Behavioural mediators of genetic life-history trade-offs: a test of the pace-of-life syndrome hypothesis in field crickets

This is the author accepted manuscript. The final version is available from the publisher via the DOI in this record.The pace-of-life syndrome (POLS) hypothesis predicts associations between life history and 'risky' behaviours. Individuals with 'fast' lifestyles should develop faster, reproduce earlier, exhibit more risk-prone behaviours, and die sooner than those with 'slow' lifestyles. While support for POLS has been equivocal to date, studies have relied on individual-level (phenotypic) patterns in which genetic trade-offs may be masked by environmental effects on phenotypes. We estimated genetic correlations between life history (development, lifespan, size) and risky behaviours (exploration, aggression) in a pedigreed population of Mediterranean field crickets (Gryllus bimaculatus). Path analyses showed that behaviours mediated some genetic relationships between life history traits, though not those involved in trade-offs. Thus, while specific predictions of POLS theory were not supported, genetic integration of behaviour and life history was present. This implies a major role for risky behaviours in life history evolution.F.S. and N.J.D. were supported by the Max Planck Society, F.S. by the International Max Planck Research School for Organismal Biology, A.J.W. by a BBSRC David Phillips Research Fellowship, and P.T.N. by a postdoctoral fellowship of the German Science Foundation (DFG)

Interacting with the enemy: indirect effects of personality on conspecific aggression in crickets

In animal contests, individuals respond plastically to the phenotypes of the opponents that they confront. These ‘opponent’ – or ‘indirect’ – effects are often repeatable, e.g., certain opponents consistently elicit more or less aggressiveness in others. ‘Personality’ (repeatable among-individual variance in behavior) has been proposed as an important source of indirect effects. Here, we repeatedly assayed aggressiveness of wild-caught adult male field crickets Gryllus campestris in staged dyadic fights, measuring aggressiveness of both contestants. Measurements of their personality in non-social contexts (activity and exploration behavior) enabled us to ask whether personality caused indirect effects on aggressiveness. Activity, exploration, and aggressiveness were positively associated into a behavioral syndrome eliciting aggressiveness in conspecifics, providing direct evidence for the role of personality in causing indirect effects. Our findings imply that a multivariate view of phenotypes that includes indirect effects greatly improves our ability to understand the ecology and evolution of behavior

Adaptive individual variation in phenological responses to perceived predation levels

The adaptive evolution of timing of breeding (a component of phenology) in response to environmental change requires individual variation in phenotypic plasticity for selection to act upon. A major question is what processes generate this variation. Here we apply multi-year manipulations of perceived predation levels (PPL) in an avian predator-prey system, identifying phenotypic plasticity in phenology as a key component of alternative behavioral strategies with equal fitness payoffs. We show that under low-PPL, faster (versus slower) exploring birds breed late (versus early);the pattern is reversed under high-PPL, with breeding synchrony decreasing in conjunction. Timing of breeding affects reproductive success, yet behavioral types have equal fitness. The existence of alternative behavioral strategies thus explains variation in phenology and plasticity in reproductive behavior, which has implications for evolution in response to anthropogenic change

Male song stability shows cross‐year repeatability but does not affect reproductive success in a wild passerine bird

Abstract Predictable behaviour (or ‘behavioural stability’) might be favoured in certain ecological contexts, for example when representing a quality signal. Costs associated with producing stable phenotypes imply selection should favour plasticity in stability when beneficial. Repeatable among‐individual differences in degree of stability are simultaneously expected if individuals differ in ability to pay these costs, or in how they resolve cost–benefit trade‐offs. Bird song represents a prime example, where stability may be costly yet beneficial when stable singing is a quality signal favoured by sexual selection. Assuming energetic costs, ecological variation (e.g. in food availability) should result in both within‐ and among‐individual variation in stability. If song stability represents a quality signal, we expect directional selection favouring stable singers. For a 3‐year period, we monitored 12 nest box plots of great tits Parus major during breeding. We recorded male songs during simulated territory intrusions, twice during their mate's laying stage and twice during incubation. Each preceding winter, we manipulated food availability. Assuming that stability is costly, we expected food‐supplemented males to sing more stable songs. We also expected males to sing more stable songs early in the breeding season (when paternity is not decided) and stable singers to have increased reproductive success. We found strong support for plasticity in stability for two key song characteristics: minimum frequency and phrase length. Males were plastic because they became more stable over the season, contrary to expectations. Food supplementation did not affect body condition but increased stability in minimum frequency. This treatment effect occurred only in 1 year, implying that food supplementation affected stability only in interaction with (unknown) year‐specific ecological factors. We found no support for directional, correlational or fluctuating selection on the stability in minimum frequency (i.e. the song trait whose stability exhibited cross‐year repeatability): stable singers did not have higher reproductive success. Our findings imply that stability in minimum frequency is not a fitness quality indicator unless males enjoy fitness benefits via pathways not studied here. Future studies should thus address the mechanisms shaping and maintaining individual repeatability of song stability in the wild. </jats:p

