Selection on behaviour and life histories across generations in a natural population

Lead Research Organisation: University of Sheffield
Department Name: Animal and Plant Sciences

Abstract

Insects make up the vast majority of animal biodiversity and have been studied intensively in the lab, providing numerous insights into how evolution works. However, there is now a serious imbalance between what we know about evolutionary biology in the lab and what we know about how things actually work in nature. This discrepancy is a source of concern for two reasons: Firstly, laboratory situations may be misleading as they remove sources of selection that may be very important in wild populations; for instance, it may be that male crickets that sing louder get more mates in the lab but in the field this is balanced by being more likely to be eaten by birds. Secondly, we urgently need to improve our understanding of how natural populations can respond to environmental change, and for this, we need studies of insects as well as vertebrates. Four years ago we began monitoring a population of field crickets in Spanish meadow. Over the last 2 years we have studied the population intensively, tagging every individual and recording their lives using a network of 96 video cameras. The reproductive success of every individual and the pattern of relationships across generations have been estimated using DNA fingerprinting techniques. This has already provided important insights, such as showing that males vary more than females in how many offspring they have and that the traits displayed by males that have lots of mates are different from the traits typical of males that have lots of offspring. In this project we will dramatically improve our video monitoring and our ability to determine the relationships between individuals (by using new digital camera technology and new SNP genotyping techniques). We will combine information across years about the population as a whole, how individuals are related, their life histories, behaviour and reproductive success. This comprehensive information about every individual will allow us to address our major aims of determining how much genetic variation is present and whether natural and sexual selection, which drive evolution in populations, are consistent across years or whether they vary a lot. This is important because if in some years certain types of individual do well, whereas in others, different traits are more advantageous, this will help maintain genetic variation. Such variation allows populations to adapt to environmental change, so we need to understand how much there is and how it is maintained. A related aim will be to investigate how population density affects selection, something that we can only investigate with data from a number of years. A second set of objectives relate to examining aspects of sexual selection that have been well studied in laboratories, but neglected in the wild. These include finding out whether particular males and females or particular pairs of mates tend to be more successful either because they have genes that produce offspring that are intrinsically superior to the offspring of some other pairs or because certain combinations of individuals are more genetically compatible with one another, for instance because they are not close relatives. We will address these questions by comparing the reproductive success of pairs of wild crickets and examining how they differ genetically from one another. This will also allow us to look for evidence of genes that can persist in populations even though they reduce the fitness of one sex, because they increase the fitness of the other sex, something that has been demonstrated in the lab, but little studied in the wild. We will use the comprehensive data we have on the life histories of all the crickets in our population to investigate the question of whether short lived animals such as crickets actually die of old age, or whether they just keep going until something kills them. There are very few studies of the lives of wild invertebrates so even major questions like this remain to be answered

Publications

10 25 50
 
Description See submission from lead PI - Prof T Tregenza (Exeter, Falmouth Campus).
Briefly, we developed genetic markers and profiling techniques to examine reproductive success, inbreeding, mate choice, natural selection and sexual selection in a wild population of crickets.
This study system is unique in the sense that entire life histories are recorded for individuals in the population; something that is usually only possible in vertebrates.
Exploitation Route We have developed methods and results that other researchers of wild insect populations can take forward.
Follow-up projects (run by the PI and the Sheffield coI) have been funded on the back of our findings, especially in relation to studying ageing.
Sectors Digital/Communication/Information Technologies (including Software)

Electronics

Environment

Culture

Heritage

Museums and Collections

URL http://www.wildcrickets.org/
 
Description See submission from lead-PI, Prof T Tregenza for information.
First Year Of Impact 2008
Sector Digital/Communication/Information Technologies (including Software),Education,Electronics
Impact Types Cultural

Economic

 
Title Additional file 1: Fig. S1-3. of Wild cricket social networks show stability across generations 
Description Plots of the full (left box in each panel) and reduced (right box in each panel) simulations and their predictive distances (y axis). The predictive distance is the difference between the simulated values and the real value from the network. S1 is for mean path length, S2 for degree correlation and S3 for clustering coefficient. See Methods (in the main text) for details on how these were calculated and see Results for which comparisons are statistically significant. (ZIP 21Â kb) 
Type Of Material Database/Collection of data 
Year Produced 2016 
Provided To Others? Yes  
URL https://springernature.figshare.com/articles/dataset/Additional_file_1_Fig_S1-3_of_Wild_cricket_soci...
 
