The Bold and the Spineless: Invertebrate Personalities

The bold and the spineless: Invertebrate personalities

Jennifer A. Mather1 and David M. Logue2

1 Department of Psychology, University of Lethbridge, AB, Canada

2 Department of Biological Sciences, University of Lethbridge, AB, Canada

Reviewing the study of personalities of invertebrates offers a series of challenges.First and most importantly, there are a huge number of invertebrate species, sometimes estimated to represent 98% of the animal species on the planet (Pechenik 2000).Invertebrates exhibit a tremendousarray of life history strategies, developmental trajectories, modes of reproduction and physiological bases of behavior, many of which are poorly known.Another challenge arises from the diversity of perspectives and research backgrounds that characterize invertebrate personality researchers. Researchers from different fields often use different terms to describe suites of correlated behaviors (e.g., axes of personality, behavioral syndromes).Gosling (2001), who conducted a wide-ranging survey of animal personalities, emphasized consistency by defining personality as “those characteristics of individuals that describe and account for consistent patterns of feeling, thinking and behavior” (p 46).Thoughts and feelings of invertebrates and other animals are not measurable, sowe will focus on behavior and to a lesser degree physiology, recognizing that we may be ignoring certain inaccessible processes that contribute to personality. Sih and colleagues (2004) use the term ‘behavioral syndromes’, which they define as “suites of correlated behaviors” (p 242).Groothuis and Carere (2005) meld these ideas into a concept called ‘behavioral profile’ (p. 139), which describes differences between individuals that are more-or-less consistent over time and includemore than one feature.

In keeping with the theme of this volume, we rely primarily on the term ‘personality’, but emphasize that we are interested in both consistent individual differences and suites of correlated behaviors. Thus for a species to qualify as exhibiting personality, behavioral tendencies must differ among individuals and behavior must be correlated across contexts. One of the goals of this review is to determine the degree to which invertebrates, often viewed as animals of limited behavioral repertoires, exhibit personality thus defined.We begin with a survey of reports that relate to personality in invertebrates. We categorize these as 1) descriptive, 2) physiological/genetic linkages (see van Oers et al. 2005), 3) ontogenetic studies (sensu West-Eberhard 2003) and 4) ecological/selection studies (Groothuis & Carere 2005; Smith & Blumstein 2008).There will be some bias towards papers that represent under-studied groups, even if their evidence is fragmentary.We then evaluate particularly thorough and influential research programs in depth.In the final section, we provide recommendations for future research directions and attempt to summarize the current state of the field.

This review does not evaluate the division of labour (polyethism) in colonies of social insects, or the discrete morphologies (polyphenism) found in many invertebrates. Although we recognize that both of these phenomena relate to our definition of personality, we have chosen to focus on subtler forms of personality (i.e., those that form continuous rather than discrete distributions). We refer readers interested in polyethism and polyphenism to reviews by Beshers and Fewell (2001) and Emlen and Nijhout (2000), respectively.

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Table 1.Studies of invertebrates that assess individual differences and/or correlated behaviors.

