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Differences in resource acquisition, not allocation, mediate the relationship between behaviour and fitness: a systematic review and meta‐analysis

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Within populations, individuals often show repeatable variation in behaviour, called ‘animal personality’. In the last few decades, numerous empirical studies have attempted to elucidate the mechanisms maintaining this variation, such… Click to show full abstract

Within populations, individuals often show repeatable variation in behaviour, called ‘animal personality’. In the last few decades, numerous empirical studies have attempted to elucidate the mechanisms maintaining this variation, such as life‐history trade‐offs. Theory predicts that among‐individual variation in behavioural traits could be maintained if traits that are positively associated with reproduction are simultaneously associated with decreased survival, such that different levels of behavioural expression lead to the same net fitness outcome. However, variation in resource acquisition may also be important in mediating the relationship between individual behaviour and fitness components (survival and reproduction). For example, if certain phenotypes (e.g. dominance or aggressiveness) are associated with higher resource acquisition, those individuals may have both higher reproduction and higher survival, relative to others in the population. When individuals differ in their ability to acquire resources, trade‐offs are only expected to be observed at the within‐individual level (i.e. for a given amount of resource, if an individual increases its allocation to reproduction, it comes at the cost of allocation to survival, and vice versa), while among individuals traits that are associated with increased survival may also be associated with increased reproduction. We performed a systematic review and meta‐analysis, asking: (i) do among‐individual differences in behaviour reflect among‐individual differences in resource acquisition and/or allocation, and (ii) is the relationship between behaviour and fitness affected by the type of behaviour and the testing environment? Our meta‐analysis consisted of 759 estimates from 193 studies. Our meta‐analysis revealed a positive correlation between pairs of estimates using both survival and reproduction as fitness proxies. That is, for a given study, behaviours that were associated with increased reproduction were also associated with increased survival, suggesting that variation in behaviour at the among‐individual level largely reflects differences among individuals in resource acquisition. Furthermore, we found the same positive correlation between pairs of estimates using both survival and reproduction as fitness proxies at the phenotypic level. This is significant because we also demonstrated that these phenotypic correlations primarily reflect within‐individual correlations. Thus, even when accounting for among‐individual differences in resource acquisition, we did not find evidence of trade‐offs at the within‐individual level. Overall, the relationship between behaviour and fitness proxies was not statistically different from zero at the among‐individual, phenotypic, and within‐individual levels; this relationship was not affected by behavioural category nor by the testing condition. Our meta‐analysis highlights that variation in resource acquisition may be more important in driving the relationship between behaviour and fitness than previously thought, including at the within‐individual level. We suggest that this may come about via heterogeneity in resource availability or age‐related effects, with higher resource availability and/or age leading to state‐dependent shifts in behaviour that simultaneously increase both survival and reproduction. We emphasize that future studies examining the mechanisms maintaining behavioural variation in populations should test the link between behavioural expression and resource acquisition – both within and among individuals. Such work will allow the field of animal personality to develop specific predictions regarding the mediating effect of resource acquisition on the fitness consequences of individual behaviour.

Keywords: resource acquisition; behaviour; reproduction; fitness

Journal Title: Biological Reviews
Year Published: 2021

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