Chromosome rearrangement linked to less mobile quail

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BIn 2015, researchers reported sightings of strange quails in continental western Europe and northwest Africa. The birds appeared to be common quails (Coturnix coturnix), but they were larger and had darker throat feathers. They also had rounded wings, a shape associated with less efficient flight, suggesting they might not migrate as far as a common quail should. Common quails are very mobile animals that emigrate thousands of kilometers between Europe and sub-Saharan Africa during the breeding season to increase mating opportunities, but so far dark forms have mainly been seen in southern Europe.

CARLES VILA

But perhaps the strangest thing about these darker birds is that they exist at all. Usually different forms of species appear due to restricted gene flow. Phenotypic divergences could occur in geographically separated populations, for example. But with all their travel — and lay eggs As time goes on, common quails should not have any real obstacles to gene flow.

The evolutionary biologist of Estación Biológica de Doñana, Carles Vilà, took a particular interest in these strange birds and decided to deepen his research. He and his colleagues captured 80 common quails from the area where dark forms were seen during the breeding season and collected data on their physical traits and samples for genetic analysis. They found that the morphs had massive chromosome inversion, which meant that much of their DNA was turned over. In addition, isotopic analyzes of the feathers of the form found almost no difference between feathers cultivated during the breeding and wintering seasons. This would indicate that there was little change in the diet over the course of the year, which could happen if the quails did not stray too far from one location.

In animals, such inversions have already been bound negative impacts on reproduction, including reduced fertility. In this case, the inversion appears to reduce the migratory behavior of these generally highly mobile birds, likely leading to the dark-throated form’s limited geographic range, Vilà and colleagues report on November 29 in Current biology.

The scientist corresponded with Vilà via email on the process of identifying chromosomal inversions and what these data suggest about the evolution and ecology of this quail species.

The scientist: Why [common quails] chosen as target species for this research?

Carles Vilà: One of the team, JD Rodríguez-Teijeiro, had been studying the biology of quail populations for decades. He was interested in the social and reproductive behavior of this species, as well as the dynamics of its population. Although common quails are a popular game bird in southern Europe, they have a secretive way of life, mostly hidden in grain fields or meadows, and very little is known about their social behavior ( they appear to form pseudo-leks and are a very interesting species; a lek is a grouping of males that come together to participate in competitive displays which may attract visiting females who study potential mates for copulation; in quails, the number of males that can be together is relatively small). After examining thousands of quails, he commented that common quails look morphologically different in the south of the Iberian Peninsula. We were curious about this because quails migrate and move around a lot. For this reason, differentiation between populations was not expected. If present, this population structure could suggest that the displacements were not as extensive as expected, and this could be important from a conservation perspective and to understanding their social dynamics. We started the genomic study of these quails hoping to see a little differentiation in the population, but instead we found a large chromosome inversion.

ST: Why are chromosome inversions important in the study of animal evolution and ecology?

CV: Recombination is a mechanism by which genes inherited from the father and mother are rearranged, leading to new combinations of traits in the offspring. When an individual inherits a chromosome with an inversion and a chromosome without inversion from its parents, these chromosomes do not match correctly during meiosis. As a result, recombination cannot occur in this region and the genes within the inversion cannot be rearranged. As a result, these genes evolve separately in individuals with and without inversion. This implies that two lines are generated within the same population and the mutations which appear in these genes cannot be transferred from one line to another; the inversion genes begin to evolve in separate directions. The genes will accumulate mutations which may be important for adaptation and / or evolution separately in each lineage. This process could even lead to speciation without geographic isolation between the two lineages.

ST: How did you and your team detect genome inversions?

CV: When we looked at several thousand genetic markers spread throughout the genome to assess population structure, comparing populations with different pigmentation, we observed that a large region of chromosome 1 had much higher differentiation than the rest. of the genome. One possible explanation for this was that an inversion had occurred in this region. We have confirmed this by developing probes that can be detected by immunofluorescence and which would attach to the quail genome inside and outside this region. This allowed us to see that these probes were separated by different distances in individuals we assumed carried the inversion compared to individuals who did not carry the inversion, as one would expect if a fragment of the chromosome had the opposite orientation in one group versus the other, an inversion.

Vilà’s colleague José D. Rodriguez-Teijeiro holding a common quail with the inversion.

CARLES VILA

ST: What challenges have you encountered?

CV: As the common quail genome was not available, preparation of probes for immunofluorescence was not obvious and our experiments were repeatedly unsuccessful. In addition, for these experiments, we needed chromosomes obtained from testes of sexually active males from different regions, which required specific fieldwork campaigns with equipment to keep these samples at very low temperatures.

ST: The extent [of the] chromosome inversion. . . over 7,000 genes, or about 12% of the genome: did this surprise you or what did you find surprising?

CV: It is VERY surprising and exceptional. This is one of the biggest reversals ever described. In fact, it is surprising that heterozygous individuals (carrying one chromosome with the inversion and one without) can be fertile. Since it affects so many genes, one can expect very large differences between the two lines.

ST: Do you have any idea why or how genome inversion occurs in this species of quail?

CV: Our molecular dating suggests that this is a very old reversal. He was probably born over a million years ago. It could be from the same species, or it could have arrived by hybridization with another extinct species. However, we do not know for sure what could be the origin.

ST: According to the article, quails with inversions had different physical characteristics compared to quails without inversions. Could you expand on what these physical differences are?

CV: Individuals carrying the inversion are heavier, and males have darker throat pigmentation. In addition, in these birds the wings are more rounded (suggesting lower flight efficiency) and individuals accumulate less fat. The accumulation of fat is an important detail because migrating quails need to accumulate large reserves of fat before starting to migrate.

Vilà colleague and main author of the article Inés Sanchez-Donoso holding a vulgar quail with the inversion.

CARLES VILA

ST: Why are quail migratory behavior and mobility important?

CV: When winter arrives, suitable habitats [for the quail] are very rare. Most of the quail use the grain fields that are harvested; at the same time, temperatures drop across the range and resources are very limited. Then the quails migrate south of the Sahara Desert, to areas with suitable habitats. However, analysis of stable isotopes of feathers grown during winter and breeding seasons shows that quails with inversion have very reduced migratory movements or do not migrate at all. Perhaps these quail can only survive in the southern latitudes of the species’ breeding range, as winter conditions are not as extreme here as in more northern latitudes.

ST: Where do you see the future of this research?

CV: Since chromosomes with and without inversion evolve separately, it might be interesting to see if the two lines retain the same genes or if some genes show adaptation to local conditions. . . . Finally, we want to continue to compare the genomes of quails from the entire range as well as extinct quails to try to understand the origin of the inversion.

Editor’s Note: This interview has been edited for brevity.

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