Authors / Species/
Group / Category / Study design / Results / Comments
de Bono & Bargmann 1998 / Caenorhabdita worm / physiological/
genetic / 1 measure of activity in 2 morphotypes / Activity is controlled by mpr-1 gene / One behavior
Turner et al. 2006 / Physa snail / ecological/
selection / 2 measures of antipredator behavior across experience levels / Mostly inherited, a little learned / One situation
Mather & Anderson 1993 / Octopus cephalopod / descriptive / 19 behaviors in 3 contexts over 2 weeks / 3 dimensions (activity reactivity avoidance) / Descriptive
Sinn et al. 2001 / Octopus cephalopod / ontogenetic / 15 behaviors in 3 contexts over 6 weeks / 4 components, development program / Early lifespan
Sinn & Molschaniwskyj 2005 / Euprymna squid / physiological/
genetic / 12 behaviors in 3 contexts and morphological characteristics / Four axes of variation, all context-specific / Lab
Sinn et al. 2006 / Euprymna squid / ecological/ selection / 12 behaviors in 2 contexts, and heritability of behavior / Heritability greater for antipredator behavior than foraging / Lab
Sinn et al. 2008 / Euprymna squid / ontogenetic / 10 behaviors relating to shy-bold dimension in 2 contexts over 13 weeks / Different correlations across situations/time / One dimension
Sinn et al. in sub / Euprymna squid / ecological/
selection / 10 behaviors relating to shy-bold dimension in 2 contexts in 2 populations over 2 years / Personality structure varied by population and year / One dimension
Reaney & Backwell 2007 / Uca fiddler crab / ecological/
selection / Activity, aggression and courtship success, over variable time scales / Risk taking predicts courtship success / Males grouped shy or bold
Briffa et al. 2008 / Pagurus hermitcrab / descriptive / 1 behavior relating to startle response in 5 contexts over 5 days / Plasticity and consistency / One measure, females
Johnson & Sih 2005 / Dolomedes spider / ecological/
selection / 2 behaviors in 1 and 2 contexts, respectively, over variable time scales / Correlations between contexts and over time suggest behavioral spillover / Females
Johnson & Sih 2007 / Dolomedes spider / descriptive / 1 measure of boldness in 4 contexts and 2 developmental stages / Structure of syndrome changes over development, behaviors correlated between contexts in adults / One female measure
Hedrick & Riechert 1989 / Aglenopsis spider / ecological / selection / 1 measure of fearfulness in 2 populations, in field and F2 in lab / Inherited population differences / Females, one behavior
Riechert & Hall 2000 / Aglenopsis spider / ecological / selection / 1 measure of fearfulness in 2 field populations, reciprocal transplant, and lab-reared / Past selection has produced habitat-specific risk taking / Females, one behavior
Riechert & Hedrick 1990 / Agelenopsis spider / ecological/
selection / 1 behavior each in antipredator and feeding contexts in 2 field populations, and lab-reared / Population differences, between-context correlations in one population / Mostly at population level, females
Riechert & Hedrick 1993 / Agelenopsis spider / descriptive / 1 behavior each in antipredator and agonistic contexts in 2 field populations and lab reared / Contest winners exhibit shorter latencies / Females
Maupin & Riechert 2001 / Agelenopsis spider / physiological/
genetic / 1 behavior in feeding context across 4 populations in 2 habitats, planned crosses / Population differences, sex-linked inheritance / One behavior, mostly at population level
Pruitt et al. in press / Anelosimus
spiders / ecological/
selection / 11 behaviors in 4 contexts and index of sociality in 2 populations / Sociality covaried with behaviors across contexts / Females
Hedrick 2000 / Gryllus crickets / ecological/
selection / 1 behavior in calling context, 2 behaviors in antipredator context, field caught and lab-raised / Tradeoff between calling and antipredator behavior / Males
Kortet et al. 2007 / Gryllus crickets / physiological/
genetic / 3 antipredator behaviors, 2 physiological measures, 3 populations / Correlation pattern differ populations, mixed evidence for immune / antipredator tradeoff / Males mostly population
Kortet & Hedrick 2007 / Gryllus crickets / ecological/
selection / 2 behaviors in antipredator context, success in agonistic context, all lab reared / Positive correlation between boldness and contest winning / Males mostly population
Despland & Simpson 2005 / Schistocerca locust / ecological/
selection / 1 behavior in feeding context, 2 phases (solitarious vs. gregarious) / Phases differ in food choice / One behavior
Rutherford et al. 2007 / Enallagma damselflies larval / ecological/
selection / 5 behaviors in antipredator, antiparasite, and mixed contexts / One behavior repeatable across contexts, limited plasticity / Not across time
Weinstein & Maelzer 1997 / Perga sawfly larva / descriptive / 1 behavior in dispersal context, over 12-15 days / 20% are 'leaders’ / One behavior
Nemiroff & Despland 2007 / Malacosoma tent caterpillars / descriptive / 4 behaviors in activity context over 4 days / 2 somewhat discrete levels of activity / Lab
Sokolowski 2001 / Drosophila fly / physiological/
genetic / Genetics and individual behavior review / Review / Gene influence
Higgins et al. 2005 / Drosophila fly / physiological/
genetic / 5 behaviors summed into one measure of activity in 9 isogenic lines / Within group (20%) & between group differences in activity / Behavior observed at group level
Blankenhorn 1991 / Gerris water striders / ecological/
selection / 2 composite measures in foraging context and 2 composite measures in agonistic context over 17 weeks, plus fecundity / Foraging behavior correlated to dominance rank; foraging behavior and to a lesser degree dominance predicted fecundity / Females
Logue et al. in sub / Gromphadorina cockroach / ecological/
selection / 25 behaviors in 5 contexts, morphology and reproductive success / 2 behavioral syndromes, 1 of which predicts reproductive success / Males
Starks & Fefferman 2006 / Polistes wasp / ecological / selection / Game-theoretic model of nest founding / Predicts frequency of alternative tactics given starting conditions / Females, not stable
Retana & Cerda 1991 / Categlyphis ants / descriptive / 20 measures from 5 nests over six months / Activity was variable across group and over time / Observational

