Life history and Ageing in the wild

Lead Research Organisation: University of Exeter
Department Name: Biosciences

Abstract

The study of why we, and all other living things, progressively deteriorate and become more likely to die as we get older is an issue of relevance to almost every other question in biology. However, the vast majority of ageing research is concerned with mechanistic explanations for declines in function. We have only really scratched the surface in terms of functional explanations for why ageing occurs in the first place, and we are even more in the dark in relation to how ageing proceeds in natural populations. We need to understand ageing in the wild, because it is clear that how ageing works in nature will affect the dynamics of key process such as sexual selection and the evolution of life-histories.

Insects make up the vast majority of animal biodiversity and have been studied intensively in the lab, where they have become important model systems for understanding ageing. However, it seems very likely that when they are taken out of an environment where they have unlimited food and no parasites or predators, insects may show different patterns of senescence. It is now clear that even short lived insects experience senescence on the timescales of their natural life-spans. The importance of insects as laboratory systems for understanding ageing, and the potential for developing a model that can be studied in both field and lab makes understanding ageing in wild insects an exciting prospect. We will carry out a study of senescence in a natural population of field crickets by monitoring the population in great detail. We will DNA fingerprint and tag every individual, and then observe them 24 hrs a day using a network of 160 video cameras. This will enable us to not only measure lifespan and reproduction, but also to collect detailed behavioural information, allowing us to detect what may be quite subtle declines in performance in traits like singing, movement around their burrow, movement over longer distances, mating rate, success in fights with other individuals etc.

By combining the data we will collect during this project with data we have collected over the previous 6-8 years, we will address a series of questions which have been very difficult to answer in the wild because other studies have not had the detailed information that we have:

1. The main evolutionary explanation for ageing is that individuals deteriorate because they pass on more genes by putting all their energy into reproduction early in life even if this takes its toll later in life. We will determine whether individuals that put more effort into early reproduction, for instance by mating more, end up declining faster.

2. We will determine whether environmental conditions affect how rapidly individuals age, and whether years which are more stressful due to climate and competition among individuals are associated with more rapid senescence.

3. Males have been predicted to age faster than females because their reproductive rate isn't capped by how fast they can lay eggs; so they have more potential to evolve to invest heavily in early reproduction even if it kills them. We will see if our males age faster than our females.

4. Females may benefit from mating with old males because their offspring get genes from a male that was able to survive a long time. If males with good genes age slower than males with poorer genes then ageing will make female choice for old males even more beneficial. We will test whether males with other signs of good genes also age slower.

5. It has been suggested that different sources of mortality will have different effects on the evolution of ageing depending on whether they can be avoided by individuals in better condition. We will determine whether the sources of mortality in our population vary in this respect. For instance, whether you get eaten by a robin may simply be a matter for luck, whereas being killed by another cricket may depend on how able you are to defend yourself.

Planned Impact

This project investigates fundamental questions about the evolutionary biology of ageing. It is largely curiosity-driven, although clearly the experience of ageing in human populations means that we are contributing to understanding an issue of great significance to most people. To understand ageing properly we will need to understand it in an ecological and evolutionary context, which is the aim of this proposal. In the longer term, this will benefit all those likely to experience ageing.

The study utilises novel video-based monitoring technology which has wide application and potential 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. We expect continued impact of this sort contributing to the economic performance of the UK in this potentially major export market.

We have an established partnership with Ruthern Instruments (based in Bodmin, Cornwall) and have worked with this company to develop an automated multi-channel acoustic monitoring device. The latest version of this device is more flexible and cheaper to manufacture than previous models and Ruthern have now sold several units to other users. We intend to build on this experience to integrate our acoustic monitoring and IP camera system and develop further systems which have commercial potential.

The researcher co-investigator on this project will benefit from acquiring skills across a broad range of areas, including deploying monitoring systems, database design, data analysis etc.
We will ensure that the named PDRA is provided with the opportunity to develop their awareness and skills in knowledge exchange as detailed in our pathways to impact.

The technician on the project will gain new skills in a wide range of areas through their work in analysing video data and collecting data in the field.

The general public 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 cricket-meadow project (www.wildcrickets.org). We will develop this site and associated materials to focus on the use of our system to understand ageing in natural populations, and concepts about selection and trade-offs in life history traits. We will add live video feeds from the meadow, with multiple camera feeds available during the breeding season and a simple web-cam type live overview available year around. We will facilitate public participation in research using a citizen science approach to the task of analysing field cricket behaviour. Using technology to involve people in the research in this way creates beneficiaries; disseminating knowledge about the animals and habitats strengthens understanding of the scientific process and engages people in a deeper way as they feel their effort is valued and contributes to something worthwhile.

