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Seasonal changes in recombination characteristics in a natural population of Drosophila melanogaster

Abstract

Environmental seasonality is a potent evolutionary force, capable of maintaining polymorphism, promoting phenotypic plasticity and causing bet-hedging. In Drosophila, environmental seasonality has been reported to affect life-history traits, tolerance to abiotic stressors and immunity. Oscillations in frequencies of alleles underlying fitness-related traits were also documented alongside SNPs across the genome. Here, we test for seasonal changes in two recombination characteristics, crossover rate and crossover interference, in a natural D. melanogaster population from India using morphological markers of the three major chromosomes. We show that winter flies, collected after the dry season, have significantly higher desiccation tolerance than their autumn counterparts. This difference proved to hold also for hybrids with three independent marker stocks, suggesting its genetic rather than plastic nature. Significant between-season changes are documented for crossover rate (in 9 of 13 studied intervals) and crossover interference (in four of eight studied pairs of intervals); both single and double crossovers were usually more frequent in the winter cohort. The winter flies also display weaker plasticity of both recombination characteristics to desiccation. We ascribe the observed differences to indirect selection on recombination caused by directional selection on desiccation tolerance. Our findings suggest that changes in recombination characteristics can arise even after a short period of seasonal adaptation (~8–10 generations).

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Fig. 1: The location of the studied markers on the genetic map (A) and the overall scheme of experiment (B).
Fig. 2: The effect of season on desiccation tolerance in the autumn and the winter parental isofemale lines and their hybrids with three marker stocks.
Fig. 3: The effect of season on crossover rates in hybrids reared in normal conditions.
Fig. 4: The effect of desiccation stress on crossover rates in the autumn (A) and the winter (B) hybrids.

Data availability

The raw data (desiccation tolerance of all examined lines and genotypes of all test-cross progeny) are publicly available at Dryad: https://doi.org/10.5061/dryad.g1jwstqr8.

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Acknowledgements

We are grateful to Prof. SC Lakhotia (Banaras Hindu University, India) for kindly providing all the laboratory facilities to conduct the experiments. We thank Prof. II Dzeverin (Schmalhausen Institute of Zoology, National Academy of Sciences of Ukraine) and two anonymous reviewers for their helpful comments on the manuscript. SR is deeply thankful to Nataliya and Sandra Rybnikova for their assistance in surveying the literature and processing the data.

Funding

The study was supported by DS Kothari postdoctoral research project (grant F.4-2/2006(BSR)/BL/16-17/0330 University Grants Commission, India) sanctioned to DDA, the Israel Science Foundation (grant 1844/17), and the Israeli Ministry of Aliyah and Integration.

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Aggarwal, D.D., Rybnikov, S., Sapielkin, S. et al. Seasonal changes in recombination characteristics in a natural population of Drosophila melanogaster. Heredity (2021). https://doi.org/10.1038/s41437-021-00449-2

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