Introduction

Understanding how organisms adapt to complex environments is a core task of biological research. Drosophila melanogaster and Drosophila simulans are sister species, both originating from Africa and recently spreading worldwide. They serve as ideal models for studying the genetic and evolutionary mechanisms of environmental adaptation.

This project aims to elucidate the molecular mechanisms and evolutionary patterns of environmental adaptation in Drosophila natural populations through comparative population genomics. The research mainly includes: analyzing the genetic architecture of Drosophila adaptation to complex natural environments (e.g., starvation, temperature, insecticides, and other common environmental stressors) and performing functional verification; reconstructing the global migration and evolutionary history of D. melanogaster and D. simulans to reveal the association between evolutionary history and environmental adaptation; and clarifying the common laws and species-specific mechanisms of environmental adaptation in these two species.

Evolutionary History and Environmental Adaptation Mechanisms of Drosophila

The genetic mechanism of environmental adaptation is a crucial issue in evolutionary biology, but many unsolved problems remain regarding molecular mechanisms and genetic laws in natural populations. Drosophila melanogaster is an important model organism, originating from tropical Africa and recently spreading to various parts of the world, providing excellent material for systematically studying the genetic mechanisms of adaptation. However, previous studies have mostly focused on European, North American, and African populations, with a lack of understanding of Drosophila in Asian regions. The evolutionary history of natural populations on a global scale and the genetic mechanisms of adapting to different environments remain unclear. This project obtained genomes of D. melanogaster and D. simulans from various locations in China through field sampling and sequencing. Using population genomics analysis, we systematically revealed the population genetic structure, gene flow between populations, divergence history, and natural selection signals. We also combined population cage experiments to verify the relationship between positive selection signals in natural populations and environmental selection pressures.

Migration and Diffusion History of D. melanogaster

Sexual Conflict in Starvation Resistance Genes of D. melanogaster

Although males and females share most of the genome, significant differences exist in physiological structure, hormonal environment, reproductive strategies, and more. The same genetic variation may produce different fitness effects on the two sexes, such as affecting only one sex (sex-specific), affecting one sex more strongly (sex-biased), or even being beneficial to one sex while harmful to the other (sexual conflict). In addition to genetic factors, environmental changes may also have differential impacts on the fitness of both sexes. This project conducted unified phenotypic screening and pool-seq on D. melanogaster strains collected from different locations in China using population cages, focusing on starvation tolerance—a phenotype closely related to environmental adaptation. The study systematically identified genetic variations associated with starvation tolerance, revealing the roles of regulatory regions and protein sequence changes in the genetic architecture of starvation tolerance. Combined with RNA interference and CRISPR/Cas9 for functional verification of candidate genes, we found that about 74% of candidate genes showed sex-dependent phenotypic effects, among which 12 genes exhibited sexually conflicting phenotypic effects. These results provide new perspectives for understanding the genotype-phenotype association of fitness-related traits, as well as the roles of genetic background, sex differences, and pleiotropy in trait evolution.

Phenotypic Effects of Candidate Genes Verified by RNA Interference

High-Quality Drosophila Genome Assembly

This project performed high-depth sequencing on male individuals of the Drosophila simulans w501 strain. Combining PacBio HiFi, ONT, Hi-C, and other sequencing results, a high-quality genome of D. simulans was assembled. The total genome length is 156.08 Mb, consisting of 28 scaffolds, with a scaffold N50 of 53.73 Mb. The D. simulans genome contains 4 main scaffolds corresponding to the 4 main chromosomes. Specifically, the lengths of chromosome 2 (chr2), chromosome 3 (chr3), and chromosome 4 (chr4) are 53.73 Mb, 59.32 Mb, and 1.16 Mb, respectively, while the X chromosome (chrX) is 23.74 Mb. In addition, the genome includes a circular mitochondrial genome (chrM) of 18,473 bp and 23 unplaced contigs. Among them, there are 13 Y-linked contigs with a total length of 12.64 Mb. Repetitive sequences account for 31.54% (49.22 Mb) of the genome, mostly located in telomeric and centromeric regions.

Drosophila simulans Genome Assembly

Adaptive Convergence in Closely Related Species

Whether biological evolution is repeatable is a core question in biology. Natural selection, as a key driving force of evolution, plays a vital role in the process of organisms adapting to the environment. Adaptive convergent evolution mediated by natural selection is an effective way to explore the repeatability of evolution. This project took closely related species D. melanogaster and D. simulans as research objects. Based on their similarities in biological characteristics, phylogenetic relationship, global distribution patterns, and migration history, we conducted a large-scale comparative genomics study of global natural populations to reveal the genetic architecture of biological adaptation to complex natural environments and further explore the universal laws and repeatability of environmental adaptation in related species. Through sampling, sequencing, and data collection, the project obtained 681 genomes from 11 D. simulans populations and 1,335 genomes from 22 D. melanogaster populations. Analysis revealed similarities in population structure and evolutionary history between the two species. Combining multiple methods to detect natural selection signals at different time scales, the study found that about 9%–14% of genes underwent adaptive convergent evolution between species, and convergence often occurred at the gene and pathway levels rather than at the site level. This study provides new insights into understanding the mechanisms of environmental adaptation and the repeatability of evolution.

Adaptive Convergence in D. simulans and D. melanogaster