The ecology of evolution: the role of environmental heterogeneity in evolutionary dynamics.

Lead Research Organisation: University of Edinburgh
Department Name: Sch of Biological Sciences


Although we have a good general understanding of how evolution operates, we have only limited insight into its detailed workings in natural populations. A prominent challenge is to understand the extent to which variation in environmental conditions affects evolutionary change within natural populations. Improved knowledge in this area will greatly advance our understanding of how genetic diversity is maintained in natural populations and of how populations are likely to respond to predicted changes in climate. The characteristics of individuals in a population are a consequence of their genes, the environment in which they live and the evolution that has occurred up to that point. So much is clear, but this simple statement conceals much complexity. Specifically, the consequences of carrying particular genes can vary with environmental conditions; it is possible (but not generally proven) that organisms express more of their genetic potential under good rather than bad environmental conditions. Similarly, the strength of natural selection, whereby some individuals have higher survival or reproductive success than others, may vary with environmental conditions. Since evolutionary change occurs when natural selection acts on inherited characters, environmental fluctuations can therefore have a substantial impact on evolution. Finally, because some of the genes underlying a particular character (e.g. body size) may be the same as, or associated with, the genes underlying another character (e.g. parasite resistance), characters are not free to evolve independently of one another. Instead the effect of natural selection on one character will be constrained by any selection that is also occurring on other characters to which it is genetically tied. Recent research suggests that these constraints also vary with environmental conditions. Currently, we have very little understanding of how these various processes interact to shape evolution in natural populations. In this study we will investigate the effect of environmental conditions on evolutionary processes using data from an unmanaged study population of Soay sheep on the island of St Kilda, NW Scotland. The data set is particularly useful for this study because, firstly, we have records on the individual life histories of several thousand sheep measured across 23 years. DNA profiling has been used to determine paternity and provide a family tree suitable for the kind of genetic analyses proposed here. Secondly, our previous research has demonstrated that there are four kinds environmental variation which show strong temporal variation affecting sheep performance, and we will be investigating all four kinds of variation in this study: the weather, sheep population density, food availability and parasite abundance. We will address the effect of the environmental conditions described above on the expression of genetic variation, the strength of natural selection and the genetic relationships between characters. Specifically we will ask how the environmental affects first, the expression of genetic variation in single characters like body weight: is more genetic variation always expressed when conditions are good? Second does environmental variation affect genetic relationships between characters? For example, are body size and parasite resistance freer to evolve separately under good or bad conditions? Third, is selection stronger or weaker under good environmental conditions? Together these analyses will allow us to predict the course of evolution under specific time series of environmental conditions - for example systematic climate change. Long-term studies of individually-recognised wild animals such as these are an important source of information on many aspects of ecology and evolutionary biology, and the proposed grant would guarantee continuity of data collection for one of the UK's most valuable ecological and evolutionary field data sets.


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Description In this grant we are investigating the process of natural selection in the wild in great detail, and specifically asking how environmental variation in time and space affects the outcome. here are a small number of our recent findings.

How does fitness vary with spatial variation in habitat quality?

We have addressed this question at very fine scale. The % cover of each plant species for each ha of the study area was estimated. Male and female Lifetime Reproductive Success (LRS) was analysed in relation to two metrics: % Holcus lanatus (a grass) in the home range and % Calluna vulgaris (heather) in the home range.

In both sexes the % Holcus is associated with increased LRS. In females this higher LRS is due to higher fecundity, higher lamb survival and longer lifespan. The cause of the association is less clear for males.

In males the % Calluna is associated with higher LRS which comes about through longer lifespan. No effects were seen for females.

How best to predict an evolutionary (i.e. genetic) response to selection?

We have investigated predictions of the response to natural selection using methods from agriculture (specifically the univariate and multivariate forms of the breeder's equation) and by estimating the genetic tie-up (genetic covariance) of trait and fitness, for four size traits in Soay sheep. There are appreciable differences in the predictions, with the breeder's equation consistently predicting increase in body size while the covariance measure does not. The genetic covariance predictions are closer to observation (the sheep are actually getting smaller). These results suggest that predictions of selection from the breeder's equation are upwardly biased by unmeasured factors in natural populations, i.e. the effects of environmental heterogeneity.

Is there selection against fecundity?

Each year most Soay females have singleton lambs, but some have twins. We have investigated an array of potential effects of twinning on life history (survival and reproduction), and their dependence on age, sex, and environmental conditions. These analyses reveal substantial fluctuations in the costs of twinning (and costs of being a twin) with environmental conditions. We have combined these inferences with estimates of genetic variation for the propensity to twin (simultaneously accounting for ewe age, own twin status, and the population-level probabilistic reaction norm to population density, etc.) in an integral projection model. The model predicts that twinning should be declining in the population.

How does selection and the expression of genetic variation vary with environmental conditions?

Despite consistent experimental evidence for genotype-by-environment interactions (G*E), studies estimating the extent of G*E in wild populations are rare. Estimating selection-by-environment interactions is also crucial to enable predictions about the impact of environmental change upon evolutionary dynamics. We used 24 years of data collected from wild Soay sheep to quantify how an important environmental variable, population density, impacts upon (1) selection through annual contribution to fitness and (2) expression of genetic variation, in six morphological and life-history traits. Selection analyses revealed that all traits were associated with annual fitness and that the association in five traits was stronger in years of higher population density, suggesting that selection strengthened under more adverse conditions. Quantitative genetic animal models showed that five traits showed significant additive genetic variance. Finally, random regression animal models did not support the presence of G*E for any trait, and showed that individual-by-environment interactions were present for only two traits. We conclude that while environmental variation may profoundly alter the strength of selection, its impact upon the expression of genetic variance may be weaker. Despite this, the presence of selection and additive genetic variance for most of our traits still suggests that responses to selection are to be expected.

A paper on this subject is now published.
Exploitation Route This is curiosity-driven research in the natural world that may not have immediate application. However, as a set of research findings these results, especially those summarised in the last paragraph above, which were published in Jan 2018 (Hayward et al (2108) Genetics) move the field on appreciably.
Sectors Environment

Description This is curiosity-driven research in the natural world that may not have immediate application.
First Year Of Impact 2014
Sector Environment
Impact Types Policy & public services

Description ERC Advanced Grant
Amount € 2,500,000 (EUR)
Funding ID 250098 
Organisation European Research Council (ERC) 
Sector Public
Country Belgium
Start 09/2010 
End 08/2015
Description NERC Standard Grant
Amount £464,402 (GBP)
Funding ID NE/M003035/1 
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 02/2015 
End 01/2015
Description NERC Standard Grant
Amount £464,402 (GBP)
Funding ID NE/M003035/1 
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 04/2015 
End 04/2018
Description Anglia Ruskin University field course talk 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Undergraduate students
Results and Impact 30 students on the ARU field course were given a talk about the red deer research on Rum while on a visit to the field site, where they also watched the deer and examined cast antlers and the post mortem skeletal collection.
Year(s) Of Engagement Activity 2015
Description Media interest (ecology and behaviour) 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Media (as a channel to the public)
Results and Impact BBC Coast came to St Kilda to film Soay sheep behaviour and filmed our research team at work in the field.

Broadcast August 2014. Many people saw it.
Year(s) Of Engagement Activity 2013
Description Visitor interest (evolution, ecology and behaviour) 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Visitors who come to St Kilda (who are from right around the world) are always interested in the sheep and we provide written material about them in the museum and talk to any that ask questions.

This is hard to comment on, but visitors certainly go away better informed than when they arrive.
Year(s) Of Engagement Activity 2010,2011,2012,2013,2014