Ecological and evolutionary effects of climate change on rainforest food webs

Lead Research Organisation: University of Bristol
Department Name: Biological Sciences

Abstract

Ecological communities are complex, interacting networks of species, linked by competition, mutualism, predation and parasitism. In the 'Origin of Species', Charles Darwin famously wrote of 'an entangled bank', comprising a bewildering richness of species and an even more complex web of connections among them. Fundamentally, ecologists and evolutionary biologists seek to unravel this complexity, by establishing why species occur where they do, why they replace each other under certain conditions, and how the species interactions that make up ecosystems will change as environments change.

As the climate warms and extreme events become more frequent, existing connections between species are changing in strength, or being severed completely; and new connections are forming as species change in abundance and shift their distributions (e.g. colonising cooler habitats, while becoming locally extinct in warmer habitats). Biologists use information about the range of temperatures where species currently occur to predict where species will occur in a future, warmer world. However, better predictions about the consequences of climate change will be possible if we can also take into account changing interactions between species, as well as the potential for species to evolve to cope with new conditions.

We urgently need to test how whole food webs of interacting species are structured by biological processes (e.g. competition and predation) and by temperature, and how these ecological networks will respond to climate change. It is also important to test the extent to which current adaptive divergence across species' geographical ranges will increase their resilience to future climate change. To achieve this, our project will exploit a unique model system (Drosophila fruit-flies and parasitic wasps that are associated with them, called parasitoids) in a high-diversity ecosystem threatened by climate change (Australian tropical rainforests). With this system we will use field observations, field transplant experiments and mathematical models to test: (i) what determines species' local distributions and food web structure; (ii) the responses of natural and simulated networks of interacting species to simulated climate change; and (iii) the underlying mechanisms driving these changes, including the effects of genetic variation among populations within species and the potential for rapid evolutionary adaptation to warmer temperatures. The outcome will be a better and more predictive understanding of how climate change will affect the biotic interactions that characterise biodiversity and underpin the functions and services of natural ecosystems.

Planned Impact

We have identified three categories of beneficiary:

(1) The General Public:
The UK public has an enormous interest in wildlife, and a particular fascination with rainforests. People are concerned about how biodiversity is responding to climate change, and the future consequences of biodiversity loss for human economies, climate stability, and our health and happiness.

(2) Policy-makers and conservation organisations:
The ability to predict species' responses to climate change is critical for conservation, agriculture and medicine, but the mechanisms governing these responses remain poorly understood. An important knowledge gap concerns the direct influence of climate on species distributions versus its effects via interacting species and habitats. Our work will thus be of interest to policy-makers, landscape-planners and stakeholders in agriculture and medicine who are concerned by how climate change may alter interactions among invertebrates, with relevance for species acting as disease vectors, agricultural pests or invasive alien species in natural and managed landscapes.

(3) Wider society:
By examining the mechanisms driving observed changes to species distributions resulting from climate change, our research will contribute to UK leadership in predicting the regional and local impacts of environmental change. Of particular importance at the moment is defining a safe "operating limit" for key environmental pressures. Of these pressures, there is greatest uncertainty about biodiversity loss, and how it will reduce planetary resilience in the face of anthropogenic climate change. Our research will contribute new data to the evidence base that will empower society to respond to global climate change. It will do this by refining forecasts of how species and ecological communities respond to the interacting effects of climate change and interacting species. In particular, our data will address these issues in tropical rainforests which are the planet's most species-rich ecosystems, and also amongst the most sensitive to climate change.

Publications

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Bridle J (2020) Discovering the limits of ecological resilience. in Science (New York, N.Y.)

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Churchill ER (2021) Social and physical environment independently affect oviposition decisions in Drosophila. in Behavioral ecology : official journal of the International Society for Behavioral Ecology

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Meier JI (2021) Haplotype tagging reveals parallel formation of hybrid races in two butterfly species. in Proceedings of the National Academy of Sciences of the United States of America

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Nadeau CP (2017) Climates Past, Present, and Yet-to-Come Shape Climate Change Vulnerabilities. in Trends in ecology & evolution

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O'Brien EK (2022) Environmental variation and biotic interactions limit adaptation at ecological margins: lessons from rainforest Drosophila and European butterflies. in Philosophical transactions of the Royal Society of London. Series B, Biological sciences

 
Description We have conducted extensive sampling and field transplant experiments along four ecological transects in North Queensland in order to test for (a) the combined effects of climate variation and the density of interacting species on fitness and (b) genetic variation in this effect. This is a test of Darwin's "tangled bank hypothesis" for the evolution of diverse ecological communities. Current findings suggest that there are strong effects of competition within and across species on growth, and that these effects become more intense at higher, or more fluctuating field temperatures. There is genetic variation in the ability to compete at different temperatures, suggesting that these traits have the potential to evolve, as well as some evidence of local adaptation, although it is quite limited. In particular, these data demonstrate that (as predicted by Tangled Bank theory), competition with other species has a bigger effect on fitness at the ecological margins, whereas competition within species has a bigger effect at the centre of the range. This finding has important implications for understanding how ecological communities are structured.

We have conducted additional experiments to investigate the effect of competition on fly behaviour in more detail (funded by a BES project grant). Analysis of these data is underway, but they suggest that these effects are not also seen under lab conditions. However, other important results are suggested, including high levels of sensitivity of these flies to the (former) presence of closely-related species in mating traits.

