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Croft, D. P.

Publications and source records attributed to Croft, D. P..

13 recordsLinked to original sources

A landscape of intergroup conflict shapes den site choice in banded mongooses

BackgroundFor many social animals, intergroup conflict has major impacts on fitness and should therefore influence how groups navigate their environment. Yet most studies of group movement focus on the behaviour of single groups, usually foraging groups studied in isolation of all others. In many systems rival groups present both threats and opportunities, contributing to a landscape of intergroup conflict. This landscape could have a profound impact on group movement. MethodsHere we test how the potential for intergroup conflict influences movement decisions of wild cooperatively breeding banded mongooses, using 14 years of behavioural and GPS data. In this species, encounters between groups can present both risks (e.g. injury/mortality) and opportunities (e.g., extragroup mating). We expected that, to minimise risks and maximise rewards, the motivation to engage in conflict would depend on the groups state. Such that vulnerable groups (those that were babysitting young offspring) would select den sites closer to the core of their territory than groups without young offspring. ResultsWe found support for this pattern; non-babysitting groups were unusually risk prone choosing den locations in areas of frequent use by outgroups. During times of heightened recent conflict even choosing to den closer to the core of their rivals territory than their own. ConclusionsThese results suggest that groups of banded mongooses choose den sites that reflect not only the risks but also the potential rewards of defensive or competitive claims on space. Rival groups thus form an integral part of the social landscape shaping patterns of collective movement.

animal behavior and cognition↗

Predicting kinship dynamics during pre- and post reproductive life stages

Individuals relatedness to their groups often changes with age, potentially favouring age-linked trends in social behaviours, and these kinship dynamics have been invoked to explain the evolution of life history traits such as early reproductive cessation and post-reproductive helping. While models showed that simple demographic parameters (e.g., the rates of male and female philopatry vs dispersal, and of local vs non-local mating) suffice to predict the patterns of kinship dynamics breeders experience, they make the unrealistic assumptions that survival and fecundity are age-independent, thus fail to capture the full complexity of kinship dynamics. In particular, they cannot consistently predict how individuals relatedness to their groups should change during their pre- and post-reproductive phases. Here, we extend existing models of kinship dynamics to allow any age-linked changes in mortality and fecundity of both sexes. We describe the new model, and demonstrate its improved predictive power, by comparing the observed kinship dynamics of the killer whales to the predictions of the previously available models (assuming constant mortality and fecundity) and of our new model (considering any observed age-specific survival and fecundity). We show the new model better predicts the data, successfully capturing the observed three-stage female kinship dynamics: an individuals relatedness to her group decreases initially while juvenile, increases across reproductive lifespan, and decreases again during post-reproductive life. These predictions demonstrate the power of our model in generating new insights into the theory of social life history evolution (e.g., explaining why post-reproductive lifespan evolved yet are constrained).

evolutionary biology↗

Menopause has not evolved as a general trait in mammals: A response to "Do mammals have menopause?"

Reproductive senescence is widespread across mammals, but only a small number of species have physiological reproductive cessation and an extended post-reproductive lifespan. A recent commentary in Cell by Winkler & Goncalves (2023) suggests that menopause is actually a widespread trait of mammals, which would change our understanding of senescence and have implications for the study of menopause in humans. Here, we identify three main issues with the methodology of this commentary: the use of captive populations, the use of maximal lifespan, and misinterpretations of the data sources. We show that this methodology does not support the conclusions at the species-level, and conclude that, in line with the predictions of classic life-history theory, menopause is indeed a rare trait.

evolutionary biology↗

Group size modulates kinship dynamics and selection on social traits

An individuals relatedness to its group may change with age due to demographic processes, and such kinship dynamics can shape age-linked social behaviors. Existing models, however, have focused almost exclusively on dispersal and mating, leaving the consequences of group size local variation unexplored. Here, we extend these models to incorporate such variation within a single, genetically connected meta-population. We then contrast predicted kinship dynamics and age-linked selection for helping/harming in coexisting smaller and larger groups in three typical social mammal systems characterized by distinct patterns of dispersal and mating, followed by exploring how group size local variation impacts female and male kinship dynamics across broader demographic contexts to clarify the population-genetic mechanisms. We show that, within the adult reproductive lifespans of these social systems, an individuals age-specific relatedness to others is higher, and changes faster (especially when younger), in smaller groups; consequently, smaller groups favor more extreme helping/harming (especially when younger) -- in social system with bi-sexual philopatry with non-local mating (e.g., whales) that favors female shifts from harming to helping with age (which explains the evolution of menopause and post-reproductive helping), such shifts are earlier in smaller groups. Further explorations suggest that, in a genetically connected population with group size local variation, group size effects on local relatedness are shaped by the relative strengths of ancestry dilution versus lineage coalescence, and kinship dynamics in a group reflect not only its local demographic conditions, but also those in coexisting groups of different size. Collectively, our study generates new insights into how female and male kinship dynamics emerge and vary under within-population group-size heterogeneity, and how such locally dynamic, varying kinship environments may help to explain variation in age-linked trends in social traits, such as the timing of menopause in social mammals.

