The genomics of thermal adaptation in a model pest insect

Lead Research Organisation: University of East Anglia
Department Name: Biological Sciences

Abstract

One sixth of the world's crop production is lost to pests and diseases each year. Rises in global temperatures are expected to cause dramatic shifts in the range and abundance of food pests, with potentially alarming consequences for global food supplies. To protect food security in the context of a changing climate therefore requires multidisciplinary research into how pest species adapt to their environments, drawing from the fields of molecular biology, genetics, ecology and evolutionary biology. Understanding how organisms adapt to high temperature is especially important, as temperature increases affect organisms in a wide range of ways, from their DNA to their complex social behaviours.

Combining the principles of Darwinian evolution with DNA sequencing is an excellent way of studying how pests adapt to temperature. Pest species usually have very short life-cycles, so can evolve rapidly in response to changing temperatures. Studying how pests evolve in response to temperature using DNA sequencing is a promising way forward because i) many of the characteristics and processes thought to be important for how pests adapt to temperature, such as body size, development and stress response, have a genetic basis; and ii) it will enable us to identify new genes, and new biological processes, involved in adapting to climate. At present, however, we know very little about what kinds of genes are involved in adapting to temperature, and less still about how rapidly these genes can evolve and allow pests to spread.

I will study how food pests adapt to temperature. My study organism will be the red flour beetle, a major pest of stored grain that causes enormous amounts of wheat, rice and corn to be discarded each year. It is also a "model species" for DNA research, with detailed genetic information available, and is easy to rear and study in the laboratory. I will study how red flour beetles evolve in response to extreme temperatures in real time, using replicated populations that have been maintained in the laboratory at high temperature for 60 generations. By sequencing the genomes of individual flour beetles adapted to living at extreme temperatures, I will identify the genes and biological processes that govern adaptation to temperature, and find out how these genes interact with one another. Additionally, because I have samples available from every generation since this experiment was set up, I will be able to look at how genes involved in adaptation to temperature evolve over time, and in doing so determine how rapidly these important genes can respond to changing temperature.

The proposed research will give us a better understanding of how DNA enables individuals and populations adapt to their environments. And, importantly, it will help us generate better predictions of where and when food pests are likely to spread as the global climate continues to change.

Technical Summary

Understanding how pests adapt and respond to temperature at a genetic level is essential for maintaining food security in a changing climate. Changes in environmental temperature are expected to result in adaptive changes in genetically controlled traits, so determining the mechanistic basis of these changes will significantly improve models of when and where pest species are likely to spread. However, we still lack fundamental understanding of what types of genes and biological processes are involved in adapting to climate, how rapidly organisms are able to temperature from standing variation, and how genetic architecture influences adaptation to climate.

I will study the genomic basis of adaptation to temperature in the red flour beetle (Tribolium castaneum), a globally significant pest of stored products that is predicted to spread dramatically due to climate change. T. castaneum is also a model organism for genetic and developmental research, with a well annotated reference genome. I will use long-term, controlled selection lines that will have been maintained at high temperature for 60 generations. I will sequence individual genomes from these lines using a novel and cost-effective library preparation technique combined with low coverage sequencing. Using these data I will test how natural selection from extreme temperature shapes patterns of genomic variation in real time, and identify how linkage among genes, for example due to chromosomal inversions, influences genomic responses to extreme temperature. I will then use time-series analysis to map trajectories of genetic regions involved in adaptation to temperature, and determine how rapidly these key genetic regions evolve under natural selection. Finally, I will use experimentally manipulated gene flow to break up associations between genes under selection and linked neutral sites, which will enable me to identify the genes and biological processes involved in adaptation to temperature.

Planned Impact

This proposal has potential for significant impact, both in terms of content and reach. First, because T. castaneum is an economically significant pest insect, research into the mechanistic basis of adaptation to temperature has potential benefits for industry in terms of pest management. Second, using a model insect to understand adaptation to temperature has important implications for how invasive species, as well as species of conservation concern, may respond to climate change. This proposal is therefore of relevance to conservation organisations and charities. Finally, this proposal is relevant to the general public, who are highly interested in both evolution and climate change, but are rarely exposed to how these two fields are inextricably linked.

I will register for schemes to interact with local schools, the public and policy makers (e.g. the Royal Society's pairing scheme). I will also organise a one-day symposium called "Controlling stored product pests: evidence-based approaches", with invited talks from pest-management companies, local authorities and academics. Finally, I will create a public performance, called 'Sex, Death and Global warming', which will take an informal approach to explaining the importance of evolution in the global warming debate, in an accessible way. I will present this talk at UEA, local venues, and national 'Skeptics in the Pub' meetings. I will accompany the talk with a series of non-academic articles on aspects of evolution and climate change, to be pitched to leading popular science publications. I have experience in communicating science to a wide range of non-academic audiences, both orally and in writing. This experience, combined with the excellent facilities for delivering impact at UEA, will ensure that the proposed activities reach their full potential.

Publications

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Carleial R (2020) Temporal dynamics of competitive fertilization in social groups of red junglefowl (Gallus gallus) shed new light on avian sperm competition. in Philosophical transactions of the Royal Society of London. Series B, Biological sciences

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Leftwich PT (2021) Genetic pest management and the background genetics of release strains. in Philosophical transactions of the Royal Society of London. Series B, Biological sciences

 
Description We have discovered that, in an insect pest, early-life development is the most important way in which individuals and populations adapt to increased temperature. Specifically, we have found that experimental evolution lines adapted to high temperatures differ from control populations primarily in their developmental trajectories. Populations adapted to high temperature have massively increased levels of adult fertility compared to control populations when exposed to high temperature during the juvenile phase. However, this adaptation is costly, and overall levels of reproduction in adapted lines are lower than control populations at optimum temperatures. We are now honing in on the exact mechanism behind this adaptation, including identifying the genes involved in adaptation.

