Resolving the paradox of stasis: addressing the missing fraction problem

Quantitative genetics has been exceptionally successful at predicting evolution in simple scenarios, for example, the response to artificial selection on a specific traits, such as milk yield in cattle, or body size in mice. Evolutionary quantitative genetics seeks to apply the same principles in nature. This endeavor has so far had much more mixed success. It is clear that the basic ingredients for adaptive evolutionary change, i.e., genetic variation for and natural selection of a trait, both occur frequently in natural populations. However, the rapid contemporary evolutionary change that would be expected from an abundance of heritability and selection is rarely observed. This set of observations has been called the "paradox of stasis". A paradox is only an *apparently* illogical scenario: theoretical evolutionary quantitative genetics has been extremely successful at generating potential solutions to the paradox. In general, applying these more advanced theories is challenging, and there is consequently a great paucity of data on the solutions to the paradox, relative to the quantity of data on simple quantities such as heritability and selection. We propose to tackle one of the most theoretically important solutions, which is also one of the least studied empirically.

The "missing fraction problem" occurs if viability selection alters the distribution of a trait before it is expressed. For example, if individuals that would otherwise produce large values of a trait are likely to die before producing the trait (because of viability selection at an earlier stage of the life cycle on a correlated trait) then this selection will not be picked up in a selection analysis that relates available phenotypes to fitness: importantly, selection estimated in this naïve analysis will be upwardly biased. There are a number of opportunities to get around this problem, for example, by jointly modeling the selection and genetics of focal traits, along with early life viability (i.e., treat survival as a trait), or traits that may influence early survival. We organize these opportunities into a hierarchy of four levels. All of these levels make greater demands on data than typical studies of the selection and genetics of traits in the wild. However, different levels of analysis could potentially be achieved in many study systems.

In our study system, the Soay sheep population on St Kilda, we are able to apply all four levels of the hierarchy to a range of traits, with a special focus on body size and reproductive scheduling. We will conduct a coordinated series of studies on the extent of the missing fraction problem that will generate a comprehensive analysis of how much accounting for this key issue can change evolutionary inferences in the wild. Additionally, we also propose (1) theoretical work to address the potential severity of the missing fraction problem across different life histories, (2) methodological developments to help researchers (including initially ourselves!) apply some of the most advanced available statistical methods to the problem, and (3) a synthetic review, summarizing the available theory, methods and key results (which by the end of this project will come in large part from our own study). Our study will thus provide a comprehensive step forward for evolutionary quantitative genetics, and will enable the field in general to begin to properly tackle one of its biggest outstanding problems.

Academic and non-academic stakeholders

We propose to tackle one of the largest outstanding problems that faces evolutionary quantitative genetics. This will improve our understanding of how to apply evolutionary thinking in nature, including in management situations where understanding positive (e.g., evolutionary rescue) and negative (e.g., undesirable evolutionary responses to harvest) aspects of short-term evolution in the wild are becoming increasingly pressing.

The Soay sheep project is a co-operatively run interdisciplinary project from which 185 papers have been published across behaviour, ecology, population dynamics, host-parasite ecology, immunology, physiology and ageing research, as well as evolutionary genetics, many in high profile journals (please see the project website for a full list of publications: http://soaysheep.biology.ed.ac.uk/). In addition to its main objectives, this proposal will ensure continuity of the field data series which started in 1985 and which underpins research in these other disciplines, many of which are extremely active right now. Areas with currently active academic staff or independent research fellows include: immunology and ageing research (Prof. Dan Nussey, Edinburgh), population dynamics (Dr. Dylan Childs, Sheffield), grazing ecology (Prof. Mick Crawley, Imperial and Prof. Robin Pakeman, James Hutton Institute), genomic prediction (Prof. Jon Slate, Sheffield), evolutionary genetics (Dr Susan Johnston, Royal Society URF, Edinburgh).

Six PhD students at various institutions are currently using Soay sheep data to investigate a wide variety of questions, some addressing comparisons between long term studies.

Outreach

We have requested funds (see Pathways to Impact) to purchase two tablet computers. We will develop an application to illustrate evolutionary principles for children and adults of all ages. Briefly, the app will allow participants to select a phenotype (e.g., horn morphology, life history strategy) of a sheep, and then compete that phenotype against the rest of the Soay sheep population in live simulations. Each phenotype option will come with a brief description of its benefits and costs. We will initially make the options based on a previous study of selection for different horn morphologies, but towards the end of this project we will add options for the focus of much of the proposed work, female reproductive scheduling. We will use this application at different opportunities for engagement including especially by the PI at the Dundee Science Festival.

Media coverage

The Soay sheep project generates results of high general scientific interest. Newsworthy results in this system have the potential to make basic ecological and evolutionary principles widely accessible. See, for e.g., https://www.sciencenews.org/article/sheep-horns-bigger-not-better for an excellent example that arose from research showing balancing selection on the Horns locus, published in Nature.

The general public

There is great public interest in both St Kilda and the Soay Sheep Project and more generally in ecology and evolution. Our previous work has attracted considerable interest in the TV, radio and written media, because the sheep system provides many easy to understand examples of quite complex ecological and evolutionary. We have a good track record of turning published outputs into accessible stories which will help the public to understand basic genetic and evolutionary principles. On St Kilda we maintain information sheets on several aspects of the Soay sheep research in the museum, our work is described in the National Trust for Scotland booklet about the islands and we expect to contribute material about our research in the forthcoming St. Kilda Visitor Centre on Lewis (see http://www.ionadhiort.org/).

Whenever we have newsworthy outputs from the project we liaise with the press offices at our universities, who will help publicise our work.