Demystifying animal ‘personality’ (or not): why individual variation matters to experimental biologists

Abstract

Animal 'personality', defined as repeatable inter-individual differences in behaviour, is a concept in biology that faces intense controversy. Critics argue that the field is riddled with terminological and methodological inconsistencies and lacks a sound theoretical framework. Nevertheless, experimental biologists are increasingly studying individual differences in physiology and relating these to differences in behaviour, which can lead to fascinating insights. We encourage this trend, and in this Commentary we highlight some of the benefits of estimating variation in (and covariation among) phenotypic traits at the inter-and intra-individual levels. We focus on behaviour while drawing parallels with physiological and performance-related traits. First, we outline some of the confusion surrounding the terminology used to describe repeatable inter-individual differences in behaviour. Second, we argue that acknowledging individual behavioural differences can help researchers avoid sampling and experimental bias, increase explanatory power and, ultimately, understand how selection acts on physiological traits. Third, we summarize the latest methods to collect, analyse and present data on individual trait variation. We note that, while measuring the repeatability of phenotypic traits is informative in its own right, it is only the first step towards understanding how natural selection and genetic architecture shape intra-specific variation in complex, labile traits. Thus, understanding how and why behavioural traits evolve requires linking repeatable inter-individual behavioural differences with core aspects of physiology (e.g. neurophysiology, endocrinology, energy metabolism) and evolutionary biology (e.g. selection gradients, heritability).

Circadian Rhythms of Urinary Cortisol Levels Vary Between Individuals in Wild Male Chimpanzees: A Reaction Norm Approach

“…In Budongo forest the Sonso community was studied, whereas for Taï data on three groups (East, North, and South group) were available. Both are long-term field sites, with systematic observations starting in Taï in 1982 (Boesch and BoeschAchermann, 2000), and in Budongo in 1990 (Reynolds, 2005). The two long-term field sites keep track of demographic changes in the chimpanzee communities and record rainfall and temperature measurements.…”

“…Individual variation in a trait represents the raw material for natural selection and the stability of differences between individuals impacts the efficiency of adaptive responses to selection (Roche et al, 2016). Between individual variation in a trait is generated by differential exposure to relatively stable environmental factors, such as mothering styles (see for instance Liu et al, 1997;Francis and Meaney, 1999;Caldji et al, 2000), or by heritable differences between individuals (Dingemanse et al, 2010b;Forsman, 2015;Westneat et al, 2015).…”

Does the field of animal personality provide any new insights for behavioral ecology?

“…These terms have a greater or lesser link to existing fields but are placed under the umbrella of "animal personality" (David and Dall 2016;Roche et al 2016). Such a wild growth in terminology is clearly not conducive to advancement of the field, a point made earlier by others (Dall and Griffith 2014;David and Dall 2016;Roche et al 2016), but it is not the precise definitions that are of concern, but rather whether any new insight is gained from them at all. In our view, the main advance achieved by the field of animal personality is the increased use of rigorous quantitative methods to describe variance in measures of animal behavior.…”

“…In our view, this has resulted in "animal personality" studies becoming nothing more than a rebranding of existing fields of research-fields that are far more solidly grounded and hypothesis driven than the often vague and superficial focus on animal personalities. Dochtermann, et al 2010;Mathot et al 2012;Roche et al 2016). In fact, the need to quantify consistent behavioral differences has led to a separate field that has been described as "behavioral ecology of variance components," which traces its origins to the statistical framework employed in quantitative genetics (Dingemanse and Dochtermann 2014;Araya-Ajoy et al 2015;Westneat et al 2015).…”

“…In fact, the need to quantify consistent behavioral differences has led to a separate field that has been described as "behavioral ecology of variance components," which traces its origins to the statistical framework employed in quantitative genetics (Dingemanse and Dochtermann 2014;Araya-Ajoy et al 2015;Westneat et al 2015). Our criticism of the field of animal personality lies in its appropriation of existing methodological frameworks while maintaining that it constitutes an independent research field (Roche et al 2016). If the field now relies heavily on existing frameworks, we question the additional value of continuing the use of "animal personality.…”