Natural and sexual selection in a wild insect population

Lead Research Organisation: University of Exeter
Department Name: Biosciences

Abstract

To understand why animal populations change in size and distribution and why individuals behave as they do, it is essential to understand how evolution occurs. Over the past few decades a real success story in the study of ecology has been the long-term studies of mammals and birds where it has been possible to follow individuals and their offspring and their offspring's offspring and so on. The ability to measure individual success in passing on their genes has enabled researchers to address questions about how particular traits affect reproductive success and hence drive evolution. For instance, studies of Darwin's finches have been able to demonstrate evolution occurring because particular beak shapes are beneficial under particular climatic conditions. We propose to add a completely new field system to the handful of mammals and birds which have thus far been thoroughly studied in nature. We will use a network of digital video cameras and microphones to monitor a population of individually marked field crickets in a Spanish meadow. Crickets have been well studied in the laboratory, revealing that they have complex forms of sexual selection whereby females choose between males according to their songs, males fight, females manipulate sperm from several males to favour unrelated males and so forth. However, although we now have many insights into the behaviour and physiology of crickets in the laboratory, we have almost no idea how important these various aspects are in the real world. This discrepancy is a source for concern: Laboratory situations remove some sources of selection that may be very important in wild populations and may create new pressures; for instance, it may be that males that sing louder get more mates in the lab, but in the field such males may be more likely to be eaten by birds. These issues with crickets are shared with almost all other model systems: without exception the species that are well studied in the field are too difficult to study in the lab (e.g. Red Deer, Great Tits), and the species that are well studied in the lab are poorly studied in the field (e.g. Fruit Flies, Stalk Eyed Flies). What is desperately needed is a system that bridges this divide. Advances in technology mean that such a study is now possible. We propose to use 80 cameras to monitor the majority of activity occurring in a small population of crickets: who mates with whom, who wins fights, how much each males sings, how long individuals live and so on. This will be combined with DNA sampling of every adult in the population which will allow us to work out how many offspring each individual leaves in the next generation of adults. Simulations based on our genetic markers show that our pedigree will be at least as reliable as those used in the text-book studies of large vertebrates. The combination of monitoring and parentage assignment will allow us to address some key questions in evolutionary ecology: 1. Do males depend more on their ability to get matings than their ability to survive? 2. Do males vary more in their reproductive success than females? 3. Is male mating success due to them being attractive to females or good at fighting with other males? 4. Do males that devote a lot of effort to getting matings pay a price in terms of shorter lifespan? 5. Do females that mate with attractive males have healthier or more attractive offspring? 6. Are there some genes that are beneficial for one sex but detrimental to the other? 7. Do lab based estimates of the inheritance of traits match estimates made in the field? 8. Do related insects ever meet and if they do, do they mate with one another? Answering these questions in crickets will provide insights across species and provide crucial insights into the validity of a central paradigm of modern biology which is that we can do behavioural ecology in the lab.

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) Wild cricket social networks show stability across generations. in BMC evolutionary biology

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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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Hosken DJ (2009) Monogamy and the battle of the sexes. in Annual review of entomology

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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 (2010) Natural and sexual selection in a wild insect population. in Science (New York, N.Y.)

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Rodríguez-Muñoz R (2011) Guarding males protect females from predation in a wild insect. in Current biology : CB

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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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Schuett W (2010) Sexual selection and animal personality. in Biological reviews of the Cambridge Philosophical Society

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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

 
Description Our scientific objectives have all been met or else we are waiting to augment our data-set before publishing our findings in relation to these objectives:

1. The relative importance of natural vs. sexual selection in a wild population. (Determine offspring in next generation, longevity, causes of mortality, mating success, sexual signals.) We have achieved this objective as described in Rodríguez-Muñoz et al Science 2010. 328, 1269-1272 (hereafter RRM 2010)

2. Whether males vary more in LRS than females. (Use pedigree to compare variance in offspring surviving to adulthood between males and females). We have achieved this objective as described in RRM 2010.

3. Within sexual selection, relative importance of male competition vs. female choice. (Compare calling effort, call structure and success in fights, with reproductive success. Look for possible alternative mating tactics in males and heritability / condition dependence of these tactics). We have achieved this objective in that we demonstrated a relationship between male fighting behaviour (dominance) and calling behaviour (RRM 2010) we are continuing to analyse our data to determine whether there are alternative mating tactics in males.

4. The extent to which sexually selected traits are subject to naturally selected costs. (Compare longevity, causes of mortality between males differing in call effort and song structure). We have achieved this objective as described in RRM 2010.

5. Determine whether females gain indirect benefits from mate choice. (Determine whether females mating to males with high calling effort or song quality have offspring with high reproductive success). We are in the process of analysing our data to answer this question, we have demonstrated that females that mate to more males have higher fitness (RRM 2010). We also published a major review of the role of personality in sexual selection (Schuett et al 2010)

6. Evidence for sexually antagonistic alleles (intra-locus sexual conflict) (Determine whether there is a negative correlation between reproductive success of siblings of opposite sex). Our data suggest that such a negative correlation does not exist. However, because support for a negative conclusion is more demanding, we are waiting to collect more data before preparing this for publication.

7. Realised trait heritabilities in wild populations compared with lab measures. (Use pedigree and animal model approach to estimate heritabilities of all traits measured). We have a lot of data relating to this, but we are waiting to combine it with new data from the next 2 years.

8. Do female insects face an inbreeding risk in wild populations and if so, does relatedness affect mating probability? (Use pedigree to determine whether relatives meet, whether they mate, and their subsequent RS). We have achieved this objective and have a manuscript with the journal Molecular Ecology which has been revised following one round of reviewers comments.





Our General objectives to train the two PDRAs were met and both have gone on to subsequent postdoctoral positions with RRM remaining on this project. The new techniques we aimed to develop, we have developed and our Science publication and associated press releases and videos and suchlike attracted a lot of media attention with articles in several major broadsheet newspapers, radio interviews and hundreds of online articles.
Exploitation Route The work we have done on developing software for use in monitoring populations of animals has already resulted in our industrial collaborators (i-code systems) selling their product to at least 2 other research groups, and we are continuing to work with them to develop this



We have developed a website www.wildcrickets.org which is aimed at lay members of the public to help them follow our attempts to understand the natural world. This research has implications for how studies designed to understand behaviour are designed. We are also involved in developing video analysis software to make it fit for the purpose of monitoring tagged wild animals.
Sectors Digital/Communication/Information Technologies (including Software),Education,Electronics,Environment

URL http://www.wildcrickets.org
 
Description This work has yet to make an impact outisde of its original intended outcome of furthering our understanding of the living world. This is an endeavour which will have incalculable impact over the longer term.
First Year Of Impact 2009
Sector Education
Impact Types Cultural