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Low levels of genetic differentiation with isolation by geography and environment in populations of Drosophila melanogaster from across China

Abstract

The fruit fly, Drosophila melanogaster, is a model species in evolutionary studies. However, population processes of this species in East Asia are poorly studied. Here we examined the population genetic structure of D. melanogaster across China. There were 14 mitochondrial haplotypes with 10 unique ones out of 23 known from around the globe. Pairwise FST values estimated from 15 novel microsatellites ranged from 0 to 0.11, with geographically isolated populations showing the highest level of genetic uniqueness. STRUCTURE analysis identified high levels of admixture at both the individual and population levels. Mantel tests indicated a strong association between genetic distance and geographical distance as well as environmental distance. Full redundancy analysis (RDA) showed that independent effects of environmental conditions and geography accounted for 62.10% and 31.58% of the total explained genetic variance, respectively. When geographic variables were constrained in a partial RDA analysis, the environmental variables bio2 (mean diurnal air temperature range), bio13 (precipitation of the wettest month), and bio15 (precipitation seasonality) were correlated with genetic distance. Our study suggests that demographic history, geographical isolation, and environmental factors have together shaped the population genetic structure of D. melanogaster after its introduction into China.

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Fig. 1: Collection site and geographical distribution of the mitochondrial cox1 haplotypes of Drosophila melanogaster.
Fig. 2: Neighbor-joining phylogenetic relationships among mitochondrial cox1 haplotypes of Drosophila melanogaster worldwide.
Fig. 3: Population genetic structure of 16 Drosophila melanogaster populations from China based on 15 microsatellite loci.
Fig. 4: Scatter plots of isolation by geograhical distance and environment for all populations of Drosophila melanogaster in China.
Fig. 5: Partial RDA analysis on genetic variance explained environmental variables when geographical variables were constrained.

Data availability

Mitochondrial genes and microsatellite data generated in this study were deposited to the Dryad database: https://doi.org/10.5061/dryad.37pvmcvgv.

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Acknowledgements

We thank De-Qiang Pu, Qian Li, Xiang-Zhao Yue, Kai Liu, Jia-Ying Zhu, Li-Na Sun, and Jin-Yu Li for their help on the collection of the samples. This research was funded by the National Natural Science Foundation of China (32070464), the Joint Laboratory of Pest Control Research Between China and Australia (Beijing Municipal Science & Technology Commission, 201100008320013), Beijing Postdoctoral Research Foundation (2020-22-108), and Beijing Key Laboratory of Environmental Friendly Management on Pests of North China Fruits (BZ0432).

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Correspondence to Li-Jun Cao or Shu-Jun Wei.

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Yue, L., Cao, LJ., Chen, JC. et al. Low levels of genetic differentiation with isolation by geography and environment in populations of Drosophila melanogaster from across China. Heredity 126, 942–954 (2021). https://doi.org/10.1038/s41437-021-00419-8

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