The impact of ageing on male reproductive success in Drosophila melanogaster

Scientists are rapidly developing synthetic gene drive elements intended for release into natural populations. These are intended to control or eradicate disease vectors and pests, or to spread useful traits through wild populations for disease control or conservation purposes. However, a crucial problem for gene drives is the evolution of resistance against them, preventing their spread. Understanding the mechanisms by which populations might evolve resistance is essential for engineering effective gene drive systems. This review summarizes our current knowledge of drive resistance in both natural and synthetic gene drives. We explore how insights from naturally occurring and synthetic drive systems can be integrated to improve the design of gene drives, better predict the outcome of releases and understand genomic conflict in general.

Resistance to natural and synthetic gene drive systems.

The important role that mate choice plays in the lives of animals is matched by the large and active research field dedicated to studying it. Researchers work on a wide range of species and behaviours, and so the experimental approaches used to measure animal mate choice are highly variable. Importantly, these differences are often not purely cosmetic; they can strongly influence the measurement of choice, for example by varying the behaviour of animals during tests, the aspects of choice actually measured, and statistical power. Consideration of these effects are important when comparing results among studies using different types of test, or when using laboratory results to predict animal behaviour in  natural populations. However, these effects have been underappreciated by the mate choice literature to date. I focus on five key experimental considerations that may influence choice: (i) should mating be allowed to occur, or should a proxy behavioural measure of preference be used instead? (ii) Should subjects be given a choice of options? (iii) Should each subject be tested more than once, either with the same or different stimuli? (iv) When given a choice, how many options should the subject choose between? (v) What form should the experimental stimuli take? I discuss the practical advantages and disadvantages of common experimental approaches, and how they may influence the measurement of mate choice in systematic ways. Different approaches often influence the ability of animals to perceive and compare stimuli presented during tests, or the perceived costs and benefits of being choosy. Given that variation in the design of mate choice experiments is likely unavoidable, I emphasise that there is no single 'correct' approach to measuring choice across species, although ecological relevance is crucial if the aim is to understand how choice acts in natural populations. I also highlight the need for quantitative estimates of the sizes of potentially important effects, without which we cannot make informed design decisions.

Designing mate choice experiments

Senescence is accompanied by loss of reproductive functions. Here, we studied reproductive ageing in Drosophila melanogaster males and asked whether the expected decline in male reproductive success is due to diminished functionality of the male accessory gland (AG). The male AG produces the majority of seminal fluid proteins (SFPs) transferred to the female at mating. SFPs induce female postmating changes and are key to male reproductive success. We measured age-dependent gene expression changes for five representative SFP genes in males from four different age groups ranging from 1 to 6 weeks after eclosion. Simultaneously, we also measured male reproductive success in postmating traits mediated by transfer of these five SFPs. We found a decreased in male SFP gene expression with advancing age and an accompanying decline in male postmating success. Hence, male reproductive senescence is associated with a decline in functionality of the male AG. While overall individual SFP genes decreased in expression, our results point towards the idea that the composition of an ejaculate might change with male age as the rate of change was variable for those five genes.

Gene expression changes in male accessory glands during ageing are accompanied by reproductive decline in Drosophila melanogaster.

Successful reproduction requires the completion of many, often condition-dependent, stages, from mate searching and courtship through to sperm transfer, fertilisation and offspring production. Animals can plastically adjust their investment in each stage according to the physical and social environment, their own condition, their future reproductive potential, and the condition of their partner. Here we manipulate age and condition, through a nutritional challenge early or late in life, of both male and female Drosophila melanogaster and measure the effects on courtship, mating, and fitness when paired with a standardized (unmanipulated) partner. Older males were slower to start courting and mating, and courted at a slower rate, but males were indifferent to female age or condition despite older females laying and hatching fewer eggs. Female condition had a substantial effect on mating acceptance rate, which dropped dramatically after starvation, and particularly recent starvation experience. In contrast, male condition had little effect on any of the components of reproductive performance we measured. Intriguingly, we found no evidence for additive or multiplicative effects of ageing and starvation: the only significant interaction between these variables was on male latency to initiate courtship - older males were slower to start courting unless they had experienced starvation early in life. These results indicate that the immediate costs of mating differ between males and females, and that the sexes differ in their perception of the opportunity cost sustained by refusing a mating opportunity. Our results support the idea that ageing has more wide-ranging impact on reproductive behaviours than does nutritional challenge.

M. Cuss

Papers

Age-based mate choice in the monandrous fruit fly Drosophila subobscura