Genetic Background and Signatures of Selection Assessment in Wild African Harlequin and Domestic Japanese Quails Using a Genomic and Transcriptomic Approach

Abstract

Quails are increasingly becoming a vital complementary protein source, contributing to food security. In Kenya, the indiscriminate and destructive harvesting of wild African harlequin quails using traditional methods has been ongoing for generations. Yet, their genetic diversity and evolutionary history are largely unknown, thus posing a threat to extinction and genetic diversity. In this study, the genetic variation and demographic history of captured wild African harlequin quails (n = 78) were determined using mitochondrial DNA (mtDNA) and genotyping by sequencing (GBS) data. Selection signatures were also examined using composite likelihood ratio (CLR) and integrated haplotype score (iHS) tests in comparison to domestic Japanese quails (n = 22). Domestic Japanese quail transcriptome data (n = 6) was also examined. The genetic variation in wild African harlequin quails was predominantly among individuals rather than populations. Demographic analyses indicated a signal of rapid expansion. The estimated time since population expansion was 150 to 350 thousand years ago (kya), corresponding to around the Pliocene–Pleistocene boundary. A gradual decline in their effective population size was also observed, which raised concerns about their conservation status. 352 and 424 candidate genes were detected in the wild African harlequin quail and domestic Japanese quail through the CLR test, respectively, whereas 150 and 457 candidate genes were identified through iHS analysis. Candidate genes under positive selection identified in the wild African harlequin quail were associated with important traits such as immune response (MAPK13, CREB1, ITGB3, and PPP1CA) and morphological traits (WNT5A, GRIA1, and ALK), whereas, in domestic Japanese quail, production-related genes such as VIPR2, DYNLL2, PRF1, COL11A1, and GNA12 were identified. RNA-Seq analysis revealed differentially expressed genes associated with production processes such as spermatogenesis and muscle structure development. This is the first study on the wild African harlequin quails to provide information useful in biodiversity conservation and proper utilization of its genetic resources.