Results from a second transplant experiment, testing the effect of temperature on resistance to parasitoids, is now being analysed, along with data from metabarcoding experiments. These data show important patterns of fitness variation associated with elevation in the tropics. However, surprisingly, there is little change in the actual structure of host parasitoid networks with elevation (published in Ecography).

A preprint of these initial findings is here (this work is being prepared for submission to Ecology Letters).

O'Brien, E.K., Higgie, M., Jeffs, C.T., Hoffmann, A.A., Hrcek, J., Lewis, O.T. & Bridle, J.R. (2018). Interacting effects of the abiotic and biotic environment on fitness of rainforest Drosophila. bioRxiv. DOI: https://doi.org/10.1101/395624

Additional work has revealed surprisingly low levels of male mating rate, which (even more surprisingly) remain genetically variable despite having major increases in fitness. This work has been submitted for review, and is now being prepared for publication for Behavioural Ecology.

In addition, the PI and PDRA have given talks on these data at the ESEB/SSE conference (2018), and at several University seminars in 2020-1.
Exploitation Route Future discoveries will have implications for understanding ecological resilience and how easily communities will respond to climate change. In particular, the fact that the effects of competition vary at different points in a species range has major consequences for population extinction rates under ongoing climate change.
Sectors Agriculture, Food and Drink,Environment

 
Description The ecological and evolutionary legacy of extreme climatic events for food web resilience
Amount £143,733 (GBP)
Funding ID NE/X000451/1 
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 01/2023 
End 12/2025
 
Title Data on genetic variation in biotic interactions and their effects on fitness at different elevations in rainforest Drosophila 
Description Data from two extensive field transplant experiments, testing for the effect of elevational change on the impact of (a) competition and (b) parasitoids on fitness, and genetic variation in this trait and phenotypes. These data are being prepared for publications. 
Type Of Material Database/Collection of data 
Year Produced 2018 
Provided To Others? No  
Impact These data suggest important effects of inter specific competition on sex ratio, which varies along an elevational gradient 
 
Description Development of international collaborations on trade offs between ecological tolerance, immunity and sexual selection 
Organisation University of Western Australia
Country Australia 
Sector Academic/University 
PI Contribution Initial analyses of data from this grant has revealed evidence for trade-offs between ecological tolerance and sexual selection, indicating that the causes of variance in fitness is driven by sexual success and/or biotic interactions with other species. This has led to JRB developing significant collaborations with Dr Rhonda Snook (University of Sheffield, UK) and Prof Leigh Simmons (UWA, Australia). Both of these collaborations have been cemented by extended visits by the PI and supported by a WUN Fellowship to the PDRA. Additional collaborations to explore the effects of parasites and pathogens were developed with Prof Owen Lewis (Oxford, UK), and Additional potential trade-offs with stress resistance traits in fruitflies is with immunity and generalised resistance to disease. This is being investigated in collaboration with Dr Nick Priest (Bath). One of this PhD students has copies of our isofemale lines (from 2011) to generate pilot data to take this work forward. These collaborations led to a successful application for a University of Bristol scholarship studentship to take this research in this new significant direction from October 2013.
Collaborator Contribution These partners have devoted significant time and resources to running (a) initial analyses of reproductive biology in birchii (sperm number and size, accessory gland size); (b) tests of the effects of heat and cold stress on sperm production and remating ability; (c) analyses of investment in immunity across ecological gradients and variation in parasitoid load.
Impact These efforts have generated important data that led to a MSc project, and an (ongoing) PhD studentship funded by the University of Bristol. Data from these analyses are currently being prepared for publication. They also suggest important new field-based analyses to test how selection works in natural populations faced with temperature stress.
Start Year 2012
 
Description Extension of proposed genomic analysis in collaboration with NBAF Sheffield 
Organisation Natural Environment Research Council
Department NERC Biomolecular Analysis Facility (NBAF)
Country United Kingdom 
Sector Public 
PI Contribution An application to NBAF Sheffield to request technical support and consumables was successful. This has allowed our proposed microsatellite analysis to be extended substantially by the use of next-generation sequencing technology, which should generate data on variation in 1000s of SNP markers across the four ecological transects, rather than 10 microsatellite loci. This approach uses ddRAD technology and required 1000s of DNA extractions of wild-collected males and quality control, as well as preparation of libraries for sequencing at NBAF-Edinburgh. This required the additional investment of six months effort by RAs, as well as additional expense.
Collaborator Contribution Substantial technical expertise, help with planning and experimental design, and provision of consumables. In addition, project partner on the grant (Prof Ary Hoffmann) has generated an annotated genome for Drosophila birchii that will greatly aid interpretation of the results. In addition, his group have shown evidence for inversions at particular loci that correlate with latitude. A key avenue for future investigation is whether these loci also show clinal differentiation with altitude.
Impact ddRAD libraries have been sent for sequencing at Edinburgh, results expected early in 2015.
Start Year 2012
 
Description Collaboration in the creation and dissemination of an artwork 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact I participated in the development of the artwork "Hollow" by Katie Paterson. This included being involved in (a) a public panel debate on art and science at the University to celebrate its opening; (b) participation in an Open Studio during the work's development (c) website interviews and being filmed for a BBC4 documentary (d) a public lecture on science and art in rooms above a Bristol pub and (e) the recording of an audioguide for visitors to the installation.
Year(s) Of Engagement Activity 2016
URL http://www.hollow.org