In principle, a behavioural syndrome might include behavioural tendencies exhibited in any functional context such as feeding, antipredator, mating, competitive contest, cooperative, parental care and dispersal. Studying multiple contexts requires either less effort devoted to studying each context in detail or having the resources to conduct a substantially larger overall project. A fundamental issue for the study of behavioural syndromes is thus the problem of choosing which behaviours or contexts to study. In what follows, I describe the strengths and weaknesses of four different strategies that are currently being used to choose which behaviours or contexts to study in a behavioural syndromes view. These strategies are complementary and the description here is meant to help guide empirical approaches for researchers interested in including behavioural syndromes in their research programme.
One approach for studying behavioural syndromes starts with a puzzling behaviour. For example, precopulatory sexual cannibalism is mysterious from an evolutionary point of view because females eat their potential mates before mating with them, and therefore might produce unfertilized clutches. Based on a suggestion by Arnqvist & Henriksson (1997)
, Johnson & Sih (2005)
hypothesized that precopulatory sexual cannibalism was a ‘spillover’ of aggressiveness from a context in which it is beneficial. They showed that female spiders differed in their tendency to behave cannibalistically before copulation, and the females that showed this behaviour were also the individuals that were especially voracious towards food items as juveniles, resulting in faster growth and increased fecundity. Therefore, the benefits of high levels of voracity during the juvenile period might outweigh the costs of excessive aggressiveness later in life. The potential for behavioural spillovers across contexts to result in suboptimal behaviour is well illustrated by several other studies (e.g. Sih et al. 2003
; Quinn & Cresswell 2005
; Sih & Watters 2005
; Duckworth 2006
The strength of the ‘puzzling behaviour’ approach for studying behavioural syndromes is that it can potentially provide a satisfying explanation for a mysterious behaviour. This approach is probably best undertaken when a behaviour has benefits in some contexts but costs in others. In the case of the spiders, aggression is favoured when resources are scarce, but has obvious costs in terms of exposure to risk and enemies.
The second approach for studying behavioural syndromes involves looking for relationships between behaviours that have already been shown to form part of a syndrome in other animals (‘the candidate behaviour approach’). For example, individual differences along the shy–bold axis (Wilson et al. 1993
; Coleman & Wilson 1998
) and the proactive–reactive axis (Koolhaas et al. 1999
), as well as individual differences in ‘aggressiveness’ (Huntingford 1976
; Benus et al. 1991
; Riechert & Hedrick 1993
), neophobia (Cavigelli & McClintock 2003
; Keltikangas-Jarvinen et al. 2004
) and exploratory behaviour (Verbeek et al. 1994
) have all been documented in a diverse array of organisms. The advantage of this approach is that it allows us to build upon knowledge gained from other organisms, and could potentially reveal if there are fundamental axes of variation common across species and that affect behaviour in predictive ways. For example, individual differences in rates of processing information, from careful and attentive to cursory and fast, are probably widespread among animals. This fundamental axis might explain why, in many species (Benus et al. 1991
; Koolhaas et al. 1999
; Steimer & Driscoll 2003
; Ebner et al. 2005
; Overli et al. 2005
), fast explorers are also quick to attack others and readily form routines.