evolutionary biology↗

Bayesian inference of toothed whale lifespans

Accurate measures of lifespan and age-specific mortality are important both for understanding life history evolution and informing conservation and population management strategies. The most accurate data to estimate lifespan are from longitudinal studies, but for many species - especially those such as toothed whales that are wide-ranging and inhabit difficult-to-access environments - these longitudinal data are not available. However, other forms of age-structured data - such as from mass-strandings - are available for many toothed species, and using these data to infer patterns of age-specific mortality and lifespan remains an important outstanding challenge. Here we develop and test a Bayesian mortality model to derive parameters of a mortality function from age-structured data while accounting for potential error introduced by mistakes in age estimation, sampling biases and population growth. We then searched the literature to assemble a database of 269 published age-structured toothed whale datasets. We applied our mortality model to derive lifespan estimates for 32 species of female and 33 species of male toothed whale. We also use our model to characterise sex differences in lifespan in toothed whales. Our mortality model allows us to curate the most complete and accurate collection of toothed whale lifespans to date.

evolutionary biology↗

The Evolution of Democratic Peace

A major goal in evolutionary biology is to elucidate common principles that drive human and other animal societies to adopt either a warlike or peaceful nature. One proposed explanation for the variation in aggression between human societies is the democratic peace hypothesis. According to this theory, autocracies are more warlike than democracies because autocratic leaders can pursue fights for private gain. However, autocratic and democratic decision-making processes are not unique to humans and are widely observed across a diverse range of non-human animal societies. We use evolutionary game theory to evaluate whether the logic of democratic peace may apply across taxa; specifically adapting the classic Hawk-Dove model to consider conflict decisions made by groups rather than individuals. We find support for the democratic peace hypothesis without mechanisms involving complex human institutions and discuss how these findings might be relevant to non-human animal societies. We suggest that the degree to which collective decisions are shared may explain variation in the intensity of intergroup conflict in nature.

evolutionary biology↗

Partial sex linkage and linkage disequilibrium on the guppy sex chromosome

The guppy Y chromosome has been considered a model system for the evolution of suppressed recombination between sex chromosomes, and it has been proposed that complete sex-linkage has evolved across about 3 Mb surrounding this fishs sex-determining locus, followed by recombination suppression across a further 7 Mb of the 23 Mb XY pair, forming younger "evolutionary strata". Sequences of the guppy genome show that Y is very similar to the X chromosome, making it important to understand which parts of the Y are completely non-recombining, and whether there is indeed a large completely non-recombining region. Here, we describe new evidence that supports a different interpretation of the data that suggested the presence of such a region. We analysed PoolSeq data in samples from multiple natural populations from Trinidad. This yields evidence for linkage disequilibrium (LD) between sequence variants and the sex-determining locus. Downstream populations have higher diversity than upstream ones (which display the expected signs of bottlenecks). The associations we observe conform to predictions for a genome region with infrequent recombination that carries one or more sexually antagonistic polymorphisms. They also suggest the region in which the sex-determining locus must be located. However, no consistently male-specific variants were found, supporting the suggestion that any completely sex-linked region may be very small.

evolutionary biology↗

Brain monoaminergic activity during predator inspection in the Trinidadian guppy (Poecilia reticulata)

To understand the processes underpinning social decision-making, we need to determine how internal states respond to information gathered from the social environment. Brain monoamine neurotransmitters are key in the appraisal of the social environment and can reflect the internal state underlying behavioural responses to social stimuli. Here we determined the effects of conspecific partner cooperativeness during predator inspection on brain monoamine metabolic activity in Trinidadian guppies (Poecilia reticulata). We quantified the concentration of dopamine, serotonin and their metabolites across brain sections sampled immediately after ostensibly experiencing cooperation or defection from social partners whilst inspecting a predator model. Our results indicate dopaminergic and serotonergic activity differs with the cooperativeness experienced; these different neurotransmission profiles are likely to affect the expression and regulation of downstream behaviours that ultimately contribute to the patterning of cooperative interactions among individuals in the population. List of abbreviations used

animal behavior and cognition↗

Gene Expression Risk Scores for COVID-19 Illness Severity

BackgroundThe correlates of COVID-19 illness severity following infection with SARS-Coronavirus 2 (SARS-CoV-2) are incompletely understood. MethodsWe assessed peripheral blood gene expression in 53 adults with confirmed SARS-CoV-2-infection clinically adjudicated as having mild, moderate or severe disease. Supervised principal components analysis was used to build a weighted gene expression risk score (WGERS) to discriminate between severe and non-severe COVID. ResultsGene expression patterns in participants with mild and moderate illness were similar, but significantly different from severe illness. When comparing severe versus non-severe illness, we identified >4000 genes differentially expressed (FDR<0.05). Biological pathways increased in severe COVID-19 were associated with platelet activation and coagulation, and those significantly decreased with T cell signaling and differentiation. A WGERS based on 18 genes distinguished severe illness in our training cohort (cross-validated ROC-AUC=0.98), and need for intensive care in an independent cohort (ROC-AUC=0.85). Dichotomizing the WGERS yielded 100% sensitivity and 85% specificity for classifying severe illness in our training cohort, and 84% sensitivity and 74% specificity for defining the need for intensive care in the validation cohort. ConclusionThese data suggest that gene expression classifiers may provide clinical utility as predictors of COVID-19 illness severity.

