Muller developed a theoretical model to explain the evolution of these incompatibilities. Here is the short version:

Consider two allopatric populations diverging independently, with the same ancestral genotype AABB in both populations. In one population, a mutation (A -> a) appears and goes to fixation, resulting in aaBB, which is fertile and viable. In the other population, another mutation (B -> b) appears and goes to fixation, resulting in AAbb, which is also fertile and viable. When these populations meet and interbreed, this will result in the genotype AaBb. Alleles a and b have never “met” each other and it is possible that allele a has a deleterious effect that becomes apparent when allele b is present, or vice versa. Over evolutionary time, numerous of these incompatibilities may arise, each possibly contributing to hybrid sterility or unviability.

These genetic incompatibilities can arise between countless interacting genes, but one specific situation concerns mitonuclear genes. The mitochondria – also known as the powerhouses of the cell – only contain 13 protein-coding genes. However, this small collection of genes interacts with thousands of genes in the nuclear genome. The rapid evolution of mitochondrial DNA requires compensatory changes in the nuclear genes to ensure proper functioning. The resulting high rate of molecular evolution in mitonuclear genes increases the likelihood of genetic incompatibilities as closely related species adapt to different environments. Moreover, a mismatch in the mitonuclear machinery can have devastating consequences for the energy balance – and thus livelihood – of hybrid individuals.

A graphical representation of the Dobzhansky-Muller model of genetic incompatibilities. From: Wikipedia.

Sex Chromosomes and Colors

Another place to look for genetic incompatibilities are sex chromosomes, which often play an important role in speciation (see for example this study in Barn Swallows). Numerous studies have reported how sex-linked genes contribute to hybrid dysfunction. And the situation becomes even more complicated – and interesting – when we consider the interaction between sex-linked and mitonuclear genes. A genomic survey of the Zebra Finch found that about 5% of the mitonuclear genes can be found on the Z-chromosome. Plenty of opportunities for the evolution of genetic incompatibilities there.

A final twist to this incompatibility story concerns coloration. Experiments with House Finches (Haemorhous mexicanus) uncovered a relationship between mitochondrial function and the synthesis of carotenoids (i.e. the pigments producing yellow, orange and red colors). Hybrids with mitonuclear issues will have less efficient mitochondria, which could impact the production of these pigments. The lack of red colors in male hybrids could make them less attractive to females, resulting in selection against hybrids.

Cline Analyses

In summary, it seems likely to find genetic incompatibilities in mitochondrial and sex-linked genes, possibly related to the production of reddish colors. In a recent Evolution paper, Kelsie Lopez and her colleagues tested this idea in the Long-tailed Finch (Poephila acuticauda). This Australian passerine is comprised of two subspecies with different beak colors – yellow in acuticauda and red in hecki – that interbreed along a hybrid zone. By following the distribution of genetic variants across this hybrid zone, the researchers hoped to gain more insights into potential genetic incompatibilities. Here, they relied on cline theory. I recently covered this mathematical framework in a short paper, so let me provide you with the basics:

Imagine a white and a black bird species that produce gray offspring in a hybrid zone. Tracking their plumage color along a geographical transect will reveal a clinal transition from white, to gray, to black birds. The shape of the cline provides information on the strength of selection against hybrids. If the gray hybrids interbreed with each other and the parental species, there will be a variety of differently colored backcrosses. This will result in a smooth transition from white through different shades of gray to black: a wide cline. However, if the hybrids do not reproduce, there will be similarly colored gray birds in the narrow contact zone, resulting in a rapid transition from white to black plumage: a steep cline.

In the context of the Long-tailed Finch, we would expect steep clines for genetic variants that contribute to hybrid dysfunction. Moreover, interacting genetic incompatibilities will show congruent clines.

The shape of different clines within a hypothetical hybrid zone between a black and a white bird species. The steep red cline suggests strong selection against hybrids. From: Ottenburghs (2022).

Good and Bad news

So, what did the researchers find? Let me start with the bad news: there was no relationship between mitochondrial variants and the color of the beak. The cline centers of mtDNA and bill color were almost 400 kilometers apart. It thus seems that mitochondrial function does not influence the synthesis of carotenoids in the beaks of these birds. Most sex-linked genes also showed different clines compared to the mtDNA, except for three variants. Hence, the researchers suggested that these variants might represent sex-linked mitonuclear incompatibilities. However, more research is needed to confirm this association and provide a mechanistic basis. As we all know, correlation is not causation.

It took me a long time to build up to these results, from the basic Dobzhansky-Muller model over mitonuclear interactions to cline analyses. But I hope this step-by-step explanation will help you to understand the situation in Long-tailed Finches. This study nicely illustrates how messy nature is compared to the clean theoretical models that scientists develop. It is always more complicated, especially when it comes to genetic incompatibilities.

Geographic clines of the mitochondrial DNA (in red) and several sex-linked genes showed congruent patterns with three sex-linked variants (in blue). These patterns suggests possible genetic incompatibilities. From: Lopez et al. (2021).

References

Hill, G. E., Hood, W. R., Ge, Z., Grinter, R., Greening, C., Johnson, J. D., … & Zhang, Y. (2019). Plumage redness signals mitochondrial function in the house finch. Proceedings of the Royal Society B, 286(1911), 20191354.

Lopez, K. A., McDiarmid, C. S., Griffith, S. C., Lovette, I. J., & Hooper, D. M. (2021). Evaluating evidence of mitonuclear incompatibilities with the sex chromosomes in an avian hybrid zone. Evolution, 75(6), 1395-1414.

Ottenburghs, J. (2022). Digest: Following clines along an Amazonian hybrid zone. Evolution. 76(3): 677-678.

Featured image: Long-tailed Finch (Poephila acuticauda) © Lip Kee Yap | Wikimedia Commons

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