Background

Full Title: The evolutionary ecology of individual variation in cognitive performance (Marie Curie Career Integration Grant 334383)

Understanding cognition – defined as the mechanisms by which animals acquire, process, store and act upon information from the environment – has for several decades been a major objective in biology and psychology. Establishing whether the nature of cognition is qualitatively different across humans and non-human animals generally has been a main aim in these fields. Another has been to identify proximate causes of variation in cognitive performance. More recently significant progress has been made in understanding the evolution of cognition, identifying ecological and social selective pressures responsible for variation in cognitive performance and neural substrate size. Most of this progress has been achieved using a comparative approach across species, or with captive insect populations, but the evolutionary and ecological processes that shape individual variation in cognitive performance have scarcely been investigated in the wild.

This proposal takes the disciplines of cognitive and evolutionary biology into a natural setting to explore a variety of causes and consequences of individual variation in cognitive ability (Figure 1). In the first work package, the aim is to examine how individual differences in three indicators of cognitive ability arise, how these differences are linked to life history variation, whether this necessarily leads to selection for higher cognitive performance, and whether the observed patterns are dependent on the environment or moderated by other sources of phenotypic variation. In the second work package, the aim is to explore the functional mechanisms underlying links between cognitive ability and life history variation.

Work package 1: THE EVOLUTIONARY AND ECOLOGICAL PROCESSES THAT SHAPE INDIVIDUAL VARIATION IN COGNITIVE ABILITY

Understanding the proximate factors underlying phenotypic variation is a fundamental aim of evolutionary ecology. Proximal research on cognition has focussed on a variety of topics, from intrinsic individual differences in ability linked to quantitative genetic and environmental sources of variation, and neural substrate size, to differences in performance linked to temporary environmental effects, individual state differences and social factors. For example the ‘necessity drives innovation’ hypothesis is often proposed as a major cause of variation in cognitive performance, predicting that sub-dominant classes are more likely to innovate and perform better on cognitive tasks. Similarly residual brain size is often expected to predict cognitive ability, but these predictions are rarely tested in natural populations. From an evolutionary perspective, given the basic expectation that higher cognitive ability is likely to have functional benefit, it remains unclear why individuals vary in this respect. One dominant hypothesis is that such variation is adaptive: although high ability may allow animals to occupy more cognitively demanding niches, this may also come with costs, for example pleiotropic trade-offs with other traits. Experiments on captive insect populations and common garden experiments suggest that adaptation to local environmental conditions mediated by trade-offs may indeed influence cognitive ability. Similar evidence at the individual level from the wild is lacking. Arguably the main reason for this is that characterising variation in cognitive ability in wild populations, and linking this to life history variation, controlling for crucial confounding effects caused by environmental variation and covariation with other phenotypic traits, is logistically and technically challenging. This work-package aimed to overcome these challenges across a number of objectives.

Work package 2: THE BEHAVIOURAL MECHANISMS UNDERLYING LINKS BETWEEN COGNITIVE ABILITY AND LIFE HISTORY VARIATION

Empirical evidence suggests that cognitive ability influences how well individuals secure functionally important resources and make important decisions. Nevertheless with few exceptions to date most of this work has been done under laboratory conditions and the extent to which cognitive ability influences functionally important behaviour, with demonstrated direct consequences for life history variation and fitness under natural conditions, remains largely unclear. One of the most widespread and basic expectations is that cognitive ability influences how effectively individuals exploit their environment when foraging, for example by influencing where they choose to forage, how quickly food is found and what to feed on, all of which are expected to influence foraging efficiency and diet diversity. Nevertheless foraging success may not necessarily increase with cognitive ability, which has also been negatively correlated with realized competitive ability. Since realized competitive ability can come with costs (e.g. associated with direct conflict over resources), variation in cognitive and competitive abilities may represent alternative strategies in an unpredictable heterogeneous environment. This workpackage proposed to use a variety of experimental and observational approaches to investigate how individual cognitive profiles (problem solving and associate learning performance, and brain size) explain foraging success in the wild, and how these effects might be moderated by other phenotypic variation (personality, bill morphologies), and by ecological conditions.

Outputs directly related to the Marie Curie CIG

R1) O’Shea, W. Serrano, E. & Quinn, J.L. (in press). Do personality and innovativeness influence competitive ability? An experimental test in the great tit. Behavioral Ecology.

