Combining animal personalities with transcriptomics
resolves individual variation within a wild-type
zebrafish population and identifies underpinning
molecular differences in brain function
S. REY,*
1
S. BOLTANA,* †
1
R. VARGAS,* N. ROHER* and S. MACKENZIE* †
*Institut de Biotecnologia i Biomedicina, Universitat Auto `noma de Barcelona, Barcelona, 08193 Bellaterra, Spain, †Institute of
Aquaculture, University of Stirling, Stirling, Stirlingshire FK9 4LA, UK
Abstract
Resolving phenotype variation within a population in response to environmental
perturbation is central to understanding biological adaptation. Relating meaningful
adaptive changes at the level of the transcriptome requires the identification of pro-
cesses that have a functional significance for the individual. This remains a major
objective towards understanding the complex interactions between environmental
demand and an individual’s capacity to respond to such demands. The interpretation
of such interactions and the significance of biological variation between individuals
from the same or different populations remain a difficult and under-addressed ques-
tion. Here, we provide evidence that variation in gene expression between individuals
in a zebrafish population can be partially resolved by a priori screening for animal
personality and accounts for >9% of observed variation in the brain transcriptome.
Proactive and reactive individuals within a wild-type population exhibit consistent
behavioural responses over time and context that relates to underlying differences in
regulated gene networks and predicted protein–protein interactions. These differences
can be mapped to distinct regions of the brain and provide a foundation towards
understanding the coordination of underpinning adaptive molecular events within
populations.
Keywords: proactive, reactive, behaviour, gene expression, variation
Received 18 July 2013; accepted 23 September 2013
Introduction
Understanding phenotypical variation and physiological
regulation during acclimation to external stimuli varia-
tion is a central issue in biology and underpins evolu-
tionary studies. In most studies across the biological
sciences, individuals within groups are considered as
simple replicates, and interindividual variation is
actively minimized, for example, using specific genetic
backgrounds. Such practice is commonplace in biology
and reflects the difficulties in understanding variation
and the prevalence of an approach often centred upon
differences between mean values of measured variables
for a population. However, it is common to observe sig-
nificant levels of variation, standard deviation, in many
different types of data that more probably obscure the
underlying individual differences that may have poten-
tial biological significance. Such an approach therefore
cannot be used to understand the underlying interac-
tions between individuals and their environment. Over
the past few years, an increasing interest in the diver-
sity of behavioural phenotypes and their consistency in
and between individuals within a population has
emerged (Sih et al. 2004; Wolf et al. 2007). This has been
accompanied by a growing nomenclature including
individual coping style, personality and behavioural
Correspondence: S. MacKenzie, Fax: + 44 (0) 1786 472133;
E-mail: Simon.Mackenzie@stir.ac.uk
1
These two authors contributed equally to the manuscript.
© 2013 John Wiley & Sons Ltd
Molecular Ecology (2013) 22, 6100–6115 doi: 10.1111/mec.12556