Does sexual selection accelerate adaptation in the wild?

Lead Research Organisation: University of Exeter
Department Name: Biosciences

Abstract

Our aim is to understand how sexual selection (variation among males in their ability to gain fertilisations) affects how populations evolve in response to change. This is a very broad question with implications for understanding how all sexually reproducing populations will respond to the challenges of environmental change.

Although sexual selection was originally conceived to explain traits that appeared to reduce survival, it also has the potential to accelerate adaptation. If males that are well adapted to the environment have increased mating success, then genes that contribute to this adaptation will proliferate, both through their naturally selected contributions to survival (because well adapted males live longer and can perform better) and through their sexually selected contributions to reproduction (for instance because the males that are better adapted to the environment also mate at a higher rate). There have been laboratory based studies that address the question of whether sexual selection will tend to accelerate or retard adaption, but they give conflicting results. What is lacking is an experimental study that retains the natural context: it is this context that imposes the true costs and benefits of sexual selection.

Understanding the interactions between natural and sexual selection in the process of ecological adaptation is not only a fundamentally important issue in evolutionary biology, but also has implications for understanding how populations will adapt to changing environments. For example, if sexual selection accelerates adaptation this suggests that populations should be managed to allow sexual selection to occur.

We will conduct experiments on a natural population of crickets, utilising our 'WildCrickets' project - a long term study of a meadow in Spain. This project has the unique capacity to provide detailed information about the lives of every individual in the population through a network of 160 digital video cameras and annual DNA fingerprinting.

We will replace all the males in the population with males bred from other populations so that half come from populations that are similar to our meadow and half come from high altitude where conditions are very different. For sexual selection on males to reinforce natural selection, it is a requirement that less well adapted males have reduced expression of male sexually selected traits and mating rate. This is a very simple assumption and many biologists probably regard it as uncontroversial, but in reality, it has only been tested in a very limited way in either the field or the lab. Fundamentally, we lack a clear test of this assumption and the arising major prediction that sexual selection increases adaptation. A strong test requires an experiment that directly compares well adapted and less well adapted males over the entire adult lifespan. We will make the comparison, measuring the expression of sexually selected traits, the realised reproductive success of males and the naturally selected success of their offspring. We will do this by using our video cameras to monitor the entire adult lives of the introduced crickets and the females left in the meadow and then coming back the next season and doing the same with their offspring. By using DNA fingerprinting we will know which offspring come from which males. Only males with some success in gaining fertilisations will leave any offspring, but there will still be variation in success amongst fathers, allowing us to compare the longevity and activity of individuals whose fathers were successful in sexual selection with offspring of males that were less successful.

Planned Impact

This project investigates fundamental questions about how new adaptations are established in natural populations. With environmental change occurring very rapidly, it is essential that we understand the factors that may facilitate or constrain the capacity of populations to thrive. If sexual selection accelerates adaptation this suggests that populations should be managed to allow sexual selection to occur; for instance culling regimes in managed animal populations often target the largest males, which may slow down the rate at which the population can adapt. Alternatively, if sexual selection retards adaptation, then management regimes in which a majority of males are removed from the breeding pool, or even where the most attractive males are selectively removed may be better in terms of allowing adaptive evolution to occur. We do not anticipate being able to make specific recommendations at the end of this grant, but it is clear that our findings will have implications for wildlife managers and policy makers in the near future, and we will work hard to publicise them as widely as possible.

The general public, particularly school pupils and teachers will benefit from this research as a result of our planned impact activities: Our study will generate very high quality video recordings of the cricket population studied, and we intend to exploit this resource for the purposes of wider user engagement, with the purpose of providing a high quality learning resource. We have developed a website aimed at the general public which explains the motivations and findings of our project (www.wildcrickets.org). We will develop this site and associated materials in collaboration with digitalexporer.com to produce a package of materials for teachers. Our study will be used to help students learn about natural and sexual selection, and how they affect the capacity of organisms to adapt to changes in the environment. We will add live video feeds from the meadow, with multiple camera feeds available during the breeding season.

We have developed a website which allows the general public to take part in our research: cricket-tales.exeter.ac.uk allows the public to assist in our task of analysing field cricket behaviour. Using technology to involve people in the research in this way disseminates knowledge about animals and habitats, strengthens understanding of the scientific process and engages people in a deeper way. We will further develop this site with a particular aim of engaging older people in our research.

Our study utilises novel video-based monitoring technology which has many and varied applications and commercial value. By pioneering new applications of this technology this work will be of direct benefit to the CCTV Industry including both hardware manufacturers and software developers. We have been collaborating with i-code systems (www.icode.co.uk/), who have used our input to substantially develop their software and have sold systems to other academic users in the US and NZ as a direct result of the impact of our work on the development of their product. If our impact pathway is funded we will work with i-code to add audio recording to their product, which will contribute to the economic performance of the UK in this potentially major export market.

