Testing the limits to evolution: when and why does adaptation fail in response to ecological change?

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

Abstract

Organisms on this planet are currently experiencing unprecedented rates of habitat loss and environmental change. Climate change alone is predicted to condemn at least one in ten of all species to extinction this century unless they can adapt to deal with these changing conditions. Such a high rate of biodiversity loss is likely to have catastrophic effects on the ecological networks that we depend on for food and fuel production, for sustainable development, and ultimately for political stability. There is therefore an urgent need to understand maximum rates of evolution in response to environmental change. This will allow scientists to provide clearer guidance to policymakers and economists on what the consequences of changing climate and habitat loss are likely to be for biodiversity. At species and population margins, limits to adaptation prevent expansion into novel environments. Theoretical models predict that these limits occur either because rates of ecological change become too large relative to the movement of individuals from other populations, or because populations at species' edges lack the genetic variation necessary for adaptation. Extensive preliminary data suggest that the study of Australian rainforest fruitfly populations along repeated altitudinal transitions presents a unique opportunity to distinguish between these hypotheses, and assess which ecological and genetic factors most limit evolutionary potential in nature. The proposed research will explore how levels of genetic variation affect the point where evolution fails along similar altitudinal transitions of varying steepness. It will use field experiments to measure the strength and steepness of these selective gradients from the perspective of the flies themselves, directly estimate rates of movement of individuals, and assess genetic changes in those traits expected to be evolving along these spatial gradients. Estimates of these variables will then be related back to theoretical models to test how well these models predict the maximum rates of evolution observed in real populations. Such information will not only help to identify which species and populations are most at risk of extinction, it will also provide guidance on which strategies can be employed to maximise evolutionary responses in natural populations. This will help to reduce, or plan for, the massive rates of biodiversity loss predicted for the coming centuries.
 
Title Audio interview for video art on Kafka's notes to the academy 
Description Myself and other biologists were interviewed on aspects of evolutionary biology and genetics, to be used as a voice over for a film by artist Monica Oesthler (Spike Island) 
Type Of Art Film/Video/Animation 
Year Produced 2015 
Impact The piece is still in production 
 
Description A fundamental scientific question is how quickly evolutionary change can allow populations to respond to environmental change in space and time. This depends on the distribution and type of genetic variation within populations across their geographical range, and how this variation affects fitness in the environments experienced. We have collected extensive amounts of data on the nature of this variation in 10+ important fitness traits, involving the measurement of 100s of thousands of rainforest fruitflies. Importantly, we have combined these assays of genetic variation with estimates of local density in the field. We have also conducted extensive transplants in the field to estimate the effect of genetic variation on fitness under naturally-varying conditions, using cage experiments and mark-release recapture. These data are of direct relevance to theoretical models of limits to adaptation and provide some of the first empirical tests of limits to adaptation, and the distribution of genetic variation in fitness in natural populations. These limits not only affect the resilience of species and ecosystems to climate change, they also influence the rate at which new lineage diversify when faced with spatially or temporally variable conditions. Key finding of our analyses so far are that: (1) genetic variation that generates local adaptation may be limited (despite evidence for long-standing responses to selection), and (2) Biotic interactions seem likely to limit abundances of species at the warmer limits of their distribution.


Limits to the distribution of species occur either because selective gradients become too steep relative to migration between populations, or because marginal populations lack the genetic variation necessary for adaptation. Repeated altitudinal transects in the fruitfly Drosophila birchii presents a unique opportunity to distinguish between these hypotheses, and highlight the key ecological and genetic parameters that limit evolutionary potential in natural populations.



We have used novel field experiments, and extensive quantitative genetic analysis of natural populations in Australia to estimate gene flow, additive and non-additive variation in stress-related traits, and directly assess the consequences of genetic variation in fitness on adaptive divergence along repeated ecological transitions of varying steepness. This has generated a very large dataset that is now being analysed in collaboration with our existing Project Partners (Prof Ary Hoffmann, Melbourne and Mark Blows, University of Queensland). These empirical estimates of key parameters will be used to test the generality of theoretical models for evolution at ecological margins, in collaboration with another project partner (Prof Nick Barton, IST Austria). We are preparing these results for publication as soon as possible.



Data analysis so far suggests (a) evolutionary responses to temporal as well as spatial variation along these ecological gradients and (b) evidence for trade offs between ecological tolerance and success in matings. To pursue the latter issue in more detail we have developed new links with Prof Leigh Simmons (UWA), Dr Rhonda Snook (Sheffield), as well as Dr Nick Priest (Bath).