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Focal cases

The genetic control of behavior in the fruit fly, Drosophila

Research in behavior of Drosophila fruit flies has made a considerable contribution to our knowledge of individual differences in behavior, even though the researchers conducting this work did not frame their research in terms of personalities per se.Rather, their work attempted to describe genetic influences on physiology and behavior.Sokolowski’s (2001) review of the behavioral genetics of Drosophila is particularly informative to researchers interested in the genetic underpinnings of personality.

Sokolowski (2001) makes it clear that even in flies there are nogenes ‘for’behavior. Rather, genes and the environment interact to determine anatomy and physiology, which in turn influences behavior.Variation in individual genes can influence more than one aspect of an animal’s phenotype – a phenomenon known as pleiotropy (Cheverud 1996).Variation at pleiotropic loci can result in consistent individual differences across multiple contexts - in other words, personalities (Sih et al. 2004).Much of the investigation of the behavior of Drosophila has focused on linking genetic differencesto differences in behavior.Researchers identify a variable locus in the fly genome that covaries with behavior and investigate the physiological pathway that links the genetic variation to differences in behavior.Of the many examples of research along these lines, the following two are particularly good demonstrations of the relationship between genetics and ‘personality’ in fruit flies.

In fruit fly larvae, scientists have found a gene, for, that influences foraging behavior.The R variant of the gene is the dominant allele and the s variant is the recessive one. In the presence of food, rover (Rs or RR) larvae tend to leave a food patch, but sitter larvae (ss) tend to remain (Sokolowski 2001). Natural selection favors rovers in crowded situations and sitters in less crowded ones. In other words, selection for a behavioral strategy is density dependent. Environmental variation can also affect behavior, as food deprivation turns rovers into sitters and other environmental factors can transform sitters into rovers.The difference between the two behavioral types is mediated by a small difference in cGMP-dependent protein kinase activity – on average, rovers have 12% more activity than sitters.The rover-sitter example elegantly demonstrates how one gene can influence individual differences in an important behavior linked to activity.

Several mutations cause male fruit fliesto terminate courtship prematurely.One of the most interesting of these is theduncemutation, which alters learning (Sokolowski 2001).Normal males that have encountered a mated femalesuppress courtship for three hours. The mechanism of this courtship suppressionisolfactory-based avoidance learning. Dunce males, however, do not exhibit olfactory-based avoidance associative learning and so do not suppress courtship.Learning suppression by this mutation (likely due to alteration in the mushroom bodies of the brain) couldhave pleiotropic effects.If, as seems likely, these effects influence behavior in more than one context and persist over time, pleiotropy would be causally linked to personality.

Studies of the for and dunce loci illustrate how relatively minor genetic variation can cause persistent, context-general differences in behavior, which might be measured as personality. Findings from such studies, however, should not be taken as evidence that genetic variation, rather than environmental variation or gene-by-environment interaction, is the primary determinant of personality in fruit flies. Higgins, Jones and Wayne (2005)studied “activity” in groups of flies derived from nine isogenic (i.e. genetically identical except for sex) lines.They found that less than 15% of variation in summed activity was due to lineage. A group-within-lineage effect accounted for over 20% of the variation in activity, suggesting an important contribution of social environment to activity.Phenotypic plasticity – the interaction between genes and the environment – explained another 11% of the variation in activity, meaning that various lineages responded differently to different environments. Interestingly, there were significant differences in the specific behaviors that contributed to activity (feeding, grooming, resting and walking) among different lines, so a summed activity measure may not do justice to the complexity of the problem.

Foraging-predation tradeoffs in the Western grass spider, Agelenopsis aperta

The field of behavioral ecology is defined by its hypothesis-driven, evolutionary approach to behavior.Whereas personality psychologists emphasize holism, behavioral ecologists often focus on specific behavioral traits and develop models that predictan individual’s optimal behavior in a given set of circumstances.For example, a well known optimal foraging model describes optimal prey choice (i.e., the prey type that will maximize a predator’s energy intake) given the profitability, search time, and handling time of each potential prey type (Stephens & Krebs 1986). Behavioral ecologists’ interest in optimal behavior stems from the fact that natural selection shapes behavior in ways that tend tomaximize an individual’s fitness over evolutionary time.