Exploration Behaviour Is Not Associated with Chick Provisioning in Great Tits

In biparental systems, members of the same pair can vary substantially in the amount of parental care they provide to offspring. The extent of this asymmetry should depend on the relative costs and benefits of care. Individual variation in personality is likely to influence this trade-off, and hence is a promising candidate to explain differences in care. In addition, plasticity in parental care may also be associated with personality differences. Using exploration behaviour (EB) as a measure of personality, we investigated these possibilities using both natural and experimental data from a wild population of great tits (Parus major). Contrary to predictions, we found no association between EB and natural variation in provisioning behaviour. Nor was EB linked to responsiveness to experimentally increased brood demand. These results are initially surprising given substantial data from other studies suggesting personality should influence investment in parental care. However, they are consistent with a recent study showing selection on EB is weak and highly context-specific in the focal population. This emphasises the difficulty faced by personality studies attempting to make predictions based on previous work, given that personalities often vary among populations of the same species

Extra-pair parentage and personality in a cooperatively breeding bird

Why so much variation in extra-pair parentage occurs within and among populations remains unclear. Often the fitness costs and benefits of extra-pair parentage are hypothesised to explain its occurrence; therefore, linking extra-pair parentage with traits such as personality (behavioural traits that can be heritable and affect reproductive behaviour) may help our understanding. Here, we investigate whether reproductive outcomes and success are associated with exploratory behaviour in a natural population of cooperatively breeding Seychelles warblers (Acrocephalus sechellensis) on Cousin Island. Exploratory behaviour correlates positively with traits such as risk-taking behaviour and activity in other wild bird species and might promote extra-pair mating by increasing the rate at which potential extra-pair partners are encountered. We therefore predicted that fast-exploring individuals would have more extra-pair offspring. There is also a potential trade-off between pursuing extra-pair parentage and mate guarding in males. We therefore also predicted that fast-exploring males would be more likely to pursue extra-pair parentage and that this would increase the propensity of their mate to gain extra-pair parentage. We found that neither the total number of offspring nor the number of extra-pair offspring were associated with a male’s or female’s exploratory behaviour. However, there was a small but significant propensity for females to have extra-pair fertilisations in pairs that were behaviourally disassortative. Overall, we conclude that, due to the small effect size, the association between exploratory behaviour and extra-pair paternity is unlikely to be biologically relevant. Significance statement: True genetic monogamy is rare, even in socially monogamous systems, and multiple factors, such as behaviour, social structure, morphology and physiology, determined by the biological system can cause variation in extra-pair parentage (EPP). Therefore, investigating the inherent differences in these factors among individuals could be informative. We investigated whether reproductive outcomes/success are associated with differences in the propensity to explore novel environments/objects in a promiscuous, island-dwelling cooperatively breeding bird, the Seychelles warbler. Our results showed that exploratory behaviour was not associated with the number of offspring produced by an individual, and thus the long-term fitness consequences of different exploratory tendencies did not differ. We also found that the propensity to engage in EPP in females was higher in dissimilar behavioural pairs, but due to the small effect size, we hesitate to conclude that there are personality-dependent mating outcomes in the population

The female perspective of personality in a wild songbird: repeatable aggressiveness relates to exploration behaviour

ABSTRACT: Males often express traits that improve competitive ability, such as aggressiveness. Females also express such traits but our understanding about why is limited. Intraspecific aggression between females might be used to gain access to reproductive resources but simultaneously incurs costs in terms of energy and time available for reproductive activities, resulting in a trade-off. Although consistent individual differences in female behaviour (i.e. personality) like aggressiveness are likely to influence these reproductive trade-offs, little is known about the consistency of aggressiveness in females. To quantify aggression we presented a female decoy to free-living female great tits (Parus major) during the egg-laying period, and assessed whether they were consistent in their response towards this decoy. Moreover, we assessed whether female aggression related to consistent individual differences in exploration behaviour in a novel environment. We found that females consistently differed in aggressiveness, although first-year females were on average more aggressive than older females. Moreover, conform life history theory predictions, ‘fast’ exploring females were more aggressive towards the decoy than ‘slow’ exploring females. Given that personality traits are often heritable, and correlations between behaviours can constrain short term adaptive evolution, our findings highlight the importance of studying female aggression within a multivariate behavioural framework

Personality May Confound Common Measures of Mate-Choice

The measurement of female mating preferences is central to the study of the evolution of male ornaments. Although several different methods have been developed to assess sexual preference in some standardized way, the most commonly used procedure consists of recording female spatial association with different males presented simultaneously. Sexual preference is then inferred from time spent in front of each male. However, the extent to which the measurement of female mate-choice is related to exploration tendencies has not been addressed so far. In the present study we assessed the influence of variation in exploration tendencies, a trait closely associated to global personality, on the measurement of female mating preference in the zebra finch (Taeniopygia guttata) using the widely used four-chamber choice-apparatus. The number of movements performed within both exploration and mate-choice apparatus was consistent within and across the two contexts. In addition, personality explained variation in selectivity, preference strength and consistency. High-exploratory females showed lower selectivity, lower preference scores and displayed more consistent preference scores. Our results suggest that variation in personality may affect the measurement of female mating preference and may contribute to explain existing inconsistencies across studies