The disadvantage of this approach is that it can be difficult to identify different manifestations of the same behavioural tendency, and the way in which a particular behaviour can be measured might vary greatly across different types of organisms. For instance, several different behaviours have been termed ‘bold’, such as predator inspection behaviour (Dugatkin 1992
), behaviour in an open field (Gosling 2001
) or feeding under risk (Bell 2005
), but it is an open question as to whether each of these behaviours are equivalent and correlated with other behaviours in the same way. Similarly, established protocols for measuring exploratory behaviour (e.g. Verbeek et al. 1994
) might not be appropriate for all organisms. That is, the relevance of what we perceive as the same situation might not be the same for different kinds of animals, and the behaviours might be incommensurable across species, i.e. the ‘jingle-jangle fallacy’ (Gosling 2001
A third approach for studying behavioural syndromes is from the proximate perspective; this approach is from the ‘bottom-up’ and starts with systems (neuroendocrine or genetic) that integrate environmental stimuli and have pleiotropic effects, and then looks for relationships between behaviours that we suspect are affected by those systems. For example, the manifold consequences of testosterone for male birds are well appreciated: testosterone affects aggressive behaviour, singing, courtship, spermatogenesis and parental care (Ketterson & Nolan 1999
). Other important pathways such as hormones involved in the stress response (Romero 2004
) or genes with strong pleiotropic effects (e.g. Sokolowski et al. 1997
) are promising links that could tie together packages of behaviours. The bottom-up approach is particularly powerful because it not only can explain why syndromes occur (because the behaviours share a common mechanism) but also makes clear predictions about which behaviours are likely to be correlated (the ones that share the same causal connection). The disadvantage of this approach is that it overlooks correlated behaviours that affect fitness but that do not share a common mechanism, where the correlation results from linkage disequilibrium rather than pleiotropy (Conner 2002
). As such, the bottom-up approach might inadvertently guide the course of research away from adaptive suites of trait that are the outcome of coordinated selection on independent traits.
In fact, some of the most intriguing behavioural syndromes occur when the constituent behaviours are, to the scientist's knowledge, neither functionally nor mechanistically related. For example, male crickets that produce long songs, which are attractive to both females and predators, are more cautious in a novel environment (Hedrick 2000
). An unexplored but potential explanation for this behavioural syndrome is that it is the product of correlational selection, which occurs when certain combinations of traits are favoured over others. That is, attractive and cautious males might have higher fitness than attractive and bold males or unattractive and cautious males, because they reap the benefits of increased mating success while also minimizing the costs of exposure to predation. While the fitness consequences of certain behavioural types have been documented (Reale & Festa-Bianchet 2003
; Dingemanse et al. 2004
; Dingemanse & Reale 2005
; Smith & Blumstein submitted
) and we know that correlational selection can favour certain combinations of morphological and behavioural traits (Brodie 1992
; Forsman & Appelqvist 1998
; Sinervo et al. 2001
; McGlothlin et al. 2005
), no study (to my knowledge) has yet explicitly measured correlational selection for a behavioural syndrome. This is a promising area for future investigation.
One of the strongest arguments for how behavioural ecologists can contribute to the study of animal personality and temperament is that, as a discipline, we are especially attuned to the relevant ecological factors affecting an organism and are therefore well situated to take a functional approach (Reale et al. submitted
). This sensitivity can point to behaviours that are most relevant to the ecology of the species and that have fitness consequences. Therefore, the fourth approach for studying behavioural syndromes starts with the particular details of the ecology of the species in question (‘the ecological approach’). For example, perhaps sexual conflict is really strong, or predation pressure is very high, or the animal is a cooperative breeder, but individuals vary in how they behaviourally respond to these pressures. An ecological approach to studying behavioural syndromes asks whether there are correlated behaviours that might help explain individual variation in these fitness-related traits. Arguably, behavioural syndromes are most interesting when they are surprising or non-intuitive. It might not be surprising, for example, that an individual's level of aggressiveness might be related to its dominance rank (Huntingford & Turner 1987
), but it is more unusual to think that individual differences in mating behaviour might be related to individual differences in cooperative tendency, for example.
The advantage of this approach is that it is, by definition, studying traits that are ecologically important, and it automatically prompts interesting questions about what is maintaining variation in these fitness-related traits. The disadvantage of this approach is that if we start looking for relationships between all the ecologically relevant behaviours for a given species that we can think of measuring, we could spend a lot of time on a ‘fishing expedition’, looking in the wrong direction and prone to type 1 errors. However, until theory can predict when and why certain behaviours should be correlated, we should entertain the possibility that some correlations are going to be unexpected and that new insights will emerge from considering relationships among behaviours rather than focusing on them one at a time. This point is well illustrated by evolutionary genetic studies that have found unexpected genetic correlations between seemingly unrelated traits, such as sperm motility and lung capacity (Henderson 1990
) or between coat colour and fearfulness in foxes (Trut 1999