How are life history and reproductive behaviour coordinated?
Lead Research Organisation:
University of Oxford
Department Name: Zoology
Abstract
Why do we age? In humans, as in most animals, the ability to maintain a healthy body, produce offspring and fight disease declines as we get older. This is a puzzling phenomenon. An animal that could carry on mating and reproducing forever would be at an evolutionary advantage because it would maximise its contribution of genes to the next generation. However, the vast majority of animals can't do this. The natural world shows us that, all else being equal, there is usually a negative relationship between longevity and reproduction: animals tend to be either fast reproducers or long-lived. This is thought to be because resources are limited, and animals can either invest the available resources in maintaining their body for a long life or they can invest them in lots of mating and offspring production - but not both. Alternatively, the efforts of mating and producing offspring might cause irreversible damage to the body that ultimately leads to its decline. Either way, evolutionary theories predict that eternal life and high rates of fecundity should be impossible.
Recent reports of genetic manipulations that increase lifespan without reducing reproduction have therefore generated much interest. The research, conducted in invertebrate organisms such as the nematode worm and the fruit fly, suggests that different processes might control lifespan and reproduction. If this were true, then evolutionary theory would face a major challenge. However, the long-lived, high fecundity worms and flies were genetically modified and experimented upon in the laboratory, an environment that lacks the stresses and pressures of the natural world. Furthermore, experiments are often carried out under specific sexual conditions: either where there is little or no opportunity to mate, or where mating is unlimited. This complicates matters because sexual activity per se has a large effect on lifespan: lots of mating results in early death in these species. My recent work has shown that some genetic modifications that increase the lifespan of female fruit flies, also makes them less willing to mate with males. Thus, if researchers do not control or measure the sexual activity of animals in their experiments, they could mistakenly attribute increased lifespan to the direct effect of genetic manipulations rather than long-life as a result of less sexual activity. Moreover, we don't know how differences in sexual activity affects lifespan in long-lived flies, or whether sex-specific behaviour impacts lifespan.
The aim of my project is to investigate this relationship between lifespan and reproductive behaviour in the fruit fly, Drosophila melanogaster, to address the problems posed above. Firstly, the work will identify the genetic links between the regulation of lifespan and the regulation of sexual behaviour in males and females, to find out how the genetic regulation of lifespan affects sexual activity as flies age, and thus whether it is possible for flies to be sexually active for longer. Secondly I will test whether the number of mating opportunities that males and females experience affects the genetic control of lifespan (i.e. how 'robust' long-lived mutants are to different levels of reproductive activity). Finally I will test whether sex-specific behaviours affect lifespan and can explain differences in longevity between the sexes. The results of these experiments will give us a clear picture of the relationship between sex and lifespan: how manipulating lifespan affects sexual behaviour and how changing sexual behaviour affects lifespan. This will help us understand how animals maximise their reproductive lifespan and why sex seems to have an inevitable association with senescence.
Recent reports of genetic manipulations that increase lifespan without reducing reproduction have therefore generated much interest. The research, conducted in invertebrate organisms such as the nematode worm and the fruit fly, suggests that different processes might control lifespan and reproduction. If this were true, then evolutionary theory would face a major challenge. However, the long-lived, high fecundity worms and flies were genetically modified and experimented upon in the laboratory, an environment that lacks the stresses and pressures of the natural world. Furthermore, experiments are often carried out under specific sexual conditions: either where there is little or no opportunity to mate, or where mating is unlimited. This complicates matters because sexual activity per se has a large effect on lifespan: lots of mating results in early death in these species. My recent work has shown that some genetic modifications that increase the lifespan of female fruit flies, also makes them less willing to mate with males. Thus, if researchers do not control or measure the sexual activity of animals in their experiments, they could mistakenly attribute increased lifespan to the direct effect of genetic manipulations rather than long-life as a result of less sexual activity. Moreover, we don't know how differences in sexual activity affects lifespan in long-lived flies, or whether sex-specific behaviour impacts lifespan.
