Recombination rate plasticity: revealing mechanisms by design

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 pseudoobscuraThis article is part of the themed issue 'Evolutionary causes and consequences of recombination rate variation in sexual organisms'.

Keywords: Drosophila; crossing-over; meiosis; oogenesis; plasticity; recombination.

Figure 1.

Oogenesis, meiosis and mechanisms of recombination rate plasticity. The mature ovary (top right; adapted from Miller (1950) [63]) consists of multiple ovarioles. Multiple stages of oocyte differentiation are present in each ovariole present in the adult female. Details are shown for a single ovariole (shaded region of ovary) during the first round of oogenesis within the mother, to illustrate how these initial stages may be perturbed during development. Selected events during meiosis are shown to provide context. Time points of possible mechanisms of recombination rate plasticity are highlighted (filled symbols).

Figure 2.

Temporal and developmental elements of experimental design. The timing of the experimental treatment and brood collections is diagrammed for each type of approach, highlighting the example discussed. (I) Continuous exposure during development. Example: Plough 1917 [22]. F₁ females are reared under experimental conditions throughout development (including the pupal stage, white background) and returned to control conditions after eclosion (during sexual maturation and adulthood, yellow background). One or more broods are collected (navy blue). (II) Perturbation during development. Example: Grell 1971 [,–83]. A series of perturbations in experimental conditions are conducted. Each perturbation (orange) covers a defined window of time during pupal development. Only the first 10–15 eggs, the first egg maturing from each ovariole, are assessed for recombination rate. (III) Continuous exposure in adult stages. Example: Singh et al. 2015 [84]. Experimental treatments affect physiological conditions of the adult female at the same time as progeny are collected. Mature females were infected with pathogenic bacteria (dark purple), and compared with control treatments (light purple). Multiple broods were collected concurrently with the treatment effects. (IV) Perturbation during adult stages. Example: Plough 1917 [22]. Controlled perturbations are applied during adulthood, with progeny collected before, during and after the change in experimental conditions. In all cases, broods from genetically matched control F₁ females reared in standard room temperature conditions were also collected (not shown).

Figure 3.

Here, we present our empirical results of recombination plasticity due to temperature in D. pseudoobscura. In all panels, blue indicates the 18°C results and red represents the 23°C results. Asterisks indicate significant least-squares means contrasts (see electronic supplementary material, figure S1). These graphs show raw point measurement data for recombination rate calculated from individual F₁ parents, were LOESS smoothed using the two surrounding positions, and are presented with standard error of the smoother in grey, representing the variability across replicates. Each panel in the figure represents the 48 h time period during which each recombination rate measurement was estimated.