Publications

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Fisher DN (2015) Dynamics of among-individual behavioral variation over adult lifespan in a wild insect. in Behavioral ecology : official journal of the International Society for Behavioral Ecology

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Fisher DN (2016) Comparing pre- and post-copulatory mate competition using social network analysis in wild crickets. in Behavioral ecology : official journal of the International Society for Behavioral Ecology

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Fisher DN (2016) Wild cricket social networks show stability across generations. in BMC evolutionary biology

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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) Comparing individual and population measures of senescence across 10 years in a wild insect population. 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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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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Tyler F (2015) Chemical cues mediate species recognition in field crickets in Frontiers in Ecology and Evolution

 
Description Our research has demonstrated that short-lived insects living in their natural environment "get old" - losing some of their physical abilities - before they die. Very few studies have examined whether insects such as field crickets - whose adult life lasts a few weeks - experience "ageing" (senescence) in the sense of physical decline in nature.
Insects have been used extensively to study ageing in laboratories, but it was not clear whether they only reach "old age" because they are protected from a harsh natural environment. We used a network of more than 130 video cameras to study every hour of the lives of a population of wild crickets in a Spanish meadow. We monitored reproductive effort, ageing and survival, combining the data from this project with data from previous NERC funded projects to create a ten year data set that enabled us to examine patterns of senescence across multiple years, each with a completely independent generation of wild crickets. This has allowed us to test a number of key predictions in relation to senescence in nature. Amongst our key findings are:

1. Senescence is typically characterised via assessments of the rate of change in mortality with age (actuarial senescence) or the rate of change in phenotypic performance with age (phenotypic senescence). While both phenomena are considered indicative of underlying declines in somatic integrity, whether actuarial and phenotypic senescence rates are actually correlated has yet to be established. Our study provides evidence of both actuarial and phenotypic senescence in our cricket population, suggesting similar processes occur in other wild invertebrates.
2. Both actuarial and phenotypic senescence vary substantially across ten annual generations. This variation allows us to identify a strong correlation between actuarial and phenotypic measures of senescence. Our study demonstrates age-related phenotypic declines at the individual level are reflected in population level mortality rates and reveals that observations of senescence in a single year may not be representative of a general pattern.
3. We did not find evidence of a strategy of 'live fast, die young' where those that put more energy into reproduction die earlier: There was no strong evidence of a "trade-off" between reproductive effort in early life (measured by emergence date, calling, searching and winning fights) and survival.
4. Although a reproductive-effort versus lifespan tradeoff was not apparent, there was evidence that individuals that invested more in reproduction in early life show signs of "ageing" - chirping less and losing more fights. However, the relationship was weaker than has been identified in large vertebrates. This suggests that organisms with multiple discrete breeding seasons may have greater opportunities to express trade-offs between reproduction and senescence.
Exploitation Route Our findings provide basic knowledge about the evolutionary biology of ageing; clearly the experience of ageing in human populations means that we are contributing to understanding an issue of great significance to most people. To understand ageing properly we will need to understand it in an ecological and evolutionary context, which our project has contributed towards. Our findings, model system and the techniques that we developed will be of interest to a wider user has wide application.
To bring our work to the attention of the public we have developed a Citizen Science Game "Cricket Tales"

http://cricket-tales.ex.ac.uk/

This game allows the public to take part in our research and provides education on the general themes around our project. As we have now begun a new NERC project utilising our WildCrickets system, the cricket-tales game is being re-developed, but it will continue to collect data that relate to ageing.
Sectors Education

URL http://www.wildcrickets.org/
 
Description To bring our work to the attention of the public we have developed a Citizen Science Game "Cricket Tales" http://cricket-tales.ex.ac.uk/ This game allows the public to take part in our research and provides education on the general themes around our project. As we have now begun a new NERC project utilising our WildCrickets system, the cricket-tales game is being re-developed, but it will continue to collect data that relate to ageing. In its previous incarnation, Cricket-Tales engaged with thousands of players who collectively watched 30,000 hours of video and reviewed educational material relating to senescence and evolutionary ecology
First Year Of Impact 2018
Sector Education
Impact Types Cultural

 
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 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 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 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