The field of research into personality and behavioural syndromes in animals has blossomed over the past few decades. With ample evidence for it’s existence, biologists have begun to consider its evolution; what is the adaptive benefit of personality? How are multiple personality types maintained in a population? Why do personalities exist when they sometimes result in maladaptive responses?

All these questions, and any evolutionary questions we might care to ask, make the assumption that personality is heritable. Without heritability, personality cannot be passed from generation to generation, and cannot be subject to natural selection. There is now plenty of evidence for high heritability of many personality traits in animals, although there is also an important influence of the environment too. Heritabilities estimates vary, from 0.22 – 0.61 in wild great tits, 0.32 in social spiders, 0.54 – 0.66 in humans and 0.2 – 0.8 in dumpling squid. These genetic influences may in part be reflected in brain morphology; one study in humans found differences in brain structure relating to neuroticism, conscientiousness, and extraversion. More neurotic people have a smaller total brain volume and a smaller frontotemporal surface area, whilst extraverts have a thinner inferior frontal gyrus.

Ok, so personality exists in animals, and it is heritable. How can we explain the evolution of personality when intuitively, greater behavioural plasticity and thus adaptability should be favourable? There is still no definitive answer to this one, but we have lots of ideas. If multiple different personality alleles (variants of a gene) are to be maintained in a population, they must have more or less the same fitness. I say more or less because it only has to be the same overall, across all individuals, across environments (both natural and social) and across a reasonably long period of time (a few generations, say). Thus explanations for personality try to provide reasons for which different behavioural types may be equally fit.

A fitness effect of personality type has been demonstrated for a variety of species; in great tits and zebra finches, proactive-reactive personality traits such as neophobia and exploration correlate to social dominance, which offers access to food and mates. In female baboons, personality is predictive of mate bonding, which is likely to predict reproductive success. And at the super-organism level, defensive response, foraging activity and undertaking behaviours are all related to colony productivity and winter survival in honeybees (Apis mellifera).

Variability

It seems quite intuitive to assume that different personality traits might be beneficial in different circumstances. If this is the case, then any temporal or spatial variation in an animal’s environment could maintain several different personality types in the population. As long as animals were interbreeding across environments, different personalities would thrive in different areas (or generations) averaging out to similar fitness for all types. In wild great tits, different personality types were successful indifferent years, as climatic and other environmental influences changed.

Life History

Alternatively, personality could arise if different behavioural syndromes represent different life-history strategies, each entailing different costs and benefits which re­sult in equivalent fitness. This idea suggests that each personality or syndrome type is a trade-off; this could be a trade-off between current and future reproduction or one between growth and mortality, for example. Under this view, proactive individuals might represent a ‘live fast, die young strategy’ – being bold and aggressive, they may be more likely to find females but also more likely to be eaten. Reactive individuals take a more considered, ‘a penny saved…’ strategy, investing in future success. There is some support of this in the literature; personality and anti-predator behaviour are correlated in chaffinches and proactive quail (Coturnix japonica) grow faster as reach sexual maturity earlier. In general, bolder individuals have higher annual reproductive success, but a shorter life-span.

Frequency Dependent Selection

Another promising explanation is that person­ality types are subject to frequency-dependent selection. Frequency-dependent selection is a theoretical selection regime, bourne out of the game theoretic approach to evolutionary biology. Under frequency-dependent selection, the fitness of a particular allele depends upon its prevalence in the population. This can occur if success at a particular activity (such as competing for a mate) is dependent upon not only an individual’s personality, but also the personality of it’s opponent. (Of course frequency-dependent selection can apply to any trait, not just personality!)

This is the premise of the hawk-dove game, which postulates two behavioural types that vary in aggression, competing over a food source. The aggressive hawk beats the passive dove in a contest, however when two hawks meet they engage in an escalated fight which is costly to both. By contrast, when two doves meet they share the reward (awww). Hawks do well in populations of mostly doves, but their advantage starts to disappear as their numbers increase, as they more frequently encounter other hawks and suffer the costs of fighting. Thus we expect the population to settle at some kind of stable polymorphism: the state at which both behavioural types are equally successful. Models of the hawk-dove game can produce behaviourally poly­morphic populations, however they are equally likely to produce a monomorphic population with individuals exhibiting behavioural plasticity. It is not currently clear under what circumstances selection may favour one over the other

It’s in the Mix

Further hints of the hawk-dove game in animal personality come again from the social animals. Evidence from several different species indicates that a balance of several different personality types within a social group is beneficial. Social spider groups with a mix of aggressive and non-aggressive spiders are more successful at capturing prey. In water striders, groups consisting of highly aggressive individuals had lower mating success, while the most successful groups contained a mixture of be­havioural types. Balance also exists between the sexes; anti-social male spiders (who are also more active and aggressive) enjoy higher mating success, whereas being social is the best strategy for females. Furthermore, fledgling condition in great tits is highest for the offspring of mixed-personality parents (one proactive, one reactive).

