A multivariate view of cognitive differences reveals domain-general correlation structure in the Trinidadian Guppy (Poecilia reticulata)

Cognitive variation is common among-individuals within populations, and this variation can be consistent across time and context. From an evolutionary perspective, among-individual variation is important and required for natural selection. Selection has been hypothesised to favour high cognitive performance, however directional selection would be expected to erode variation over time. Additionally, while variation is a prerequisite for natural selection, it is also true that selection does not act on traits in isolation. Thus, the extent to which performance covaries among specific cognitive domains, and other aspects of phenotype (e.g. personality traits) is expected to be an important factor in shaping evolutionary dynamics. Fitness trade-offs could shape patterns of variation in performance across different cognitive domains, however positive correlations between cognitive domains and personality traits are also known to occur. Here we aimed to test this idea using a multivariate approach to characterise and test hypothesised relationships of cognitive performance across multiple domains and personality, in the Trinidadian guppy (Poecilia reticulata). We estimate the among-individual correlation matrix (ID) in performance across three cognitive domains; association learning in a colour discrimination task; motor cognition in a novel motor task and cognitive flexibility in a reversal learning task, and the personality trait boldness, measured as time to emerge. We found no support for trade-offs occurring, but the presence of strong positive domain-general correlations in ID, where 57% of the variation is explained by the leading eigen vector. While highlighting caveats of how non-cognitive factors and assay composition may affect the structure of the ID-matrix, we suggest that our findings are consistent with a domain-general axis of cognitive variation in this population, adding to the growing body of support for domain-general variation among-individuals in animal cognitive ability.

Social hosts evade predation but have deadlier parasites

Parasites exploit hosts to replicate and transmit, but overexploitation kills both host and parasite1: parasite virulence evolves to balance these costs and benefits. Predators can in theory shift this balance by consuming hosts2–4. However, the non-consumptive effects of predators may be as important as their consumptive effects5. Here, we use an eco-coevolutionary model to show that predators select for host grouping, a common anti-predator, defensive social behaviour6. Host grouping simultaneously increases parasite transmission, thus within-host parasite competition, and therefore favours more exploitative, virulent, parasites7. When parametrized with data from the guppy-Gyrodactylus spp. system, including our experimentally demonstrated trade-off between virulence and transmission, our model accurately predicted the common garden-assayed virulence of 18 parasite lines collected from four Trinidadian guppy populations under different predation regimes. The quantitative match between theory and data lends credence to the model’s insight that the non-consumptive, social behaviour pathway is entirely responsible for the observed increase in virulence with predation pressure. Our results indicate that parasites play an important, underappreciated role in guppy evolutionary ecology. Moreover, group living is a common anti-predator defence6 and our general model accommodates host-parasite interactions across taxa: its insight into the interactions among predation, sociality, and virulence evolution may apply broadly. Our results additionally suggest that social distancing, by reducing host-host contact, can select for less virulent parasites and pathogens.

Substantial intraspecific variation in energy budgets: biology or artefact?

Dynamic energy budget (DEB) models provide a mechanistic description of life-histories in terms of fluxes of energy through biological processes. In these models, life-histories are a function of environmental conditions and of fundamental traits of the organism relating to the acquisition, allocation, and use of energy. These traits are described by the parameters of the DEB model, which have been estimated for over 2500 species. Recent work has aimed to compare species on the basis of differences in DEB parameters. We show that caution is required in such analyses, because (i) parameter estimates vary considerably as an artefact of the types of data used to fit the models, and (ii) there is substantial intraspecific variation in parameter values, reflecting biological differences among populations. We show that similar patterns of growth and reproduction can be reproduced with very different parameter sets. Our results imply that direct comparison of DEB parameters across populations or species may be invalid. However, valid comparisons are possible if differences in the types of data used to fit the models are taken into account. We estimated DEB parameters for 16 populations of Trinidadian guppy, identifying differences in resource allocation and metabolic rate consistent with evolved life-history differences among these populations. Variation in parameter values was substantial: if intraspecific variation in DEB parameters is greater than currently measured levels of interspecific variation, the detection of broad-scale patterns in energy budgets across species will be challenging.

Kin recognition in guppies uses self-referencing on olfactory cues

Kin recognition plays an important role in social evolution, but the proximate mechanisms by which individuals recognize kin remain poorly understood. In many species, individuals form a “kin template” that they compare against conspecifics’ phenotypes to assess phenotypic similarity–and by association, relatedness. Individuals may form a kin template through self-inspection (i.e. self-referencing) and/or by observing their rearing associates (i.e. family-referencing). However, despite much interest, few empirical studies have successfully disentangled self- and family-referencing. Here, we use a novel set of breeding crosses in the Trinidadian guppy (Poecilia reticulata) to definitively disentangle referencing systems by manipulating exposure to kin from conception onwards. We show that guppies discriminate among their full- and maternal half-siblings, which can only be explained by self-referencing. Additional behavioral experiments revealed no evidence that guppies incorporate the phenotypes of their broodmates or mother into the kin template. Finally, by manipulating the format of our behavioral tests, we show that olfactory communication is both necessary and sufficient for kin discrimination. These results demonstrate that individuals recognize kin by comparing the olfactory phenotypes of conspecifics against their own. This study resolves key questions about the proximate mechanisms underpinning kin recognition, with implications for the ontogeny and evolution of social behavior.

Divergence in social traits in Trinidadian guppies selectively bred for high and low leadership in a cooperative context

In many animal species, individuals with certain morphological, physiological, or behavioural traits may have a disproportionately large role in determining group behaviour. While most empirical studies of leadership have focused on behaviour of individuals exploring new environments or foraging, little is known about leading behaviour in other ecological contexts. Here, we use a selective breeding design in the Trinidadian guppy (Poecilia reticulata) to quantify the heritability of leadership in a cooperative context, and determine the behavioural traits associated with it. Firstly we found that phenotypic selection for high and low leadership (HL and LL, respectively) over three filial generations resulted in pronounced differences in leadership tendency with a moderate degree of heritability. In our assay of other social traits, LL males were more aggressive and sampled their social environment less than HL males, but HL and LL females did not differ in either aggressiveness or sociability. Traits such as boldness and exploratory tendency did not diverge between the two lines. Leading behaviour was thus associated with social traits in males, but not females; suggesting that there may be sex-specific mechanisms driving the emergence of leadership in this context. We discuss our findings in the context of the evolution of cooperation.

Habituation underpins preference for mates with novel phenotypes in the guppy

Populations harbour enormous genetic diversity in ecologically important traits. Understanding the processes that maintain this variation is a long-standing challenge in evolutionary biology. Recent evidence indicates that a mating preference for novel sexual signals can be a powerful force maintaining genetic diversity. However, the proximate underpinnings of this preference, and its generality, remain unclear. Here, we test the hypothesis that preference for novel sexual signals is underpinned by habituation, a nearly ubiquitous form of learning whereby individuals become less responsive to repetitive stimuli. We use the Trinidadian guppy ( Poecilia reticulata ), in which male colour patterns are diverse yet heritable. We show that repeated exposure to males with a given colour pattern reduces female interest in males with that pattern, and that interest recovers following brief isolation. These results fulfil two core criteria of habituation: responsiveness decline and spontaneous recovery. To distinguish habituation from sensory adaptation and fatigue, we also demonstrate stimulus specificity and dishabituation. These results provide the first evidence that habituation causes a preference for novel sexual signals, addressing the mechanistic underpinnings of this mating preference. Given the pervasiveness of habituation among taxa and sensory contexts, our findings suggest that preference for novelty may play an underappreciated role in mate choice and the maintenance of genetic variation.