R2) O’Shea, W. 2017. The Evolutionary Ecology of Personality and Life History Variation in an Anthropogenic Heterogeneous Landscape. University College Cork (submitted PhD thesis, pending examination).

R3) L Zandberg, JL Quinn, M Naguib, K Van Oers (2017). Personality-dependent differences in problem-solving performance in a social context reflect foraging strategies. Behavioural Processes 134, 95-102.

R4) Quinn JL, Cole EF, Reed TE, Morand-Ferron J. 2016. Environmental and genetic determinants of innovativeness in a natural population of birds. Phil. Trans. R. Soc. B 2016 371 20150184; DOI: 10.1098/rstb.2015.0184.

R5) Serrano, E., O’Shea, W. & Quinn, J.L. (in minor revision). Individual foraging preferences are linked to  innovativeness and personality in the great tit. Ecol. Socio.

R6) O’Shea, O’Halloran and Quinn, J.L. (in review Oecologia). Phenology, provisioning behaviour, and unusual patterns of life history variation across an anthropogenic heterogeneous landscape.

Note that R3 contains two prepared but as yet unpublished papers that have been supported by this grant.

Papers arising from or associated with the Marie Curie CIG during the project

R7) Reichert, M. & Quinn, J.L. (in press). Cognition in contests: mechanisms, ecology and evolution. TREE.

R8) Quinn, J.L. (2015), Animal personality meets community ecology: founder species aggression and the dynamics of spider communities. J Anim Ecol, 84: 1457–1460. doi:10.1111/1365-2656.12435.

R9) Morand-Ferron, J. & Quinn, J.L. (2015). The evolution of cognition in natural populations. Trends in Cognitive Science. 19:235-237.

R10) Morand-Ferron J, Hamblin S, Cole EF, Aplin LM, Quinn JL (2015) Taking the Operant Paradigm into the Field: Associative Learning in Wild Great Tits. PLoS ONE 10(8): e0133821. doi:10.1371/journal.pone.0133821

R11) Morand-Ferron, J., Cole, E. & Quinn, J.L. (2015). Studying the evolutionary ecology of cognition in the wild: a review of practical and conceptual challenges. Biological Reviews 91:367-89. doi: 10.1111/brv.12174.

R12) Quinn, J.L., Cole, E.F. and Morand-Ferron, J. 2014. Studying micro-evolutionary processes in cognitive traits: a comment on Rowe and Healy. Behavioural Ecology 25: 1297-1298.

Talks delivered

• President’s Symposium at the Animal Behavior Society, Princeton, August 2014 (invited speaker).
• NUIG, Department of Zoology, Studying personality and cognitive traits in a wild bird population” November 2014 (invited seminar).
• Trinity College Dublin, January 2013 (invited seminar).
• 2nd Nordic Evolutionary meeting in Tartu, Estonia, September 2013 (invited speaker).
• Association for the Study of Animal Behaviour, ZSL, London, December 2012 (invited plenary).
• Mar 2017, University College Dublin, Invited seminar
• August 2016, Ankara, Turkey, Invited plenary for the Ecol & Evol Biol symposium (I withdrew due to coup).
• March 2016, CNRS, Montpellier, Invited Seminar.
• June 2016, ERI Institute, UCC, Cork Ireland. Seminar.
• Feb 2016, Department of Neiurobiology, UCC, Cork. Seminar on my research.
• March 2016, St Andrews University, Conference presentation (coauthor with Will O’Shea)
• November 2016, University of Cambridge, Invited seminar.
• June 2015, School of BEES, UCC, seminar.
• Mar, 2015, “Endurance” conference at UCC, Ireland, invited keynote.
• Mar 2014, Queens University Belfast, Invited seminar.
• International Ornithological Congress, Tokyo, Japan, August 2014 (speaker on one talk and joint speaker on another talk).
• International Society for Behavioural Ecology, New York, 2014 (symposium coorganiser and co-author on two talks by my student and postdoc).
• European Ornithologists Union, UEA, UK, August 2013 (symposium organiser and talk).
• RDS Symposium on Bird Habitats in Ireland; delegate, 18/5/12.
• Excellent Research: Ireland and the ERC, held by Royal Irish Academy in Dublin, 17/11/14, (special invitation).