Theories explaining personality are not only tasked with explaining how personalities are maintained in the population. They also must explain why personality itself is beneficial over a scenario in which all individuals have the ability to respond in all possible ways, and can response to their environments in a completely plastic manner.

Frequency-dependent selection may also come in handy here. If the hawk-dove game is modified to allow eavesdropping (where individuals can base their behaviour in the current interaction on an observation of their partner’s last interaction), this can lead to selection for consistency, as this reduces the chances of conflict.

An alternate explanation for why individuals might behave consistently is that it is simply too costly to produce behavioural flexibility. DeWitt, Sih and Wilson (1998) list a variety of potential costs and limits to plasticity, including production and mainte­nance costs, information acquisition costs, genetic costs, lag-time limits, and limits to the quality and range of behaviours that can be produced within a plastic organism. Environmental variability, either spatial or temporal, is likely to increase the costs associated with plasticity, because responding adaptively to one aspect of the current environment may reduce an individuals level of adaptation to another part. Similarly, if it is difficult to obtain accurate informa­tion about current and future conditions, it may be beneficial to behave consistently rather than make mistakes.

An Evolutionary Perspective on Personality

Consistent individual differences in behaviour are widely apparent in the animal kindgom, are often highly heritable and show measurable effects on reproductive fitness. Explaining the evolution and maintenance of personality is still an active area of research, but there are now many plausible explanations available. Evolutionary biologists are tasked with explaining the lack of behavioural flexibility seen in nature (why are individuals consistent?), as well as the continued occurrence of multiple different personality types (why are individuals different?). The maintenance of multiple behavioural types indicates that each type must, in the long-term, have equivalent fitness. This could occur due to variation in the benefits and costs associated with each personality type across different conditions, if these too vary over space or time. Alternatively, the social environment could be important, if the success of a personality type depends upon the personality type of its neighbours, then frequency-dependent selection could maintain a balance of different individuals in the population. Correlated suites of personality traits could represent alternative life history strategies (live fast, die young vs a penny saved is a penny earned), and these may be informed by condition or experience in early life.

Although game theory predicts that multiple different behaviours can be maintained together in a population, this is equally likely to occur through behaviourally flexible individuals (intra-individual variation) as through distinct behavioural types (inter-individual variation). However, personality may be favoured if consistency (and therefore predictability) reduce the chances of escalated fights, or if environmental variability makes behavioural plasticity costly.

Articles in this Series:

1. Animal Personality Part I: Individual Differences
2. Animal Personality Part II: The Evolution of Personality

Want to Know More?

• Bell (2007) Animal Personalities. Nature (447), 539 – 540
• Dingemanse and Reale (2005) Natural selection and animal personality. Behaviour (142), 1159 – 1184
• Sih, Bell and Johnson (2004) Behavioural syndromes: an ecological and evolutionary overview. TREE (19), 372 – 378
• Dall, Houston and McNamara (2004) The behavioural ecology of personality: consistent individual differences from an adaptive perspective. Evology Letters (7), 734 – 739
• Carere and Eens (2005) Unravelling animal personalities: how and why individuals consistently differ. Behaviour (142), 1149 – 1157
• Bjornebekk et al (2012) Neuronal correlates of the five factor model (FFM) of human personality: Multimodal imaging in a large healthy sample. NeuroImage
• Dren, Van Oers and Van Noordwijk (2002) Realised heritabilities of personalities in the great tit (Parus major). Proceedings of the Royal Society London B (270), 45 – 51
• Wray, Mattila and Seeley (2011) Collective personalities in honeybee colonies are linked to colony fitness. Animal Behaviour (81), 559 – 568
• Dingemanse et al(2003) Fitness consequences of avian personality in a fluctuating environment. Proceedings of the Royal Society London B (271), 847 – 852
• DeWitt, Sih and Wilson (1998) Costs and limits of phenotypic plasticity. TREE (13), 77 – 81
• Sih and Watters (2005) The mix matters: behavioural types and group dynamic in water striders. Behaviour (142) 1417 – 1431
• Seyfarth, Silk and Cheney (2012) Variation in personality and fitness in wild female baboons. PNAS (109), 16980 – 16985