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

Are the Blue-faced and the Papuan Parrotfinch different species or not?

These birds are morphologically distinct, but have similar mitochondrial DNA.

Last year, I covered a study on the phylogeny of the estrildid finches (family Estrildidae). The original paper included samples of the Blue-faced Parrotfinch (Erythrura trichroa) and the Papuan Parrotfinch (Erythrura papuana). The authors – Urban Olsson and Per Alström – noticed that these two samples shared the same mitochondrial haplotype. They briefly commented that this result could be due to misidentified specimens and did not pay further attention to these samples. There might, however, be an interesting biological explanation for the identical haplotypes of these samples. Hence, a recent study in the Bulletin of the British Ornithologists’ Club took a closer look at these Parrotfinches.

Bill Morphology

Initially, the Papuan Parrotfinch was described as a subspecies of the Blue-faced Parrotfinch by Rotschild and Hartert. Later on, Hartert elevated the Papuan Parrotfinch to species level, based on differences in bill morphology. He drew parallels with the Darwin’s Finches by writing that “We have thus a similar case as in the genus Geospiza on the Galapagos Islands, a large and a small form occurring together.” Indeed, the bill of the Papuan Parrotfinch is significantly larger than that of its Blue-faced relative. However, a difference in morphology does not necessarily mean that we are dealing with distinct species. For example, in the African genus Pyrenestes, you can observe three distinct phenotypes in a genetically uniform population. The differences in morphology are due to adaptation to different resources. Could the same process be at work in the Parrotfinches?

The difference in bill morphology between the Papuan Parrotfinch (left) and the Blue-faced Parrotfinch (right). From: DeCicco et al. (2020) Bulletin of the British Ornithologists’ Club.

Three Scenarios

To solve this mystery, Lucas DeCicco and his colleagues sequenced the mitochondrial gene ND2 and compared the morphology of several specimens. They found that the Papuan Parrotfinch and the Blue-faced Parrotfinch were almost identical in the sequence of ND2, whereas they showed no overlap in several morphological measurements. This finding can be explained in several ways, nicely summarized in the discussion section:

(1) morphological differences arose in allopatry with either limited genetic divergence or gene flow upon secondary sympatry, (2) sympatric or ecological speciation is occurring with strong selection on different phenotypes, or (3) these two phenotypes represent a single panmictic population with a phenotypic polymorphism.

At the moment, we cannot draw a definitive conclusion yet. More genetic data – nuclear genes or genomic data – is needed to discriminate between these three scenarios. This study does provide the first step in unraveling the evolutionary history of these birds, showing that the result of Urban Olsson and Per Alström was not due to a misidentification. Instead, the sharing of mitochondrial haplotypes has a biological explanation. Which one remains to be determined. This how science works, slowly collecting pieces of the puzzle until we can see the bigger picture.

The two species clearly differed in several morphological measurements. From: DeCicco et al. (2020) Bulletin of the British Ornithologists’ Club.

References

DeCicco, L. H., Benz, B. W., DeRaad, D. A., Hime, P. M., & Moyle, R. G. (2020). New Guinea Erythrura parrotfinches: one species or two?. Bulletin of the British Ornithologists’ Club, 140(3), 351-358.

Featured image: Blue-faced Parrotfinch (Erythrura trichroa) © Nrg800 | Wikimedia Commons

Hybrids between Zebra Finch subspecies provide evidence for a weak meiotic driver

Subtle deviations from Mendelian expectations point to a meiotic driver in the Timor subspecies.

Every biology student has worked his or her way through the pea-experiments of Gregor Mendel, creating Punnett squares with recessive and dominant alleles. One of the most important insights from these pivotal experiments was the observation that every allele at a genetic locus has an equal probability of being transmitted to the next generation (ultimately giving rise to the predictable ratios of dominant and recessive traits). However, some alleles show clear deviations from these expected patterns. These genetic elements are known as meiotic drivers, because they “drive” the meiotic cell division process in such as way that they have a higher chance of ending up in the gametes (i.e. eggs or sperm cells).

During meiosis, the chromosomes are sorted into four daughter cells. In birds, one daughter cell develops into the mature egg, while the other three develop into polar bodies. The spindle apparatus attaches to the centromeres of the chromosomes and drags them into the different daughter cells. Meiotic drivers are often found close to centromeres, because this allows them to influence the spindle fibers and ensure that they end up in the daughter cell that becomes the mature egg. Indeed, previous research in chickens reported a meiotic driver at the centromere of chromosome 1.

An schematic representation of the meiotic process. Meiotic drivers influence the sorting of chromosomes so that they are transmitted to the next generation. From: Wikipedia.

Subspecies

Meiotic drivers can be difficult to detect, because they tend to be transient phenomena. In some cases, the meiotic drivers lead to deleterious effects and are quickly suppressed by other genetic elements that restore proper Mendelian segregation. Alternatively, meiotic drivers are so successful that they rapidly spread through a population and become fixed (i.e. all individuals have the same genetic variant). One way to identify such cryptic meiotic drivers is to cross individuals from divergent populations. If a meiotic driver evolved in one population but not the other, it will become visible in the hybrids. A recent study in the journal Ecology and Evolution used this approach to look for meiotic drivers in the Zebra Finch (Taeniopygia guttata). The researchers crossed two subspecies – Australian (castanotis) and Timor (guttata) Zebra Finches – and traced the genetic ancestry of several molecular markers. Did some deviate from the expected Mendelian patterns?

An overview of the extensive breeding scheme in this study. From: Knief et al. (2020) Ecology and Evolution.

Backcrosses

The experiments revealed “no clear evidence for any active meiotic driver in a cross between Australian and Timor Zebra Finches.” However, there was a significant deviation from Mendelian segregation in females of the first backcrossed generation. This finding suggests that there might be a weak meiotic driver which allows Timor centromeres to outcompete Australian variants in the race for the oocyte. It took numerous hybridization and backcrossing events to detect this subtle signal, indicating that weak meiotic drivers might be more common than we think. Another example of how avian hybrids can lead to exciting discoveries and new insights.

Segregation patterns in different hybrids and backcrosses between Australian an Timor Zebra Finches. Notice the slight deviation from the expected pattern (dotted line) in the female backcrosses (BC1). From: Knief et al. (2020) Ecology and Evolution.

References

Knief, U., Forstmeier, W., Pei, Y., Wolf, J., & Kempenaers, B. (2020). A test for meiotic drive in hybrids between Australian and Timor zebra finches. Ecology and evolution, 10(23), 13464-13475.

Featured image: Zebra Finch (Taeniopygia guttata) © Peripitus | Wikimedia Commons