Pool-GWAS on reproductive dormancy in Drosophila simulans suggests a polygenic architecture

Abstract

The genetic basis of adaptation to different environments has been of long-standing interest to evolutionary biologists. Dormancy is a well-studied adaptation to facilitate overwintering. In Drosophila melanogaster, a moderate number of genes with large effects have been described, which suggests a simple genetic basis of dormancy. On the other hand, genome-wide scans for dormancy suggest a polygenic architecture in insects. In D. melanogaster, the analysis of the genetic architecture of dormancy is complicated by the presence of cosmopolitan inversions. Here, we performed a genome-wide scan to characterize the genetic basis of this ecologically extremely important trait in the sibling species of D. melanogaster, D. simulans that lacks cosmopolitan inversions. We performed Pool-GWAS in a South African D. simulans population for dormancy incidence at 2 temperature regimes (10 and 12°C, LD 10:14). We identified several genes with SNPs that showed a significant association with dormancy (P-value < 1e-13), but the overall modest response suggests that dormancy is a polygenic trait with many loci of small effect. Our results shed light on controversies on reproductive dormancy in Drosophila and have important implications for the characterization of the genetic basis of this trait.

Keywords: Drosophila; adaptation; dormancy; genetic architecture.

Fig. 1.

Experimental design for the dormancy Pool-GWAS. Isofemale strains that are nondormant at 10°C (thus nondormant at both temperatures since dormancy incidence decreases from 10 to 12°C) are referred to as the “Non-Dormant Group.” Isofemale strains that are dormant at 12°C (thus dormant at both temperatures since dormancy incidence increases from 12 to 10°C) constitute the “Dormant Group.” The black diagonal line represents the expected change in dormancy incidence between the 2 temperature regimes.

Fig. 2.

Dormancy expression at 2 temperature regimes (10 and 12°C, LD 10:14) of the South African D. simulans population (562 strains). The dormancy levels between the 2 temperatures were compared with the Wilcoxon signed-rank test. The decrease in dormancy from 12 to 10°C demonstrates the plastic character of the trait.

Fig. 3.

PC analysis of the dormancy levels of 562 D. simulans isofemale strains from South Africa at 2 temperature regimes (10 and 12°C, LD 10:14). Two out of 3 vertices of the triangular-shaped position of the strains harbor the most extreme nondormant and dormant strains. The third vertex includes the strains that showed the greatest difference in dormancy incidence between the 2 temperature regimes. Please note that some isofemale strains had identical levels of dormancy, thus they are superimposed in the figure.

Fig. 4.

Manhattan plot of the adjusted chi-squared test P-values from the Pool-GWAS for dormancy. The dashed line indicates the significance threshold of 10⁻¹³. Genes that are discussed in the main text are highlighted in red.