Evolutionary biology and genetic techniques for insect control

The requirement to develop new techniques for insect control that minimize negative environmental impacts has never been more pressing. Here we discuss population suppression and population replacement technologies. These include sterile insect technique, genetic elimination methods such as the release of insects carrying a dominant lethal (RIDL), and gene driving mechanisms offered by intracellular bacteria and homing endonucleases. We also review the potential of newer or underutilized methods such as reproductive interference, CRISPR technology, RNA interference (RNAi), and genetic underdominance. We focus on understanding principles and potential effectiveness from the perspective of evolutionary biology. This offers useful insights into mechanisms through which potential problems may be minimized, in much the same way that an understanding of how resistance evolves is key to slowing the spread of antibiotic and insecticide resistance. We conclude that there is much to gain from applying principles from the study of resistance in these other scenarios – specifically, the adoption of combinatorial approaches to minimize the spread of resistance evolution. We conclude by discussing the focused use of GM for insect pest control in the context of modern conservation planning under land-sparing scenarios

Sexual Conflict: Mechanisms and Emerging Themes in Resistance Biology

Sexual conflict is acknowledged as pervasive, with the potential to generate and maintain genetic variation. Mechanistic studies of conflict have been important in providing direct evidence for the existence of sexual conflict. They have also led to the growing realization that there is a striking phenotypic diversity of adaptations whose evolution can be shaped by sexually antagonistic selection. The mechanisms involved range from the use of genital spines, claspers, songs, and smells to ejaculate molecules. In one well-studied example, sexual conflict can occur over the sexually antagonistic effects of seminal fluid proteins in Drosophila melanogaster. However, an important puzzle remains, namely, why seminal fluid proteins are so numerous and complex, hence whether all or some are involved in mediating sexual conflict. I hypothesize that this rich diversity and the complexity of traits subject to sexually antagonistic selection in general may arise, at least in part, due to the deployment of sexually antagonistic adaptations in males in a way that lessens the probability of broadscale, strong resistance evolution in females. In elaborating this hypothesis, I explore how research into the evolution of resistance to insecticides, antimicrobials, and vaccines might be used to provide insights into the evolution of female resistance to the effects of sexually antagonistic manipulative traits of males. In this manner, the manipulative traits of males can be resistance-proofed

Effect of competitive cues on reproductive morphology and behavioral plasticity in male fruitflies

Phenotypic plasticity will be favored whenever there are significant fitness benefits of responding to environmental variation. The extent and nature of the plasticity that evolves depends on the rate of environmental fluctuations and the capacity to track and respond to that variability. Reproductive environments represent one arena in which changes can be rapid. The finding that males of many species show morphological, physiological, and behavioral plasticity in response to premating and postmating reproductive competition (RC) suggests that plasticity is broadly beneficial. The developmental environment is expected to accurately predict the average population level of RC but to be a relatively poor indicator of immediate RC at any particular mating. Therefore, we predict that manipulation of average RC during development should cause a response in plasticity “set” during development (e.g., size of adult reproductive structures), but not in flexible plasticity determined by the immediate adult environment (e.g., behavioral plasticity in mating duration). We tested this prediction in Drosophila melanogaster males by manipulating 2 independent cues of average RC during development: 1) larval density and 2) the presence or absence of adult males within larval culture vials. Consistent with the prediction, both manipulations resulted in the development of males with significantly larger adult accessory glands (although testis size decreased when males were added to culture vials). There was no effect on adult plasticity (mating duration, extended mating in response to rivals). The results suggest that males have evolved independent responses to long- and short-term variation in RC

Effect of competitive cues on reproductive morphology and behavioral plasticity in male fruitflies

Phenotypic plasticity will be favored whenever there are significant fitness benefits of responding to environmental variation. The extent and nature of the plasticity that evolves depends on the rate of environmental fluctuations and the capacity to track and respond to that variability. Reproductive environments represent one arena in which changes can be rapid. The finding that males of many species show morphological, physiological, and behavioral plasticity in response to premating and postmating reproductive competition (RC) suggests that plasticity is broadly beneficial. The developmental environment is expected to accurately predict the average population level of RC but to be a relatively poor indicator of immediate RC at any particular mating. Therefore, we predict that manipulation of average RC during development should cause a response in plasticity “set” during development (e.g., size of adult reproductive structures), but not in flexible plasticity determined by the immediate adult environment (e.g., behavioral plasticity in mating duration). We tested this prediction in Drosophila melanogaster males by manipulating 2 independent cues of average RC during development: 1) larval density and 2) the presence or absence of adult males within larval culture vials. Consistent with the prediction, both manipulations resulted in the development of males with significantly larger adult accessory glands (although testis size decreased when males were added to culture vials). There was no effect on adult plasticity (mating duration, extended mating in response to rivals). The results suggest that males have evolved independent responses to long- and short-term variation in RC

MicroRNAs influence reproductive responses by females to male sex peptide in Drosophila melanogaster