We can demonstrate a strong commitment to bringing our work to as wide an audience as possible (e.g. Google "Chivalrous Crickets"). Our work has been included in BBC and Discovery Channel broadcasts, national newspapers etc. and we will continue to ensure that we use these avenues to promote our NERC-funded science with support from the university's Press Office.

The Researcher-CI on this project will benefit from acquiring a broad range of skills, including deploying monitoring systems, database design, data analysis etc. We will ensure that he has the opportunity to develop his awareness and skills in knowledge exchange.

Publications

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Tregenza T (2022) Environment and mate attractiveness in a wild insect. in Behavioral ecology : official journal of the International Society for Behavioral Ecology

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Rodríguez-Muñoz R (2019) Testing the effect of early-life reproductive effort on age-related decline in a wild insect. in Evolution; international journal of organic evolution

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Rodríguez-Muñoz R (2019) Slower senescence in a wild insect population in years with a more female-biased sex ratio. in Proceedings. Biological sciences

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Rodríguez-Muñoz R (2019) Comparing individual and population measures of senescence across 10 years in a wild insect population. in Evolution; international journal of organic evolution

 
Description We quantified genetic divergence and clustering of ten populations of the field cricket Gryllus campestris in the Cantabrian Mountains of northern Spain. Our populations were chosen to represent replicate high and low altitude habitats. 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.
Exploitation Route Our findings provide insights into the extent to which insect populations are likely to cope with changing climates
Sectors Environment

URL https://onlinelibrary.wiley.com/doi/full/10.1111/jeb.13911
 
Description An individual-level approach to understanding responses to climate in wild ectotherms
Amount £649,368 (GBP)
Funding ID NE/V000772/1 
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 09/2021 
End 09/2024
 
Title Actuarial and phenotypic senescence in a wild field cricket (Gryllus campestris) population in North Spain (2006 to 2016) 
Description Data comprise monitoring records of a population of Gryllus campestris, a flightless, univoltine field cricket that lives in and around burrows excavated among the grass in a meadow in Asturias (North Spain). The area has an altitude range from around 60 to 270 metres above sea level. The data include birth and death days, age at capture, air temperature and calling activity. Data were collected from 2006 to 2016. 
Type Of Material Database/Collection of data 
Year Produced 2019 
Provided To Others? Yes  
 
Title Chill coma recovery times and growth rates of early instar nymphs from populations of crickets (Gryllus campestris) from Northern Spain 
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 http://datadryad.org/stash/dataset/doi:10.5061/dryad.j9kd51ccx
 
Title Data from: Telomere length is highly heritable and independent of growth rate manipulated by temperature in field crickets 
Description Many organisms are capable of growing faster than they do. Restrained growth rate has functionally been explained by negative effects on lifespan of accelerated growth. However, the underlying mechanisms remain elusive. Telomere attrition has been proposed as a causal agent and has been mostly studied in endothermic vertebrates. We established that telomeres exist as chromosomal-ends in a model insect, the field cricket G. campestris, using terminal restriction fragment and Bal 31 methods. Telomeres comprised TTAGGn repeats of 38kb on average, more than four times longer than the telomeres of human infants. Bal 31 assays confirmed that telomeric repeats were located at the chromosome-ends. We tested whether rapid growth between day 1, day 65, day 85, and day 125 is achieved at the expense of telomere length by comparing nymphs reared at 23°C with their siblings reared at 28°C, which grew three times faster in the initial 65 days. Surprisingly, neither temperature treatment nor age affected average telomere length. Concomitantly, the broad sense heritability of telomere length was remarkably high at ~100%. Despite high heritability, the evolvability (a mean-standardized measure of genetic variance) was low relative to that of body mass. We discuss our findings in the context of telomere evolution. Some important features of vertebrate telomere biology are evident in an insect species dating back to the Triassic. The apparent lack of an effect of growth rate on telomere length is puzzling, suggesting strong telomere length maintenance during the growth phase. Whether such maintenance of telomere length is adaptive remains elusive and requires further study investigating the links with fitness in the wild. 
Type Of Material Database/Collection of data 
Year Produced 2021 
Provided To Others? Yes  
URL http://datadryad.org/stash/dataset/doi:10.5061/dryad.jdfn2z39z
 