The aim of my project is to investigate this relationship between lifespan and reproductive behaviour in the fruit fly, Drosophila melanogaster, to address the problems posed above. Firstly, the work will identify the genetic links between the regulation of lifespan and the regulation of sexual behaviour in males and females, to find out how the genetic regulation of lifespan affects sexual activity as flies age, and thus whether it is possible for flies to be sexually active for longer. Secondly I will test whether the number of mating opportunities that males and females experience affects the genetic control of lifespan (i.e. how 'robust' long-lived mutants are to different levels of reproductive activity). Finally I will test whether sex-specific behaviours affect lifespan and can explain differences in longevity between the sexes. The results of these experiments will give us a clear picture of the relationship between sex and lifespan: how manipulating lifespan affects sexual behaviour and how changing sexual behaviour affects lifespan. This will help us understand how animals maximise their reproductive lifespan and why sex seems to have an inevitable association with senescence.
Planned Impact
The project proposed here will increase our understanding of the relationship between sexual behaviour and lifespan. It is a topic of wide interest to scientists and the public alike. The integrative approach of the research, combining the genetics of lifespan and sex-specific regulation with the evolutionary ecology of mating behaviour, ensures that the results will have broad appeal and will impact research areas including life-history evolution, animal behaviour, reproductive biology, gerontology, molecular biology and genetics, and neuroscience.
Outside of specialist academics in the same field, the main beneficiaries are likely to be in insect pest control and in the human health sector.
The research will be of interest to researchers who are trying to develop new or more effective ways of controlling insect pests or disease vectors. For example, some human borne diseases require their insect vectors to host them for a certain amount of time before they can be transmitted to humans (e.g. mosquito borne diseases such as dengue fever and malaria). Understanding the mechanisms that regulate insect lifespan is therefore of major importance. Also important is to understand the mechanisms that control sexual behaviour. This is because the success of control methods, such as the sterile insect technique (SIT), can depend on the extent of female multiple mating (monogamy tends to make the technique more effective). Thus my research will potentially benefit pest-control technology companies and their users: people who consume insect pest-infected food or materials.
My research will also contribute to our understanding of the fundamental biology and evolution of ageing. The potential economic and health benefits of clinical interventions that prevent age-related declines in biological function are enormous. The results of my research will help us understand the impacts of ageing on reproductive behaviour and vice versa. Ultimately, the research might inform the best avenues for research aimed at producing treatments to reduce age-related health problems, including in humans.
As detailed in the Pathways To Impact section I will engage with applied insect pest control researchers to exchange knowledge and realise potential applied benefits of my findings. Furthermore I will implement several strategies to advertise my work: via the internet (webpage and podcast activity) and via the University of Oxford press office, to facilitate media publicity. In addition to presenting my research at a broad range of conferences, I will publish in open access journals (PLoS, and BMC) where possible to maximise access to my research output.
Outside of specialist academics in the same field, the main beneficiaries are likely to be in insect pest control and in the human health sector.
The research will be of interest to researchers who are trying to develop new or more effective ways of controlling insect pests or disease vectors. For example, some human borne diseases require their insect vectors to host them for a certain amount of time before they can be transmitted to humans (e.g. mosquito borne diseases such as dengue fever and malaria). Understanding the mechanisms that regulate insect lifespan is therefore of major importance. Also important is to understand the mechanisms that control sexual behaviour. This is because the success of control methods, such as the sterile insect technique (SIT), can depend on the extent of female multiple mating (monogamy tends to make the technique more effective). Thus my research will potentially benefit pest-control technology companies and their users: people who consume insect pest-infected food or materials.
My research will also contribute to our understanding of the fundamental biology and evolution of ageing. The potential economic and health benefits of clinical interventions that prevent age-related declines in biological function are enormous. The results of my research will help us understand the impacts of ageing on reproductive behaviour and vice versa. Ultimately, the research might inform the best avenues for research aimed at producing treatments to reduce age-related health problems, including in humans.
As detailed in the Pathways To Impact section I will engage with applied insect pest control researchers to exchange knowledge and realise potential applied benefits of my findings. Furthermore I will implement several strategies to advertise my work: via the internet (webpage and podcast activity) and via the University of Oxford press office, to facilitate media publicity. In addition to presenting my research at a broad range of conferences, I will publish in open access journals (PLoS, and BMC) where possible to maximise access to my research output.
