Abstract

For over a century, scientists have known that meiotic recombination rates can vary considerably among individuals, and that environmental conditions can modify recombination rates relative to the background. A variety of external and intrinsic factors such as temperature, age, sex and starvation can elicit ‘plastic’ responses in recombination rate. The influence of recombination rate plasticity on genetic diversity of the next generation has interesting and important implications for how populations evolve. Further, many questions remain regarding the mechanisms and molecular processes that contribute to recombination rate plasticity. Here, we review 100 years of experimental work on recombination rate plasticity conducted in Drosophila melanogaster. We categorize this work into four major classes of experimental designs, which we describe via classic studies in D. melanogaster. Based on these studies, we highlight molecular mechanisms that are supported by experimental results and relate these findings to studies in other systems. We synthesize lessons learned from this model system into experimental guidelines for using recent advances in genotyping technologies, to study recombination rate plasticity in non-model organisms. Specifically, we recommend (1) using fine-scale genome-wide markers, (2) collecting time-course data, (3) including crossover distribution measurements, and (4) using mixed effects models to analyse results. To illustrate this approach, we present an application adhering to these guidelines from empirical work we conducted in Drosophila pseudoobscura.This article is part of the themed issue ‘Evolutionary causes and consequences of recombination rate variation in sexual organisms’.

Highlights

  • Understanding biotic and abiotic influences on genetic variation in natural populations is a central goal of evolutionary genetics

  • We review 100 years of experimental work on recombination rate plasticity conducted in Drosophila melanogaster

  • We hope that highlighting the lessons learned from 100 years of studies in Drosophila will encourage scientists to apply these simple, yet powerful, methods to the study of recombination rate plasticity in other systems

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Summary

Introduction

Understanding biotic and abiotic influences on genetic variation in natural populations is a central goal of evolutionary genetics. We use it here to match literature referring to differences in observed recombination rates associated with various environmental, physiological or stressful conditions Classic research in this area grew from linkage studies in the model organism Drosophila. The prophase I arrest in mammals occurs during early development and is maintained for many years prior to ovulation Despite these differences, studies in both model species and non-model species inform one another; the temporal regulation of meiosis has similar properties in all animals and the stages and arrests are directly comparable [67]. The processes that can affect recombination rates are distinctly separated in time as oogenesis proceeds through subsequent stages This timing allows simple experimental designs in Drosophila, and other systems, which distinguish between two broad mechanistic hypotheses. To clearly explain how the interpretation of the data differs between different approaches we highlight a specific example for each basic type of experimental approach (figure 2), and relate these experiments to oogenesis and meiotic mechanisms suggested by the results (figure 1)

Drosophila as a model for studying recombination rate plasticity
Guidelines for studying recombination rate plasticity to uncover mechanisms
Findings
Concluding remarks
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