Back in 2015, researchers reported observations of strange quail in western mainland Europe and northwest Africa. The birds appeared to be common quail (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 may not migrate as far as a common quail should. Common quail are highly mobile animals that migrate thousands of kilometers between Europe and sub-Saharan Africa during the breeding season to increase mating opportunities, but so far, dark morphs have primarily been observed in Southern Europe.
But perhaps the strangest thing about these darker birds is that they exist at all. Usually, different morphs of species arise due to restricted gene flow. Phenotypic divergences might crop up in populations separated geographically, for instance. But with all their moving about—and laying eggs as they go—common quail shouldn’t have...
Estación Biológica de Doñana evolutionary biologist Carles Vilà took a particular interest in these odd birds and decided to investigate further. He and his colleagues captured 80 common quail from the region where dark morphs have been seen during the breeding season and collected data on their physical traits and samples for genetic analyses. They discovered that the morphs had a massive chromosomal inversion, meaning a large chunk of their DNA was flipped around. Furthermore, isotope analyses of the morph’s feathers found almost no difference between feathers grown during breeding and wintering seasons. That would indicate there was little change in diet over the year, which could happen if the quail didn’t stray too far from one place.
In animals, such inversions have previously been linked to negative impacts on reproduction, including reduced fertility. In this case, the inversion seems to be reducing the migratory behavior in these typically very mobile birds, likely leading to the dark-throated morph’s geographically limited range, Vilà and colleagues report November 29 in Current Biology.
The Scientist corresponded with Vilà by email about the process of identifying chromosomal inversions and what this data suggests about the evolution and ecology of this quail species.
The Scientist: Why were [common quail] chosen as the target species for this research?
Carles Vilà: One of the team members, JD Rodríguez-Teijeiro, had been studying the population biology of quails for decades. His interest was in the social and reproductive behavior of this species, as well as its population dynamics. Although common quails are a popular game bird in southern Europe, they have a secretive way of live, hidden mainly in cereal fields or grasslands, and very little is known about their social behavior (They seem to form pseudo-leks and are a very interesting species; a lek is an aggregation of males that gather to engage in competitive displays that may entice visiting females who are surveying prospective partners for copulation; in quails the number of males that can be together is relatively small). After looking at thousands of quails he commented that common quails seemed morphologically different in the south of the Iberian Peninsula. We were curious about this because quails migrate and move a lot. Because of this, differentiation between populations was not expected. If present, this population structure could suggest that the movements were not as extensive as anticipated, and this could be important from the conservation point of view and to understand their social dynamics. We started the genomic study of these quails expecting to see a small population differentiation, but instead we found a large chromosomal inversion.
TS: Why are chromosomal inversions important in studying animal evolution and ecology?
CV: Recombination is a mechanism by which the genes inherited from the father and from the mother are reshuffled, leading to the new combinations of traits in the offspring. When one individual inherits one chromosome with an inversion and one chromosome without the inversion from its parents, these chromosomes do not match properly during meiosis. As a result, recombination cannot occur in this region and the genes within the inversion cannot be reshuffled. As a result, these genes evolve separately in individuals with and without the inversion. This implies that two lineages are generated within the same population and mutations that appear in these genes cannot be transferred from one lineage to the other; the genes in the inversion start to evolve in separate directions. Genes will accumulate mutations that may be important for adaptation and/or evolution separately in each lineage. This process could even result in speciation without geographic isolation between the two lineages.
TS: How did you and your team detect inversions in the genome?
CV: When we screened several thousand genetic markers distributed across the genome to assess the population structure, comparing populations with different pigmentation, we observed that a large region within chromosome 1 had very much higher differentiation than the rest of the genome. One possible explanation for this was that an inversion had taken place in this region. We confirmed this by developing probes that would be detectable by immunofluorescence and that would attach to the quail genome within and outside this region. This allowed us to see that those probes were separated by different distances in the individuals that we hypothesized that were carrying the inversion compared to the individuals that were not carrying the inversion, as was expected if a fragment of the chromosome had the opposite orientation in one group compared to the other, an inversion.
TS: What challenges did you encounter?
CV: Since the common quail genome was not available, the preparation of probes for immunofluorescence was not obvious and our experiments failed many times. Also, for these experiments we needed chromosomes obtained from testes from sexually active males from the different regions, and this required specific field work campaigns with equipment to preserve these samples at very low temperatures.
TS: The extent [of the] chromosomal inversion . . . over 7,000 genes, or about 12 percent of the genome: Did this surprise you, or what did you find surprising?
CV: This is VERY surprising and exceptional. This is one of the largest inversions ever described. In fact, it is surprising that heterozygote individuals (that carry one chromosome with the inversion and another one without) could be fertile. Since it affects so many genes, we can expect very large differences between the two lineages.
TS: Do you have any ideas of why or how genome inversion occurs in this species of quail?
CV: Our molecular dating suggests that this is a very old inversion. It probably originated more than one million years ago. It could have originated within the same species, or it could have arrived through hybridization with another extinct species. However, we do not know for certain what could have been the origin.
TS: According to the paper, quail with the inversions had different physical characteristics when compared to quail without the inversions. Could you expand on what these physical differences are?
CV: Individuals carrying the inversion are heavier and males have a darker throat pigmentation. Also, in these birds, wings are more rounded (what suggests lower flight efficiency) and individuals accumulate less fat. The accumulation of fat is an important detail because migratory quails need to accumulate important fat reserves before starting migration.
TS: Why is the migratory behavior and mobility of quails important?
CV: As winter arrives, suitable habitats [for the quail] are very scarce. Most of the quails use cereal fields that are harvested; at the same time, temperatures drop over the entire range and resources are very limited. Then, quails migrate south of the Sahara desert, to areas with suitable habitats. However, the analysis of stable isotopes from feathers grown during the winter and the breeding seasons show that quails with the inversion have very reduced migratory movements or do not migrate at all. Perhaps these quails are only able to survive in southern latitudes within the species breeding range because winter conditions here are not as extreme as in more northern latitudes.
TS: Where do you see the future of this research going?
CV: Since chromosomes with and without the inversion evolve separately, it could be interesting to see if the two lineages maintain the same genes or if some genes show adaptation to local conditions. . . . Finally, we want to continue comparing genomes of quails from across the 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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