New developments in sequencing technology means that we have significantly extended the genotyping originally planned in the application. We have secured a close collaboration with the NERC NBAF (Sheffield and Edinburgh) in order to achieve this.
Exploitation Route Findings from this project have potential impact for guiding translocation or transplantation programmes to maximise evolutionary potential of natural populations. There is an urgent need to predict rates of evolution to environmental change in order to provide good scientific guidance on the consequences of climate change and habitat loss for biodiversity and ecosystem services. Our data can also predict which species and populations (and ecosystems) are more likely to be rapidly impacted by climate change and habitat loss.
Sectors Agriculture, Food and Drink,Environment

URL http://www.bristol.ac.uk/news/2017/january/species-climate-change-.html
 
Description They contributed to policy briefing documents on likely ecological and evolutionary responses to climate change
First Year Of Impact 2010
Sector Environment
Impact Types Policy & public services

 
Description Invited attendance on EU and international working groups to provide guidance on biological responses to climate change
Geographic Reach Multiple continents/international 
Policy Influence Type Membership of a guideline committee
 
Description Funding for a PhD studentship to continue research on trade offs between sexual success and stress resistance in flies
Amount £50,000 (GBP)
Organisation University of Bristol 
Sector Academic/University
Country United Kingdom
Start 10/2013 
End 03/2017
 
Description NERC Standard Grant on ecological and evolutionary responses to tropical food webs to climate change (with Owen Lewis, Oxford)
Amount £800,000 (GBP)
Funding ID NE/N010221/1 
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 03/2016 
End 03/2019
 
Description Support for molecular genetics (ddRAD) on Drosophila birchii from NBAF
Amount £15,000 (GBP)
Organisation Research Councils UK (RCUK) 
Sector Public
Country United Kingdom
Start 03/2013 
End 02/2014
 
Description World Universities Network Funding
Amount £4,500 (GBP)
Organisation Worldwide Universities Network 
Sector Academic/University
Country United Kingdom
Start 01/2013 
End 04/2013
 
Title Data on genetic variation in fitness and phenotypes in rainforest Drosophila 
Description Data from laboratory crosses of genetic variation in male mating rate and female fecundity for isofemale lines collected from four elevational transects in North Queensland. Currently being analysed for data on covariances and changes in amount of genetic variation along elevational transects (being prepared for publication). Data on remating mate in male D. birchii, and genetic variation in this trait along two of these transects (currently submitted for publication in Heredity). Data on trait variation and its effect on fitness in large-scale field transplant experiment along two transects (being prepared for publication) 
Type Of Material Database/Collection of data 
Year Produced 2013 
Provided To Others? No  
Impact These data suggest that genetic variation in fitness remains high even at ecological margins, suggesting that reduced population growth rate, perhaps driven by this genetic variation, is a cause of ecological margins. 
 
Title Environmental variation and biotic interactions limit adaptation at ecological margins: lessons from rainforest Drosophila and European butterflies 
Description Models of local adaptation to spatially varying selection predict that maximum rates of evolution are determined by the interaction between increased adaptive potential owing to increased genetic variation, and the cost genetic variation brings by reducing population fitness. We discuss existing and new results from our laboratory assays and field transplants of rainforest Drosophila and UK butterflies along environmental gradients, which try to test these predictions in natural populations. Our data suggest that: (i) local adaptation along ecological gradients is not consistently observed in time and space, especially where biotic and abiotic interactions affect both gradient steepness and genetic variation in fitness; (ii) genetic variation in fitness observed in the laboratory is only sometimes visible to selection in the field, suggesting that demographic costs can remain high without increasing adaptive potential; and (iii) antagonistic interactions between species reduce local productivity, especially at ecological margins. Such antagonistic interactions steepen gradients and may increase the cost of adaptation by increasing its dimensionality. However, where biotic interactions do evolve, rapid range expansion can follow. Future research should test how the environmental sensitivity of genotypes determines their ecological exposure, and its effects on genetic variation in fitness, to predict the probability of evolutionary rescue at ecological margins. This article is part of the theme issue 'Species' ranges in the face of changing environments (Part II)'. 
Type Of Material Database/Collection of data 
Year Produced 2022 
Provided To Others? Yes  
URL http://datadryad.org/stash/dataset/doi:10.5061/dryad.q573n5tkg
 
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 Interview for online course at University of Queensland on Climate Change denial (on biological responses to climate change 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Media (as a channel to the public)
Results and Impact I was interviewed on ecological and evolutionary responses to climate change for the online course at the University of Queensland on "Climate Change Denial". This is made freely available on youtube
Year(s) Of Engagement Activity 2015
 
Description Invitation on panel debate for BBC R4 Saving species 
Form Of Engagement Activity A formal working group, expert panel or dialogue
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Media (as a channel to the public)
Results and Impact Discussion covered the effects of climate change and habitat loss on biodiversity - sparked questions and discussions on message boards afterwards

On Open Days parents have mentioned hearing me on this programme; UG students have also mentioned it and on one occasion discussed how it encouraged them to study biology
Year(s) Of Engagement Activity 2012
 
Description Science cafe and exhibition stand at the Bristol Festival of Nature 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Schools
Results and Impact Discussions with public about biological responses to climate change

Feedback on the Festival of Nature and data gathering exercise indicated that many visitors to the FoN reported an increase in awareness and changed views following visiting the event as a whole.
Year(s) Of Engagement Activity 2010