Routes to speciation in Littorina

Lead Research Organisation: University of Sheffield
Department Name: Animal and Plant Sciences

Abstract

The diversity of organisms on earth has arisen through the evolutionary splitting of lineages to form new species (speciation). The splitting process is often lengthy, involving multiple mechanisms at different stages in separation. It may begin with natural selection operating in opposite directions in different populations, causing local adaptation. However, it may also begin with incompatibilities between populations that arise when populations are spatially separated. In either case, other traits must evolve that reduce successful interbreeding, thus completing reproductive isolation. The relative importance of these different pathways to speciation is poorly understood but they are expected to leave different patterns of differentiation in the genomes of diverging populations and may be associated with different histories.

We propose to test predictions of the major modes of speciation in a group of marine snails. One species in this group has multiple forms living in very distinct habitats. However, despite many differences in size, shape and behaviour, these forms are still able to interbreed successfully, perhaps because hybrids do not have much lower fitness than their parents in intermediate habitats. Paradoxically, there are also species that show little or no ecological separation, have diverged recently and yet show close to complete reproductive barriers. This allows a very direct comparison of population histories and patterns of genomic differentiation in very closely related populations that have, apparently, progressed towards speciation by different routes.

We will measure the effects of spatial and temporal separation of snails on the sea shore, separation in timing of reproduction, mate choice and hybrid fitness so that we know the nature of current isolation between ecotypes and between species. We will then make use of genome re-sequencing to assess the genome-wide pattern of differentiation. These genetic data can be used to test alternative scenarios for the history of the populations and so to ask whether a period of spatial separation was likely around the origin of the species but unlikely around the origin of the ecotypes. The data can also identify parts of the genome with strong barriers to gene exchange and with signatures of past selection. These will be linked to genes involved in the development and function of the distinct reproductive systems of the egg-laying and brooding species, a candidate trait for contributing to incompatibility in hybrids. Together, these data will allow us to determine the outcomes of divergent selection and evolution of incompatibility, providing an example that will inform general theories of speciation as well as other questions in evolutionary biology, particularly the genetic basis of local adaptation.

Planned Impact

While the primary beneficiaries of this research are academic scientists interested in evolutionary processes, we see two 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 a report suitable for biodiversity management professionals, primarily aimed at a senior level in Natural England, and by 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 field sites include popular holiday destinations. We will provide interpretation and demonstrations at appropriate sites where our previous experience suggests that it is easy to attract attention.

Publications

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Butlin R (2020) Is it time to abandon the biological species concept? No in National Science Review

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Butlin RK (2018) Coupling, Reinforcement, and Speciation. in The American naturalist

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Faria R (2021) Speciation in marine environments: Diving under the surface. in Journal of evolutionary biology

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Faria R (2019) Evolving Inversions. 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

 
Description Our two focal species, the rough periwinkles Littorina saxatilis and L. arcana, show nearly complete reproductive isolation but with evidence for a very low rate of gene flow that may still be continuing. Surprisingly, L. arcana is more closely related to northern than to Iberian populations of L. saxatilis. So far, we have not found any genomic regions with higher divergence than the background level, a pattern that is hard to explain. We are considering how to interpret these findings in terms of the route to speciation for these snails and conducting further analyses.
Exploitation Route The findings will provide new insights in mechanisms of speciation, of value in advancing the field of evolutionary biology.
Sectors Environment

 
Description We have undertaken outreach activities both at a field site and in Sheffield aimed at improving public understanding of evolution. We have created an animation for use in teaching (high school and starting undergraduate) and outreach activities concerning speciation. This is freely available and will be subtitled in multiple languages.
First Year Of Impact 2017
Sector Education
Impact Types Societal

 
Description CeMEB 
Organisation University of Montana
Department Marine Sciences
Country United States 
Sector Academic/University 
PI Contribution Expertise in population genetics/genomics. Joint working.
Collaborator Contribution Field facilities. System expertise. Joint working.
Impact Tage Erlander, Waernska and SciLife funding opportunities relied on this partnership. Multiple publications also relied on the interaction.
Start Year 2009
 
Description Roscoff 
Organisation National Center for Scientific Research (Centre National de la Recherche Scientifique CNRS)
Department Biological Station, Roscoff
Country France 
Sector Academic/University 
PI Contribution Research interaction on common projects
Collaborator Contribution Facilities access and personnel assistance for field work
Impact Sample sets. Not multi-disciplinary
Start Year 2017
 
Description Animated video: "Snails evolving on the sea shore" 
Form Of Engagement Activity A broadcast e.g. TV/radio/film/podcast (other than news/press)
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Schools
Results and Impact The animation is freely available via YouTube and other sites. It is intended for educational use in schools or for early-year undergraduate students, as well as for the general public. We are currently providing subtitles in multiple languages. The video illustrates the process of speciation via local adaptation.
Year(s) Of Engagement Activity 2019
URL https://www.youtube.com/watch?v=XDAuQQzQuWg&t=114s
 
Description Discovery Night 2017 
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 Displays and activities illustrating evolutionary principles using Littorina as an example as part of a University-wide open evening. Our specific display attracted nearly 100 people, mainly families.
Year(s) Of Engagement Activity 2017
URL https://www.sheffield.ac.uk/discoverynight
 
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