Experimental evolution of recombination and crossover interference in Drosophila caused by directional selection for stress-related traits

Dau Dayal Aggarwal, Eugenia Rashkovetsky, Pawel Michalak, Irit Cohen, Yefim Ronin, Dan Zhou, Gabriel G. Haddad, Abraham B. Korol

Research output: Contribution to journalArticlepeer-review

Abstract

Background: Population genetics predicts that tight linkage between new and/or pre-existing beneficial and deleterious alleles should decrease the efficiency of natural selection in finite populations. By decoupling beneficial and deleterious alleles and facilitating the combination of beneficial alleles, recombination accelerates the formation of high-fitness genotypes. This may impose indirect selection for increased recombination. Despite the progress in theoretical understanding, interplay between recombination and selection remains a controversial issue in evolutionary biology. Even less satisfactory is the situation with crossover interference, which is a deviation of double-crossover frequency in a pair of adjacent intervals from the product of recombination rates in the two intervals expected on the assumption of crossover independence. Here, we report substantial changes in recombination and interference in three long-term directional selection experiments with Drosophila melanogaster: for desiccation (~50 generations), hypoxia, and hyperoxia tolerance (>200 generations each). Results: For all three experiments, we found a high interval-specific increase of recombination frequencies in selection lines (up to 40-50% per interval) compared to the control lines. We also discovered a profound effect of selection on interference as expressed by an increased frequency of double crossovers in selection lines. Our results show that changes in interference are not necessarily coupled with increased recombination. Conclusions: Our results support the theoretical predictions that adaptation to a new environment can promote evolution toward higher recombination. Moreover, this is the first evidence of selection for different recombination-unrelated traits potentially leading, not only to evolution toward increased crossover rates, but also to changes in crossover interference, one of the fundamental features of recombination.

Original languageEnglish
Article number101
JournalBMC Biology
Volume13
Issue number1
DOIs
StatePublished - 27 Nov 2015

Bibliographical note

Funding Information:
We acknowledge with thanks the three reviewers and Graham Bell for their helpful comments and suggestions. We also thank Zeev Frenkel for productive discussions and help in computer simulations. The study was supported by Binational USA-Israeli Science Foundation (grant BSF # 2011438) and Postdoctoral fellowship for DDA from the Israeli Council for Higher Education and University of Haifa.

Publisher Copyright:
© 2015 Aggarwal et al.

Keywords

  • D. melanogaster
  • Directional selection
  • Evolution of interference
  • Negative interference
  • Positive interference

ASJC Scopus subject areas

  • Biotechnology
  • Structural Biology
  • Ecology, Evolution, Behavior and Systematics
  • Physiology
  • Biochemistry, Genetics and Molecular Biology (all)
  • Agricultural and Biological Sciences (all)
  • Plant Science
  • Developmental Biology
  • Cell Biology

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