Multivariate evolution in replicated adaptive radiations: pattern, process and the role of the environment.

Lead Research Organisation: University of Nottingham
Department Name: School of Life Sciences

Abstract

The studies of ecology and evolution are closely related. Ecologists seek to understand the environmental factors that explain the distribution and abundance of species, while evolutionary biologists investigate the process of natural selection and the evolution that results, by examination of adaptation in phenotypes and genotypes. It is curious in these times of environmental change that one of the biggest gaps in our understanding of the natural world falls exactly at the intersection between ecology and evolution: we know less than we should about how the environment shapes the evolution of biodiversity. Although it is generally understood that the environment is the cause of adaptation, the links between them have seldom been explicitly explored. Many ecological studies do not consider how the environmental variation that they measure affects evolution, while many studies of evolution measure selection or adaptation without considering their environmental causes, concentrating instead on the consequences for evolution of what is genetically possible.

Explicit study of the involvement of the environment in evolution has the potential to fuel a paradigm shift in our comprehension of fundamental evolutionary patterns. For example: (i) Divergence. Evolution has resulted in abundant diversity in the natural world, but the extent of this divergence within related groups of organisms is often circumscribed. Are these limits, on the kind of organisms that evolve, a consequence of what is genetically possible, or do they result from similarities in the environments to which the organisms are exposed? (ii) Convergence. Within the greater divergence, organisms have often apparently converged on similar evolutionary solutions, suggesting that evolutionary outcomes are to some extent repeatable. Is the repeated evolution of similar organisms in different places the result of genetic biases or environmental determinants? If the latter, do similar organisms always evolve in similar environments, or can different environments favour the same outcome of organismal form? Vice versa, do similar environmental combinations always result in essentially the same organism, or are there different evolutionary solutions to similar environmental problems? (iii) Novelty. Although similar organisms in different places often converge on repeated evolutionary solutions, evolution also occasionally comes up with solutions that are different from the general pattern, by dint of developing, or having lost, some distinguishing feature or combination of features. Is such evolutionary novelty the result of particularly unusual environments?

Most previous studies of how the environment affects evolution have measured only a single, or small number of aspects of both the organism and the environment, but thorough answers to the questions we pose require a more comprehensive understanding of multiple different aspects of organism and environment, and of how they interact and affect other. Our approach requires the use of recently developed multivariate statistical methods that allow the simultaneous analysis of many organismal traits and many environmental variables.

Adaptive radiation is the differentiation of an ancestral species into divergent new populations or species. The abundance of variation in both environment and biodiversity make adaptive radiations the perfect natural laboratories to address our questions. We will use data from replicated adaptive radiations of three-spined stickleback fish in Scotland, Iceland, western Canada and Alaska in order to answer our questions and achieve a comprehensive understanding of how the environment affects evolution. Three-spined stickleback are originally marine fish that have invaded freshwater throughout the northern hemisphere since the last ice age. Freshwater stickleback can occupy contrasting environments and exhibit great phenotypic variation, providing a perfect system for our study.

Planned Impact

The current proposal is for responsive mode, 'blue skies' research. Its principal benefit is 'simply' a better understanding of how the world around us works. We should never underestimate the value of this knowledge in its own right. We envisage the following impacts:

(1) The project will lead to improved excellence in UK research by supporting the NERC mission of promoting high quality basic research in freshwater systems, and by addressing fundamental but empirically unexplored questions about the role of the environment in generating biodiversity at the intra-species level.

(2) Funding will give a PDRA the opportunity to codirect a major international collaborative project, while gaining skills in fieldwork, environmental analysis, geometric morphometrics and quantitative and molecular genetics. The technician employed on the grant will gain skills in fieldwork, fish husbandry, phenotypic analysis techniques and molecular genetics. Funding would also support the career of Alan Crampton, widening his experience and strengthening the development of facilities for stickleback research in Nottingham. Biological material and data collected during the project will be used as the basis for Masters and Honours project theses for years to come.

