The MacColl Lab

University of Nottingham


Adaptation to environmental change:

We are most interested in adaptation to environmental variation and change. It is easy to think of evolution as a one-way, temporal process to some kind of adaptive perfection, that occurs in situ, perhaps because many well-known, long-term studies of evolution have taken place within small geographical areas, especially islands, or their aquatic equivalent, lakes. But evolution is a dynamic process, with populations and lineages having to adapt to constantly changing environmental conditions that may result in a waxing and waning of adaptation. The process has important spatial as well as temporal components. Species have finite geographical distributions. Populations and lineages, including modern humans, experience expansion and contraction. They may migrate between habitats and and sometimes undergo large scale movements, resulting in the invasion of new adaptive zones and the meeting and hybridisation of lineages. When lineages move they encounter variation in abiotic conditions like temperature, salinity, and pH, as well as associated biotic variation in food availability, competition, predation and parasitism. The long-term movement and mixing of lineages, and the different conditions they experience, gives adaptation a deep historical context, for example because of the genetic variation and combinations that may be present in some lineages and not others.

These considerations naturally give rise to questions about how adaptation arises, the agents of selection that drive it, its genomic basis and whether that is shared across locations or is idiosynchratic, the consequences of the movement and hybridisation of lineages, the conditions that favour, or constrain range expansion, changes in abiotic conditions, the availability of critical nutrients and food sources and the changing importance of natural enemies.

Answering these questions matters at a fundamental level, if we are ever to understand the evolution of life on Earth, but also at a more practical level, if we want to be able to predict and manage the consequences for nature of anthropogenic environmental change. Environments are changing rapidly as a result of human activity, leading to e.g. increases in temperature, rises in sea level and acidification of aquatic environments.

The evolutionary ecology of geographical range margins:
Many species will either have to adapt or move if they are to avoid the consequences of environmental change. An obvious way for this to happen is through adaptation at range margins. But the fact that all species have finite geographical distributions, suggests that adaptation fails at range margins. Despite this having fascinated evolutionary biologists for over half a century, and become a pressing question as global climates change, we still do not understand why adaptation fails. The answer probably lies in some decline in the efficiency of selection, because of unfavourable environmental and genomic circumstances at range margins. Modern sequencing technology, coupled with high-quality environmental data might unlock this conundrum. Three-spined stickleback have a phenomenal ability to adapt to environmental variation, and a wide geographic distribution, but they are contracting at their warm margins in the south and expanding north. We are collaborating with stickleback biologists at the geographic limit of this species in order to understand what combinations of genomic and environmental circumstances constrain or favour adaptation and expansion at range margins.

Functional consequences of mitochondrial variation:
Long-distance dispersal of lineages is nevertheless possible, as evidenced by countless studies showing substantial mitochondrial geographic structure within species. This sometimes leads to populations being supplanted by long-distance conspecific movements from elsewhere. For decades, mitochondrial variation was used as a marker of deep population history, and assumed to be selectively neutral. However, mitochondrial genes code for fundamental energy processing proteins in all eukaryotic life, and research is beginning to reveal that mitochondrial variation may have important consequences for adaptation. Stickleback have abundant mitochondrial variation, some of which appears to be affected by selection, and has strong habitat associations. We are beginning to investigate the functional consequences of this variation in the lab and the field.

Costs and benefits of migration:
In the populations of stickleback that we study on North Uist, there is a marked difference in mitochondrial genetics between populations that are resident in inland waters and those that migrate to sea to mature. This suggests one consequence of mitochondrial variation, and also underscores how limited is our knowledge of migration in fish, especially non-salmonids. Although many stickleback populations are anadromous, we understand little about the costs and benefits of this strategy relative to being resident in freshwater, or even the simple basics of when stickleback migrate and how far. We are investigating this using field observations, otolith measurements and genetic analyses.

Adaptation to variation in salinity:
A significant challenge facing anadromous fish is the change from salt- to freshwater. Anadromous stickleback appear to achieve this effortlessly, and have succeeded in establishing populations across the northern hemisphere that have rapidly adapted to freshwater environments. The genomic differences between marine and freshwater stickleback have been well described. Some of these changes are presumably immediately critical to living in freshwater, while others may be secondary consequences of doing so. In an ongoing, NERC funded project, we are tracking the population genetics of marine three-spined stickleback following artificial introductions into freshwater ponds. Examining these changes could help to reveal how other organisms might adapt to the rapid environmental change which they face.

Adaptation to variation in diet:
Fish species also experience a substantial change in diet when they migrate to, or colonise freshwater. One of the biggest of these is a sharp reduction in the availability of fatty acids in freshwater ecosystems. Fatty acids are a major source of metabolic energy for fish. The decrease in their availability can prevent certain lineages from colonising freshwater, but those with appropriate genetic changes can enter a new adaptive zone, potentially facilitating further divergence. The full genetic ‘toolkit’ necessary to adapt to differences in diet and energetic demands in freshwater, and the wider consequences of these changes, are poorly understood.

Ionomic variation:
Apparently smaller differences in chemistry and diet among freshwater environments may have much larger consequences for evolution than previously realised. Lochs (lakes) on the Scottish island of North Uist have unusual variation in water chemistry within a small area. We are using this to investigate the ionomic variation (differences in the elemental composition of individual organisms) among stickleback populations, the extent to which these are phenotypically plastic or genetically hard-wired, and their consequences for the wider evolution of populations. Such differences between animal, especially vertebrate, populations are rich vein of our present research.