Links between mitochondrial function and social behaviour in a warming world

How does an animal’s physiology affect its sociability, and how will this be altered in a warming world? Group living is key to foraging, predator-avoidance, migration, and reproduction in many animal species, but the costs and benefits of living in groups differ between individuals, partly in relation to their energetic needs (Ward & Webster 2016; Webster, Whalen & Laland 2017). This leads to variation in the sociability of animals within a species: it is not only in humans that we find a spectrum of social behaviour from those that are gregarious to those that are loners.

This diversity is partially explained by physiological differences. It is a widespread finding that there are consistent differences among members of a species in both their minimum and maximum rates of metabolism, and that this variation in metabolic rates influences a range of behaviours (Metcalfe, Van Leeuwen & Killen 2016). For instance, individuals with a higher metabolic rate are often observed to be less social, possibly because they prioritise food acquisition over the safety of group membership (Killen et al. 2021). It also influences the spatial structure of such groups. For example, the position of an individual within a school of fish is not random, but is influenced by both its capacity for aerobic swimming (Killen et al. 2012) and the energetic costs it incurs when digesting a meal (McLean et al. 2018).

In the case of ectotherms, this means that global warming – which causes increases in metabolic costs – will potentially alter the dynamics of social groups. However, the mechanisms underlying these effects are currently unclear. Metabolic rate is usually measured in terms of oxygen consumption by the whole animal, but using this proxy of metabolic rate may generate variability in links between behaviour and metabolic traits. Furthermore, it provides limited insight into the root causes of variation in metabolic demand and potential links with sociability.

A more informative approach is to examine the production rate of ATP, the molecule that powers all cellular processes. ATP is generated in the mitochondria of cells, which consume oxygen in the process. Interestingly, the efficiency of this process is highly variable: some animals require 2-3 times as much oxygen to produce a molecule of ATP as do others (Salin et al. 2015). This is a striking finding, and has led to work revealing that mitochondrial efficiency predicts whole animal performance, such as variation in growth rate (Salin et al. 2019). Moreover, in the case of ectotherms such as fish, mitochondrial efficiency is a stronger predictor of growth when they are living at high temperatures, when metabolic costs are more severe (Dawson et al. 2022). However, no one has yet examined whether mitochondrial efficiency influence social interactions.

This project will use an experimental approach to test for the first time how the social interactions of shoaling fish are influenced by the efficiency with which an individual’s cells can generate energy; it will also test how these interactions are likely to change in the face of global warming. Preliminary data with a social fish species shows that while some individuals display changes in gregariousness as temperature increases, the sociability of others remains constant. This project will test whether this plasticity in sociability with temperature is underpinned by variation in mitochondrial function. Specifically, individuals least able to thermally compensate at the mitochondrial level may be those that show the greatest changes in social behaviour as environmental conditions shift. This interdisciplinary project will thus combine behavioural ecology with ecophysiology, and will be the first to examine how thermal shifts brought on by climate change will alter the biochemical basis of energy metabolism and the potential links with the costs and benefits of group living.

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Image Captions

Shoal of colour-tagged minnows used in experiments on shoaling behaviour,Automated tracking of individually marked fish within a shoal


To address this issue, the proposed studentship will initially involve experiments using shoaling species of fish to :
(1) test whether spatial positions within fish schools are related to mitochondrial function, through its effect on swimming efficiency;
(2) examine how acute and long-term temperature changes affect the interplay among metabolism, mitochondrial function, and the behaviour of individual animals in their social group;
(3) test how mitochondrial efficiency affects the preferred environmental temperature of the fish, in isolation and in social groups
(4) investigate how changes in individual mitochondrial efficiency with temperature affect leader-follower dynamics, foraging and predator-avoidance, and social learning.
Methods will follow those used successfully in other contexts by the supervisor team in their previous work (see references below).

Project Timeline

Year 1

Literature review, training in animal handling and application for Home Office personal licence. Training in experimental techniques (mitochondrial and whole animal respiration, swim tunnel, temperature choice chamber, behavioural assays). Experiments designed to test Q1.

Year 2

Further experimental work to test Q2-4; analyse data and write up initial experiments for publication. Presentation of work at conferences.

Year 3

Details of experiments will depend on the outcome of the initial experiments and the interests of the student. Further analysis and write up of experiments for publication and conference presentations.

Year 3.5

Completion of writing up of experimental work and submission of thesis; further submission of papers for publication.

& Skills

In addition to teaching generic skills such as communication (verbal, social media, written) to scientific and lay audiences, this project will provide a broad training in behavioural, ecological, physiological and cellular techniques. In addition to learning about experimental design and statistical analysis, the student will learn how to quantify behaviour (e.g. sociability, temperature preference through use of dynamic choice chambers), automated tracking of animal movements, measure whole animal performance (e.g. swimming endurance, minimum and maximum metabolic rate) and cellular traits (e.g. mitochondrial function using high resolution respirometry).

References & further reading

Dawson, N.J., Millet, C., Selman, C. & Metcalfe, N.B. (2022) Inter-individual variation in mitochondrial phosphorylation efficiency predicts growth rates in ectotherms at high temperatures. FASEB Journal, 36, e22333.

Killen, S.S., Marras, S., Steffensen, J.F. & McKenzie, D.J. (2012) Aerobic capacity influences the spatial position of individuals within fish schools. Proceedings of the Royal Society Biological Sciences Series B, 279, 357-364.

Killen, S.S., Nadler, L.E., Grazioso, K., Cox, A. & McCormick, M.I. (2021) The effect of metabolic phenotype on sociability and social group size preference in a coral reef fish. Ecology and Evolution, 11, 8585-8594.

McLean, S., Persson, A., Norin, T. & Killen, S.S. (2018) Metabolic costs of feeding predictively alter the spatial distribution of individuals in fish schools. Current Biology, 28, 1144-+.

Metcalfe, N.B., Van Leeuwen, T.E. & Killen, S.S. (2016) Does individual variation in metabolic phenotype predict fish behaviour and performance? Journal of Fish Biology, 88, 298-321.

Salin, K., Auer, S.K., Rey, B., Selman, C. & Metcalfe, N.B. (2015) Variation in the link between oxygen consumption and ATP production, and its relevance for animal performance. Proceedings of the Royal Society B-Biological Sciences, 282, 20151028.

Salin, K., Villasevil, E.M., Anderson, G.J., Lamarre, S.G., Melanson, C.A., McCarthy, I., Selman, C. & Metcalfe, N.B. (2019) Differences in mitochondrial efficiency explain individual variation in growth performance. Proceedings of the Royal Society B-Biological Sciences, 286, 20191466.

Ward, A. & Webster, M. (2016) Sociality: the Behaviour of Group-Living Animals. Spring International Publishing AG, Switzerland.

Webster, M.M., Whalen, A. & Laland, K.N. (2017) Fish pool their experience to solve problems collectively. Nature Ecology & Evolution, 1, 0135.

Further information from Neil Metcalfe (neil.metcalfe@glasgow.ac.uk), Mike Webster (mmw1@st-andrews.ac.uk) or Shaun Killen (shaun.killen@glasgow.ac.uk)

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