Experimental adaptation and speciation in rotifers

Lead Research Organisation: University of Sheffield
Department Name: School of Biosciences

Abstract

Evolutionary biology seeks to explain two features of the natural world: the fit of organisms to their environment (adaptation) and the diversity of different species. Diversity depends on a balance between two key processes, division of existing species into two or more distinct daughter species (speciation) and extinction. In sexually-reproducing organisms, species are defined by successful interbreeding within species combined with barriers to interbreeding between species. Thus speciation consists of the evolution of new barriers to interbreeding between populations. The evolution of these barriers can be initiated by divergent natural selection that generates adaptation of populations within a species to different environments. To complete the speciation process, this adaptation needs to be combined with other barriers to successful interbreeding such as assortative mating.

Theory suggests that two major forces oppose divergent adaptation and the progression towards speciation. These are gene flow, due to the movement of individuals from one population to another, and recombination, the genetic process that breaks up combinations of genes generated by natural selection or other factors. However, it is difficult to test the effects of these forces in natural systems because of the complex and unknown history of extant species or divergent populations. In this project, we will take a different approach, using experimental control of migration and recombination in pairs of populations under divergent selection to test their effects, independently and jointly, on both adaptation and the evolution of barriers to interbreeding.

We will use rotifers in the Brachionus plicatilis species group. These are small aquatic animals that are easily cultured in the laboratory with a generation time of only a few days. They have both sexual and asexual modes of reproduction and this will allow us to control recombination by varying the frequency of the sexual mode. We will maintain replicated pairs of lines without sexual reproduction, with rare sex and with frequent sex. Within each pair, each line will be subjected to a different novel, stressful environment, resulting in divergent selection. We will also control gene flow between paired lines by having replicates without connection, replicates where one individual is moved between lines each time we renew cultures, replicates with a higher rate of movement and replicates that are completely mixed. We will follow the progress of divergent adaptation in these pairs of lines over more than 100 generations and also test whether they evolve other barriers to interbreeding by measuring assortative mating and the fitness of hybrids. We will sequence the genomes of our starting populations and of the experimentally-evolved lines. This will allow us to determine whether gene flow and recombination influence the number and distribution of genetic changes underlying the evolutionary changes we observe.

Experimental evolution has rarely been used in the context of speciation research but there is now an increasing recognition that experimental work is needed to complement theory and analysis of natural systems. With this project, we will apply this approach to central issues in speciation research using a powerful model system that has not previously been used in this context. The further understanding of adaptation and speciation to which this project will contribute is critical for the management of biological diversity in a changing environment.

Planned Impact

While the primary beneficiaries of this research are academic scientists interested in evolutionary processes, we see three other groups of beneficiaries:

1. Policy makers and practitioners concerned with the management of biological diversity in the face of climate change. The effectiveness of management measures will be enhanced by better understanding of the process of adaptation to changing environments (both spatially and temporally), the nature of differentiation among populations and the nature of species. We propose to address this group by summarising our results and their implications in an article aimed at a wider audience in a periodical such as British Wildlife.

2. The public, whose interest in biological diversity and evolution is clear but whose knowledge and understanding of evolutionary processes is generally quite limited. We will exploit the fact that our controlled experiment will provide an accessible introduction to the critical tension between natural selection and opposing processes. We will develop a display for use at the highly-successful University of Sheffield public science event 'Researcher Night' and at other similar venues.

3. The fish farming and aquarium trade, which uses huge numbers of commercially-produced rotifers to feed juvenile fish and other aquarium animals. We are in contact with a company involved in rotifer production to discuss research that may help to improve culture methods and the genetic quality of commercial rotifer strains. We also propose to organize a workshop for companies that produce algae and aquatic invertebrates. This will be aimed at understanding of evolutionary changes in the cultured organisms during large-scale production that might be either beneficial or harmful. See Impact statement for further information.

Publications

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Butlin RK (2020) Is it time to abandon the biological species concept? No. in National science review

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White NJ (2020) The Past and Future of Experimental Speciation. in Trends in ecology & evolution

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Kulmuni J (2020) Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers. in Philosophical transactions of the Royal Society of London. Series B, Biological sciences

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White NJ (2021) Multidimensional divergent selection, local adaptation, and speciation. in Evolution; international journal of organic evolution

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Butlin RK (2021) Homage to Felsenstein 1981, or why are there so few/many species? in Evolution; international journal of organic evolution

 
Description Using novel analyses of whole-genome sequence data and gene expression data, we show that a key evolutionary innovation (live birth) evolved progressively through changes in at least 50 genes and over a long period. This significantly advances understanding of a major evolutionary question.
Exploitation Route The finding that live birth evolved in multiple steps raises fascinating questions about the nature of those steps. Dr Sean Stankowski plans to pursue this direction of research now that he has a lectureship at the University of Sussex.
Sectors Environment

 
Description Serra 
Organisation University of Valencia
Country Spain 
Sector Academic/University 
PI Contribution Research discussions. Co-supervision of student.
Collaborator Contribution Assistance with sampling, provision of biological material, advice.
Impact Sets of rotifer clones and field samples. Not multi-disciplinary.
Start Year 2017
 
Description Discovery Night 2018 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Public/other audiences
Results and Impact We provided displays and activities illustrating local adaptation in snails and rotifers and so principles of evolution.
Year(s) Of Engagement Activity 2018
 
Description Discovery Night 2019 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Public/other audiences
Results and Impact We provided displays and activities illustrating local adaptation in snails and rotifers, thus illustrating general principles of evolution.
Year(s) Of Engagement Activity 2019