Chromosomal Inversion Associated With Diet Differences in Common Quails Sharing Wintering Grounds

Abstract

Chromosomal inversions can contribute to genetic differentiation and ecological adaptation. In common quails (Coturnix coturnix), a large chromosomal inversion encompassing over 1200 genes is associated with key phenotypic traits, including increased body size, darker throat pigmentation, and reduced flight efficiency, which may influence migratory behavior. We hypothesized that the presence of resident common quails in the south of the Iberian Peninsula is the consequence of the high frequency of this chromosomal inversion, found in a high proportion of the breeding individuals in the region. We surveyed one wintering population in southern Spain and analyzed the genomic composition, morphology, and deuterium, nitrogen, and carbon stable isotope composition of primary feathers. Our results revealed the coexistence of birds with different karyotypes and morphologies that also differed in migratory behavior, as inferred from the comparison of the stable isotope signature in feathers. While quails with the inversion showed limited evidence of migratory movements, quails without the inversion seemed to have reached the area from other latitudes. Interestingly, our results also revealed that these migratory quails that reached this population in winter had differences in their diet. Thus, two separately evolving chromosomal lineages, characterized by the presence/absence of the inversion, coexist in the wintering area, leading to differences in morphology, behavior, and resource use. Due to the lack of recombination in the inversion, the divergence is expected to continue increasing.

Keywords: chromosomal inversion; diet; genotyping by sequencing; migration; stable isotopes.

FIGURE 1

Study area, habitat, and principal component analysis (PCA) of genetic variation in common quails. (A) Location of the study area within the Iberian Peninsula. Colored areas correspond to breeding (orange), resident (green) and wintering areas (purple) for the common quail, according to BirdLife International (2018). Breeding grounds extend to the north reaching Scandinavia and most of the wintering grounds are located in the Sahel, south of the Sahara desert. The study site is within the range where resident quails are expected and it is crossed by migratory quails. (B) Male common quails captured in the same location with (individual with the dark throat) and without the inversion; grasslands in the study area. (C) PCA using the complete set of SNPs (25,416). In red, Japanese quail samples; green, game farm admixed quails (common × Japanese quail); black, wintering quails captured for this study. Yellow, pink and blue mark reference individuals genotyped in a previous study (Sanchez‐Donoso et al. 2022), carrying different inversion karyotypes (inversion haplotype: B; karyotypes: AA, AB and BB) (D) PCA using 3705 SNPs located within the inversion in chromosome 1 and classifying individuals based on their karyotype. (E) PCA using the entire SNP dataset after excluding those in the inverted region and removing one individual identified as first order relative of another one.

FIGURE 2

Stable isotopes in two primary feathers from 32 quails captured during winter in one location in southern Spain. One of the feathers was grown during the breeding season when the individual was born (b), the other one was grown during the wintering season when it was captured and sampled (w). Panels (A–C) represent the isotopic values for deuterium (δ²H), carbon (δ¹³C) and nitrogen (δ¹⁵N) for the three karyotypes (AA, AB, BB). Braces mark significant differences (Appendix A; ***p < 0.001; *p < 0.05). Panel (D) represents carbon (δ¹³C) versus deuterium (δ²H), linking the feather grown during the breeding season (squares) with the one grown during the wintering season (circles) from the same individual. Wintering feathers of AA quails show similar δ²H values to those for AB and BB quails (which suggests that they were formed at similar latitudes) but different δ¹³C values. That suggests AA quails have a different diet during the wintering season while they remain at similar latitudes than the rest of the quails.

FIGURE 3

Phenotypic variation by karyotype. PCA of phenotypic data for common quails, colored according to karyotype group (AA: Yellow, AB: Pink and BB: Blue). Arrows point in the direction of the variables and are colored to reflect statistically significant differences between karyotypes: Orange represents variables significantly different across all three karyotypes (AA, AB, and BB); green indicates variables where AA differs significantly from AB and BB; and purple indicates variables with significant differences only between AA and BB.