In 2018-2019, we have discovered that the mechanism behind the effect of high temperature on reproductive development lies in reproductive morphology. High temperature during the developmental, but not adult, phase results in impaired development of the reproductive organs in a manner not yet demonstrated in insects. We are now finishing up analyses and preparing manuscripts for publication, and honing in on the genetic basis of this these effects.
Exploitation Route We hope to identify key genes and phenotypes that enable development at high temperature. These may be useful in the future for pest control, via RNAi, or gene drive.
Sectors Agriculture, Food and Drink,Retail

 
Description I helped my PhD student draft a talk on pest ecology for a regional farmers conference. This included information on pests and climate change, including results from the current project. I ran a public exhibition called "Nature's dazzling diversity", highlighting the benefits and problems facing biodiversity, including findings from the fellowship research. This was exhibited at Latitude Festival and Norwich Science Festival
Sector Agriculture, Food and Drink,Environment
Impact Types Cultural,Societal,Economic

 
Description Population genomics course Canada
Geographic Reach North America 
Policy Influence Type Influenced training of practitioners or researchers
 
Description Population genomics course Germany
Geographic Reach Europe 
Policy Influence Type Influenced training of practitioners or researchers
 
Description NRP DTP
Amount £70,000 (GBP)
Organisation Norwich Research Park 
Sector Private
Country United Kingdom
Start 10/2019 
End 10/2023
 
Description NRP DTP
Amount £70,000 (GBP)
Organisation Norwich Research Park 
Sector Private
Country United Kingdom
Start 10/2017 
End 10/2021
 
Description NRP Science Links Seed Fund
Amount £14,914 (GBP)
Organisation Norwich Research Park 
Sector Private
Country United Kingdom
Start 01/2017 
End 12/2018
 
Title Data from: Genomic variation, population history and within-archipelago adaptation between island bird populations 
Description Oceanic island archipelagos provide excellent models to understand evolutionary processes. Colonisation events and gene flow can interact with selection to shape genetic variation at different spatial scales. Landscape-scale variation in biotic and abiotic factors may drive fine-scale selection within islands, while long-term evolutionary processes may drive divergence between distantly related populations. Here, we examine patterns of population history and selection between recently diverged populations of the Berthelot's pipit (Anthus berthelotii), a passerine endemic to three North Atlantic archipelagos. First we use demographic trees and f3 statistics to show that genome-wide divergence across the species range is largely shaped by colonisation and bottlenecks, with evidence of very weak gene flow between populations. Then, using a genome scan approach, we identify signatures of divergent selection within-archipelagos at SNPs in genes potentially associated with craniofacial development and DNA repair. We did not detect within-archipelago selection at the same SNPs as were detected previously at broader spatial scales between archipelagos, but did identify signatures of selection at loci associated with similar biological functions. These findings suggest that similar ecological factors may repeatedly drive selection between recently separated populations, as well as at broad spatial scales across varied landscapes. 
Type Of Material Database/Collection of data 
Year Produced 2020 
Provided To Others? Yes  
URL http://datadryad.org/stash/dataset/doi:10.5061/dryad.pc866t1kt
 
Title Data from: Temporal dynamics of competitive fertilization in social groups of red junglefowl (Gallus gallus) shed new light on avian sperm competition 
Description Studies of birds have made a fundamental contribution to elucidating sperm competition processes, experimentally demonstrating the role of individual mechanisms in competitive fertilisation. However, the relative importance of these mechanisms and the way in which they interact under natural conditions remain largely unexplored. Here, we conduct a detailed behavioural study of freely-mating replicate groups of red junglefowl, Gallus gallus, to predict the probability that competing males fertilise individual eggs over the course of 10-day trials. Remating frequently with a female and mating last increased a male's probability of fertilisation, but only for eggs ovulated in the last days of a trial. Conversely, older males, and those mating with more polyandrous females, had consistently lower fertilisation success. Similarly, resistance to a male's mating attempts, particularly by younger females, reduced fertilisation probability. After considering these factors, male social status, partner relatedness and the estimated state of a male extragonadal sperm reserves did not predict sperm competition outcomes. These results shed new light on sperm competition dynamics in taxa such as birds, with prolonged female sperm storage and staggered fertilisations. 
Type Of Material Database/Collection of data 
Year Produced 2020 
Provided To Others? Yes  
URL http://datadryad.org/stash/dataset/doi:10.5061/dryad.cz8w9gj1d
 
Description Farmers conference 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Industry/Business
Results and Impact My PhD student Siobhan Hillman presented a talk on "the ecology of pests" at a regional level farming conference organised by the NFU and British Sugar. The aim was to raise awareness of the importance of understanding the biology, life history and ecology of pests, as a prerequisite to control. Impact was monitored via a survey, in which farmers responded that they had increased levels of support for research into pest ecology.
Year(s) Of Engagement Activity 2018
 
Description Festival exhibition 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact I led a public facing exhibition called "Nature's dazzling diversity", which highlighted the benedifts and problems facing the natural world. This was exhibited at Latitude Festival (70,000 attendees) and Norwich Science Festival (~2000 attendees). Attendees directly interacted with exhibitions, asked questions, and were able to make badges to take away. Feedback on social media and via email was overwhelmingly positive.
Year(s) Of Engagement Activity 2019