Using optimal foraging theory as an example, suppose that foraging preference (for prey A versus prey B) differs among individuals and covaries with boldness in the presence of predators, such that bolder individuals tend to prefer prey A. Optimal foraging theory does not consider individual differences because it assumes that all individuals behave optimally; if A is the optimal prey, all individuals should choose A until it is depleted to the point that B becomes the optimal choice. Further, optimal foraging theory treats foraging as a context-specific behavior, whose fitness consequences are independent of behavior in other contexts. If prey choice is linked (e.g., by pleiotropy, by genetic linkage) to boldness, the fitness consequences of boldness will affect the evolution of prey choice, and vice versa.

Thebehavioral syndromes paradigm incorporates individual differences and between-context correlations in behavior into an evolutionary framework (Sih et al. 2004; Bell 2007). A series of studies on the Western grass spider,Agelenopsis aperta, is an early example of the behavioral syndromes approach.The Western grass spider is a funnel web spider that occurs in both dry grassland and moist riparian habitats. Grassland dwellers experience lower prey availability, higher competition for webs, and lower predation from birds (Riechert & Hedrick 1990). The authors asked how the very different selection regimes in these two habitats affected spiders’ behavior.

Riechert and Hedrick’s (1990, 1993) work contributes to the personality literature because it measures multiple behavioral traits and quantifies the relationships between them. The traits that they examined -- boldness, latency to forage, success in agonistic contests – might be said to constitute the ‘shy-bold’ axis of personalitywidely studied in vertebrates (Gosling 2001). The authors, however, call these behaviors manifestations of ‘aggression’ and ‘fear’, which they view as separate, but correlated axes (Smith & Riechert 1984). Regardless of the terminology or the underlying mechanisms, these traits areevolutionarily important because they affectpredator avoidance, foraging, and other factors that determine fitness.

Riechert and Hedrick (1990) reasoned that natural selection should favor more fearful spiders in riparian habitats, and more aggressive spiders in grasslands. Becauseriparian spiders experience high predation risk and high food availability, spending a lot of time hiding (an expression of fearfulness) should provide high benefits in the form of reduced risk of predation at a relatively low cost – if they miss a meal because they are hiding, another meal will probably be available soon. In contrast, grassland spiders are under low predation risk, but they must maintain large territories and be vigilant for potential food because prey is scarce. Grassland spiders would benefit from low fearfulness and high aggressiveness if these traits help them to defend large territories and capture more prey. Because predation is relatively uncommon in the grassland population, the costs of being exposed on the web should be lower than in the riparian population. The investigators measured fearfulness by simulating an approaching avian predator and recording whether the resident spider retreated into its funnel and, if so, how long it took to re-emerge.Their predator stimulus was simple but appropriate to their subject’s umwelt; experimenters blew puffs of air onto the web sheet with a rubber bulb designed to clean camera lenses. As predicted, free-living spiders from the riparian habitat exhibited significantly longer latencies to re-emerge from the funnel than their grassland counterparts (Riechert & Hedrick 1990). The same pattern was found among second-generation laboratory-raised spiders, showingthat genetic are responsible for at least part of the difference in latency to emerge between the two populations.

Emergence time was not the only trait that differed between the populations. The researchers deposited standardized prey items into spiders’ webs and measured their latency to attack. They foundthat riparian spiders took longer than grassland spiders to attack prey that had been deposited in their webs (14.1 vs. 6.6 sec, on average; Hedrick & Riechert 1989). The hypothesis thatlatency to attack and latency to recover from disturbance are constrained to evolve together can be used to generate the prediction that the two traits will covary within a given population. Indeed, recovery from disturbance and latency to attack prey were related among individuals in the riparian population, suggesting such a constraint. Further, when spiders exhibiting short latencies to recover from disturbance were pitted against spiders with long latencies in agonistic contests, the short latency spiders tended to win (Riechert Hedrick 1993). Thus, behaviors associated with fighting, recovery from disturbance, and predation all covary in A. aperta. Similar results from lab-raised spiders indicate that some of this covariation (which represents a ‘behavioral syndrome’ or a ‘dimension of personality’) is attributable to genetic variation. Genetic causes of behavioral syndromes include pleitropy (i.e., multiple effects attributable to a given genetic variant) or linkage disequilibrium (i.e., when two or more genes tend to be inherited together; Riechert & Hedrick 1990;Sih et al. 2004).