Across taxa, female behavior and physiology changes significantly following the receipt of ejaculate molecules during mating. For example, receipt of sex peptide (SP) in female Drosophila melanogaster significantly alters female receptivity, egg production, lifespan, hormone levels, immunity, sleep and feeding patterns. These changes are underpinned by distinct tissue- and time-specific changes in diverse sets of mRNAs. However, little is yet known about the regulation of these gene expression changes, and hence the potential role of microRNAs (miRNAs), in female post-mating responses. A preliminary screen of genomic responses in females to receipt of SP suggested that there were changes in the expression of several miRNAs. Here we tested directly whether females lacking four of the candidate miRNAs highlighted (miR-279, miR-317, miR-278 and miR-184) showed altered fecundity, receptivity and lifespan responses to receipt of SP, when mated once or continually to SP null or control males. The results showed that miRNA-lacking females mated to SP null males exhibited altered receptivity, but not reproductive output, in comparison to controls. However, these effects interacted significantly with the genetic background of the miRNA-lacking females. No significant survival effects were observed in miRNA-lacking females housed continually with SP null or control males. However, continual exposure to control males that transferred SP resulted in significantly higher variation in miRNA-lacking female lifespan than did continual exposure to SP null males. The results provide the first insight into the effects and importance of miRNAs in regulating post-mating responses in females

Evolution of ageing as a tangle of trade-offs:energy versus function

Despite tremendous progress in recent years, our understanding of the evolution of ageing is still incomplete. A dominant paradigm maintains that ageing evolves due to the competing energy demands of reproduction and somatic maintenance leading to slow accumulation of unrepaired cellular damage with age. However, the centrality of energy trade-offs in ageing has been increasingly challenged as studies in different organisms have uncoupled the trade-off between reproduction and longevity. An emerging theory is that ageing instead is caused by biological processes that are optimized for early-life function but become harmful when they continue to run-on unabated in late life. This idea builds on the realization that early-life regulation of gene expression can break down in late life because natural selection is too weak to optimize it. Empirical evidence increasingly supports the hypothesis that suboptimal gene expression in adulthood can result in physiological malfunction leading to organismal senescence. We argue that the current state of the art in the study of ageing contradicts the widely held view that energy trade-offs between growth, reproduction, and longevity are the universal underpinning of senescence. Future research should focus on understanding the relative contribution of energy and function trade-offs to the evolution and expression of ageing

Testing for assortative mating by diet in Drosophila melanogaster

Experimental studies of the evolution of reproductive isolation in real time are a powerful way to reveal the way that fundamental processes, such as mate choice, initiate divergence. Mate choice, while frequently described in females, can occur in either sex, and can be affected by the genetics or environment of an individual. Here we describe simple protocols for assessing mating outcomes in fruit flies, which in this context can be used to assess reproductive isolation derived from rearing on different diets over multiple generations

Diet, Gut Microbes and Host Mate Choice:Understanding the significance of microbiome effects on host mate choice requires a case by case evaluation

All organisms live in close association with microbes. However, not all such associations are meaningful in an evolutionary context. Current debate concerns whether hosts and microbes are best described as communities of individuals or as holobionts (selective units of hosts plus their microbes). Recent reports that assortative mating of hosts by diet can be mediated by commensal gut microbes have attracted interest as a potential route to host reproductive isolation (RI). Here we discuss logical problems with this line of argument. We briefly review how microbes can affect host mating preferences and evaluate recent findings from fruitflies. Endosymbionts can potentially influence host RI given stable and recurrent co-association of hosts and microbes over evolutionary time. However, observations of co-occurrence of microbes and hosts are ripe for misinterpretation and such associations will rarely represent a meaningful holobiont. A framework in which hosts and their microbes are independent evolutionary units provides the only satisfactory explanation for the observed range of effects and associations

Sex-Specific Responses of Life Span and Fitness to Variation in Developmental Versus Adult Diets in Drosophila melanogaster

Nutritional variation across the lifetime can have significant and sex-specific impacts on fitness. Using Drosophila melanogaster, we measured these impacts by testing the effects on life span and reproductive success of high or low yeast content in developmental versus adult diets, separately for each sex. We tested two hypotheses: that dietary mismatches between development and adulthood are costly and that any such costs are sex-specific. Overall, the results revealed the rich and complex responses of each sex to dietary variation across the lifetime. Contrary to the first hypothesis, dietary mismatches between developmental and adult life stages were not universally costly. Where costs of nutritional variation across the life course did occur, they were sex-, context-, and trait-specific, consistent with hypothesis 2. We found effects of mismatches between developmental and adult diets on reproductive success in females but not males. Adult diet was the main determinant of survival, and life span was significantly longer on high yeast adult food, in comparison to low, in both sexes. Developing on a high yeast diet also benefited adult female life span and reproductive success, regardless of adult diet. In contrast, a high yeast developmental diet was only beneficial for male life span when it was followed by low yeast adult food. Adult diet affected mating frequency in opposing directions, with males having higher mating frequency on high and females on low, with no interaction with developmental diet for either sex. The results emphasize the importance of sex differences and of the directionality of dietary mismatches in the responses to nutritional variation