(3) Part of the project will be carried out in the Western Isles, where ADCM has been engaged in research for five years, and where there is already interest in our research within the community, as a result of contributions that ADCM has made to websites, by giving talks to the local natural history society and donating posters about our research to the local museum and arts centre. We will seek to strengthen these links by: (a) organising a workshop with local conservation bodies (e.g. RSPB, Scottish Natural Heritage, Comann na Mara) and landowners to (i) highlight the astonishing local variation in freshwater and brackish environments, which result in waterbodies on the Hebrides supporting what is certainly one of the best examples of adaptive radiation among temperate freshwater fishes. (ii) Discuss our research and identify how it might contribute to conservation policy and land management e.g. by helping to identify evolutionary significant units. (b) Developing activities that promote our engagement with the local general public such as (i) Website: We will make contributions to the website of a local conservation organisation, Comman na Mara that seeks to promote interest in the importance of local aquatic habitats. We will also enhance our existing group web pages to include more details about our research project and the wider background of adaptive radiation and three-spined sticklebacks. (ii) Posters: We will supplement existing posters that we have supplied for display in the local community centre with others about adaptive radiation and environmental change. (iii) Educational workshops: We will undertake to organise workshops with schoolchldren in the local primary and secondary schools, to be run by the PDRA. These will include similar content to those outlined in 3a (i), but delivered in appropriate ways for schoolchildren.

(4) ADCM has a history of engagement with public interest groups in the Sheffield and Nottingham areas. He has visited local primary schools to give slide shows and given seminars about his research to night school classes. For this project he will undertake to deliver talks to Cafe Scientifique meetings in Nottingham and Sheffield. The PDRA will be encouraged to engage with the public in similar ways. The School of Biology at the University of Nottingham is home for two very active schools outreach programmes (Public Understanding of Science Project and the Open Air Laboratories (OPAL) network), which offer training in outreach. The PDRA will be encouraged to take part in these.
 
Description For the first time, we have documented patterns of phenotypic evolution and underlying population genetic patterns across multiple, widely spaced adaptive radiations of a vertebrate animal, in response to environmental variation. Our data demonstrate that genes associated with phenotypic and environmental variation are shared between radiations significantly more than expected by chance, demonstrating on an unprecedented scale the phenomenon of evolutionary parallelism that has been widely debated in evolutionary biology and other areas of science.
Exploitation Route Our findings contribute to a growing understanding of the mechanisms by which biodiversity is generated and will inform the work of a wide community of evolutionary biologists and ecologists.
Sectors Education,Environment,Culture, Heritage, Museums and Collections

 
Description Genomic responses to rapid environmental change: selection, plasticity and adaptation.
Amount £579,369 (GBP)
Funding ID NE/R00935X/1 
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 05/2018 
End 10/2022
 
Description Alaska 2015 
Organisation State University of New York
Country United States 
Sector Academic/University 
PI Contribution Contribution of personnel and funding to carry out fieldwork
Collaborator Contribution Support for execution of fieldwork, academic discussions, application for follow-up funding
Impact Successful completion of fieldwork
Start Year 2012
 
Description BC 2015 
Organisation University of British Columbia
Department Department of Zoology
Country Canada 
Sector Academic/University 
PI Contribution Contribution of personnel and funding to carry out fieldwork
Collaborator Contribution Support for execution of fieldwork, academic discussions, application for follow-up funding
Impact Successful completion of fieldwork
 
Description Iceland 2014 
Organisation Holar University College
Country Iceland 
Sector Academic/University 
PI Contribution Contribution of personnel and funding to carry out fieldwork
Collaborator Contribution Support for execution of fieldwork, academic discussions, application for follow-up funding
Impact Successful completion of fieldwork
Start Year 2013
 
Description Public talk 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Public/other audiences
Results and Impact Talk led to questions, discussion and increased awareness about our research

Improved contact with local community, which aids execution of research
Year(s) Of Engagement Activity 2013