Organisations
Publications
Hopkins BR
(2019)
BMP signaling inhibition in Drosophila secondary cells remodels the seminal proteome and self and rival ejaculate functions.
in Proceedings of the National Academy of Sciences of the United States of America
Carazo P
(2014)
Within-group male relatedness reduces harm to females in Drosophila.
in Nature
Bath E
(2017)
Sperm and sex peptide stimulate aggression in female Drosophila.
in Nature ecology & evolution
| Description | My research has driven forward our understanding of Drosophila reproductive behaviour and evolution. In particular, the work has revealed the roles of relatedness and inbreeding in mating behaviour, and the consequences for lifespan. Elsewhere my research has identified key routes for future ejaculate research, to understand the function and evolution of male seminal fluid components, and their effects on females. |
| Exploitation Route | The research provides insights into the basic biology of reproduction and lifespan in insects. As such the data might ultimately be of use in developing insect pest control strategies. Also, where similar mechanisms exist in higher organisms the work on ejaculates may ultimately help inform assisted reproduction techniques. |
| Sectors | Agriculture Food and Drink Environment Pharmaceuticals and Medical Biotechnology |
| Description | My research has generated a lot of media exposure and thus contribute to the public understanding of science. For example the altimetric scores of 3 of my papers were in the top 5% of all articles, ranked by attention. |
| Sector | Other |
| Impact Types | Cultural |
| Title | Data from: Developmental environment effects on sexual selection in male and female Drosophila melanogaster |
| Description | The developmental environment can potentially alter the adult social environment and influence traits targeted by sexual selection such as body size. In this study, we manipulated larval density in male and female Drosophila melanogaster, which results in distinct adult size phenotypes - high (low) densities for small (large) adults - and measured sexual selection in experimental groups consisting of adult males and females from high, low, or a mixture of low and high larval densities. Overall, large adult females (those reared at low larval density) had more matings, more mates and produced more offspring than small females (those reared at high larval density). The number of offspring produced by females was positively associated with their number of mates (i.e. there was a positive female Bateman gradient) in social groups where female size was experimentally varied, likely due to the covariance between female productivity and mating rate. For males, we found evidence that the larval environment affected the relative importance of sexual selection via mate number (Bateman gradients), mate productivity, paternity share, and their covariances. Mate number and mate productivity were significantly reduced for small males in social environments where males were of mixed sizes, versus social environments where all males were small, suggesting that social heterogeneity altered selection on this subset of males. Males are commonly assumed to benefit from mating with large females, but in contrast to expectations we found that in groups where both the male and female size varied, males did not gain more offspring per mating with large females. Collectively, our results indicate sex-specific effects of the developmental environment on the operation of sexual selection, via both the phenotype of individuals, and the phenotype of their competitors and mates. |
| Type Of Material | Database/Collection of data |
| Year Produced | 2017 |
| Provided To Others? | Yes |
| URL | https://datadryad.org/stash/dataset/doi:10.5061/dryad.cg0gn |
| Title | Data from: Social group composition modulates the role of last male sperm precedence in post-copulatory sexual selection |
| Description | In many species, the order in which males mate with a female explains much of the variation in paternity arising from post-copulatory sexual selection. Research in Drosophila suggests that mating order may account for the majority of the variance in male reproductive success. However, the effects of mating order on paternity bias might not be static but could potentially vary with social or environmental factors. To test this idea, we used an existing dataset, collated from an experiment we previously published (Morimoto et al. 2016), with the addition of unpublished data from the same experiment. These previous experiments manipulated larval density in Drosophila melanogaster which generated variation in male and female body size, assembled groups of individuals of different sizes, and measured the mating success and paternity share of focal males. The data presented here provide information on each focal male's mating order and the frequency in which focal males remated with the same females ('repetitive matings'). We combined this information with our previously reported focal male reproductive success to partition variance in paternity into male mating order and repetitive matings across groups that differed in the body size composition of males and females. We found, as expected, that male mating order explained a considerable portion of the variance in male paternity. However, we also found that the impact of male mating order on male paternity was influenced by the body size composition of groups. Specifically, males that tended to mate last had a greater paternity advantage, and displayed lower variance, in groups containing a heterogenous mixture of male body sizes than in groups with a single male body size. Repetitive mating only had a minor contribution to the variance in male paternity share across all experiments. Overall, our findings contribute to the growing body of research showing that post-copulatory sexual selection is subject to socio-ecological influences. |
| Type Of Material | Database/Collection of data |
| Year Produced | 2023 |
| Provided To Others? | Yes |
| URL | https://datadryad.org/stash/dataset/doi:10.5061/dryad.tb2rbp05t |