Title Additional file 1: Fig. S1-3. of Wild cricket social networks show stability across generations 
Description Plots of the full (left box in each panel) and reduced (right box in each panel) simulations and their predictive distances (y axis). The predictive distance is the difference between the simulated values and the real value from the network. S1 is for mean path length, S2 for degree correlation and S3 for clustering coefficient. See Methods (in the main text) for details on how these were calculated and see Results for which comparisons are statistically significant. (ZIP 21Â kb) 
Type Of Material Database/Collection of data 
Year Produced 2016 
Provided To Others? Yes  
URL https://springernature.figshare.com/articles/dataset/Additional_file_1_Fig_S1-3_of_Wild_cricket_soci...
 
Title Data from: Slower senescence in a wild insect population in years with a more female-biased sex ratio 
Description Life-history theories of senescence are based on the existence of a trade-off in resource allocation between body maintenance and reproduction. This putative trade-off means that environmental and demographic factors affecting the costs of reproduction should be associated with changes in patterns of senescence. In many species, competition among males is a major component of male reproductive investment, and hence variation in the sex ratio is expected to affect rates of senescence. We test this prediction using nine years of demographic and behavioural data from a wild population of the annual field cricket Gryllus campestris. Over these generations the sex ratio at adulthood varied substantially, from years with an equal number of each sex to years with twice as many females as males. Consistent with the predictions of theory, we found that in years with a greater proportion of females, both sexes experienced a slower increase in mortality rate with age. Additionally, phenotypic senescence in males was slower in years when there were more females. Sex ratio did not affect the baseline mortality rate in males, but females suffered higher age-independent mortality rates when males were in short supply. 
Type Of Material Database/Collection of data 
Year Produced 2019 
Provided To Others? Yes  
URL https://datadryad.org/stash/dataset/doi:10.5061/dryad.fk52454
 
Title Environment and mate attractiveness in a wild insect 
Description Abstract The role of female choice in sexual selection is well established, including the recognition that females choose their mates based on multiple cues. These cues may include intrinsic aspects of a male's phenotype as well as aspects of the environment associated with the male. The role of the spatial location of a potential mate has been well studied in territorial vertebrates. However, despite their role as laboratory models for studies of sexual selection, the potential for insects to choose their mates on the basis of location has scarcely been studied. We studied a natural population of individually tagged crickets (Gryllus campestris) in a meadow in Northern Spain. Adults typically move between burrows every few days, allowing us to examine how pairing success of males can be predicted by the burrow they occupy, independent of their own characteristics. We observed the entirety of ten independent breeding seasons to provide replication and to determine whether the relative importance of these factors is stable across years. We find that both male ID and the ID his burrow affect the likelihood that he is paired with a female, but the burrow has a consistently greater influence. Furthermore, the two factors interact: the relative attractiveness of an individual male depends on which burrow he occupies. Our finding demonstrates a close interaction between naturally and sexually selected traits. It also demonstrates that mate choice studies may benefit from considering not only obvious secondary sexual traits, but also more cryptic traits such as microhabitat choice. 
Type Of Material Database/Collection of data 
Year Produced 2022 
Provided To Others? Yes  
URL https://datadryad.org/stash/dataset/doi:10.5061/dryad.0cfxpnw5h
 
Title Evidence for genetic isolation and local adaptation in the field cricket Gryllus campestris 
Description Understanding how species can thrive in a range of environments is a central challenge for evolutionary ecology. There is strong evidence for local adaptation along large-scale ecological clines in insects. However, potential adaptation among neighbouring populations differing in their environment has been studied much less. We used RAD-sequencing to quantify genetic divergence and clustering of ten populations of the field cricket Gryllus campestris in the Cantabrian Mountains of northern Spain, and an outgroup on the coastal plain. Our populations were chosen to represent replicate high and low altitude habitats. We identified genetic clusters that include both high and low altitude populations indicating that the two habitat types do not hold ancestrally distinct lineages. Using common-garden rearing experiments to remove environmental effects, we found evidence for differences between high and low altitude populations in physiological and life-history traits. As predicted by the local adaptation hypothesis, crickets with parents from cooler (high altitude) populations recovered from periods of extreme cooling more rapidly than those with parents from warmer (low altitude) populations. Growth rates also differed between offspring from high and low altitude populations. However, contrary to our prediction that crickets from high altitudes would grow faster, the most striking difference was that at high temperatures, growth was fastest in individuals from low altitudes. Our findings reveal that populations a few tens of kilometres apart have independently evolved adaptations to their environment. This suggests that local adaptation in a range of traits may be commonplace even in mobile invertebrates at scales of a small fraction of species' distributions. 
Type Of Material Database/Collection of data 
Year Produced 2021 
Provided To Others? Yes  
URL https://datadryad.org/stash/dataset/doi:10.5061/dryad.j9kd51ccx