Title Life history of a wild field cricket population (Gryllus campestris) in North Spain (2006 to 2016) 
Description Data comprise monitoring records of a population of Gryllus campestris, a flightless, univoltine field cricket that lives in and around burrows excavated among the grass in a meadow in Asturias (North Spain). The area has an altitude range from around 60 to 270 metres above sea level. Data include basic traits, behavioural data, genotypes and pheromones. Data were collected from 2006 to 2016. 
Type Of Material Database/Collection of data 
Year Produced 2019 
Provided To Others? Yes  
 
Title Male behaviour in a wild field cricket (Gryllus campestris) population in North Spain, 2019 
Description The data provide information on a number of male cricket behaviours organized according to time and duration of the behaviour. Also included are the mean temperature at the ground level for the duration of each observation. 
Type Of Material Database/Collection of data 
Year Produced 2022 
Provided To Others? Yes  
URL https://catalogue.ceh.ac.uk/id/f56d3d1c-28f2-4667-90b0-ef352243dd2a
 
Title Trade-off between reproduction and body maintenance in a wild field cricket (Gryllus campestris) population in North Spain (2006 to 2016) 
Description Data comprise monitoring records of a population of Gryllus campestris, a flightless, univoltine field cricket that lives in and around burrows excavated among the grass in a meadow in Asturias (North Spain). The area has an altitude range from around 60 to 270 metres above sea level. The data present information on various mating-related activities of male crickets, including age, singing activity, dominance in fights, and lifespan. Data were collected from 2006 to 2016. 
Type Of Material Database/Collection of data 
Year Produced 2019 
Provided To Others? Yes  
 
Description Aarhus University 
Organisation Aarhus University
Country Denmark 
Sector Academic/University 
PI Contribution I have been collaborating on developing analytical approaches to understanding the role of genetic and nongenetic variants in modulating phenotypes. This is central to our knowledge of adaptive responses to local conditions and environmental change, particularly in species with such low population genetic diversity that it is likely to limit their evolutionary potential. With colleagues the University of Aarhus we have carried out environmental association studies that represent a first step towards uncovering the molecular mechanisms underlying population-specific responses to the environment.
Collaborator Contribution They have collected the data that we used in the project.
Impact We have published two papers: Aagaard, A., Liu, S., Tregenza, T., Braad Lund, M., Schramm, A., Verhoeven, K. J. F., Bechsgaard, J. & Bilde, T. 2022. Mol. Ecol. Adapting to climate with limited genetic diversity: Nucleotide, DNA methylation and microbiome variation among populations of the social spider Stegodyphus dumicola. https://doi.org/10.1111/mec.16696 Tregenza, T., Rodríguez-Muñoz, R., Boonekamp Jelle, J., Hopwood, P., E., Sørensen, J., G., Bechsgaard, J., Settepani, V., Hegde, V., Waldie, C., May, E., Peters, C., Pennington, Z., Leone, P., Munk, E., M., Greenrod, S., TE., Gosling, J., Halliwell, L., Coles, H., Gruffydd, R., Capria, L., Potter, L. & Bilde, T. 2021. Evidence for genetic isolation and local adaptation in the field cricket Gryllus campestris. J. Evol. Biol. 34, 1624-1636. DOI: 10.1111/jeb.13911
Start Year 2020
 
Description Cricket Tales at the Eden Project 
Form Of Engagement Activity Engagement focused website, blog or social media channel
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact We developed a citizen-science game "Cricket Tales" and installed it on a publically accessible terminal at "The Eden Project" in Cornwall on the 29/3/2019 in their 'invisible worlds' public engagement area. Photographs of the installation can be seen here https://www.flickr.com/photos/foam/albums/72157707613925095. The game educates the public about how scientsts collect dta is designed to allow players to collect data on the daily activity patterns of a population of wild crickets in a meadow in Northern Spain. The game serves players with 30 second video sequences and invites them to record changes in the position of the cricket, the weather and how often the cricket moves in and out of its burrow. The game allows players to repeatedly record data from the same cricket on 5 occasions, and provides players with a simple analysis of the behaviour of the cricket they have studied in comparison with the data we have from other players.
Year(s) Of Engagement Activity 2019,2020,2021,2022
URL http://cricket-tales.ex.ac.uk/
 
Description Development of engagement focussed website: WildCrickets.org 
Form Of Engagement Activity Engagement focused website, blog or social media channel
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact We built and have subsequently continued to develop, a website "WildCrickets.org" providing public facing information about our project's aims, methods and outcomes. The site includes numerous videos, photographs, participatory games etc. There is a YouTube Channel "WildCrickets" associated with the site which hosts video relating to our work.
Year(s) Of Engagement Activity 2014,2015,2016,2017,2018,2019,2020,2021,2022,2023
URL http://www.wildcrickets.org