genomics↗

Social partner cooperativeness influences brain oxytocin transcription in Trinidadian guppies (Poecilia reticulata)

For non-kin cooperation to be maintained, individuals need to respond adaptively to the cooperative behaviour of their social partners. Currently, however, little is known about the biological responses of individuals to experiencing cooperation. Here, we quantify the neuroregulatory response of Trinidadian guppies (Poecilia reticulata) experiencing cooperation or defection by examining the transcriptional response of the oxytocin gene (oxt; also known as isotocin), which has been implicated in cooperative decision-making. We exposed wild-caught females to social environments where partners either cooperated or defected during predator inspection, or to a control (non-predator inspection) context, and quantified the relative transcription of the oxt gene. We tested an experimental group, originating from a site where individuals are under high predation threat and have previous experience of large aquatic predators (HP), and a control group, where individuals are under low predation threat and naive to large aquatic predators (LP). In HP, but not LP, fish brain mid-section oxt relative transcription varied depending on social partner behaviour. HP fish experiencing cooperation during predator inspection had lower oxt transcription than those experiencing defection. This effect was not present in the control population or in the control context, where the behaviour of social partners did not affect oxt transcription. Our findings provide insight into the neuromodulation underpinning behavioural responses to social experiences, and ultimately to the proximate mechanisms underlying social decision-making.

animal behavior and cognition↗

Sensory-based quantification of male colour patterns in Trinidadian guppies reveals nonparallel phenotypic evolution across an ecological transition in multivariate trait space

Parallel evolution, in which independent populations evolve along similar phenotypic trajectories, offers insights into the repeatability of adaptive evolution. Here, we revisit a classic example of parallelism, that of repeated evolution of brighter males in the Trinidadian guppy. In guppies, colonisation of low predation habitats is associated with emergence of more colourful phenotypes since predator-induced viability selection for crypsis weakens while sexual selection by female preference for conspicuity remains strong. Our study differs from previous investigations in three respects. First, we adopt a multivariate phenotyping approach to characterise parallelism in multi-trait space. Second, we use ecologically-relevant colour traits defined by the visual systems of the two selective agents (i.e. guppy, predatory cichlid). Third, we estimate population genetic structure to test for adaptive (parallel) evolution against a model of neutral phenotypyc divergence. We find strong phenotypic differentiation that is inconsistent with a neutral model, but only limited support for the predicted pattern of greater conspicuity at low predation. Effects of predation regime on each trait were in the expected direction, but weak, largely non-significant, and explained little among-population variation. In multi-trait space, phenotypic trajectories of lineages colonising low from high predation regimes were not parallel. Our results are consistent with reduced predation risk facilitating adaptive differentiation by female choice, but suggest that this proceeds in (effectively) independent directions of multi-trait space across lineages. Pool-sequencing data also revealed SNPs showing greater differentiation than expected under neutrality and/or associations with known colour genes in other species, presenting opportunities for future genetic study.

evolutionary biology↗

Calculating effect sizes in animal social network analysis

O_LIBecause of the nature of social interaction or association data, when testing hypotheses using social network data it is common for network studies to rely on permutations to control for confounding variables, and to not also control for them in the fitted statistical model. This can be a problem because it does not adjust for any bias in effect sizes generated by these confounding effects, and thus the effect sizes are not informative in the presence of counfouding variables. C_LIO_LIWe implemented two network simulation examples and analysed an empirical data set to demonstrate how relying solely on permutations to control for confounding variables can result in highly biased effect size estimates of animal social preferences that are uninformative when quantifying differences in behaviour. C_LIO_LIUsing these simulations, we show that this can sometimes even lead to effect sizes that have the wrong sign and are thus the effect size is not biologically interpretable. We demonstrate how this problem can be addressed by controlling for confounding variables in the statistical dyadic or nodal model. C_LIO_LIWe recommend this approach should be adopted as standard practice in the statistical analysis of animal social network data. C_LI

animal behavior and cognition↗

Common datastream permutations of animal social network data are not appropriate for hypothesis testing using regression models

O_LISocial network methods have become a key tool for describing, modelling, and testing hypotheses about the social structures of animals. However, due to the non-independence of network data and the presence of confounds, specialized statistical techniques are often needed to test hypotheses in these networks. Datastream permutations, originally developed to test the null hypothesis of random social structure, have become a popular tool for testing a wide array of null hypotheses. In particular, they have been used to test whether exogenous factors are related to network structure by interfacing these permutations with regression models. C_LIO_LIHere, we show that these datastream permutations typically do not represent the null hypothesis of interest to researchers interfacing animal social network analysis with regression modelling, and use simulations to demonstrate the potential pitfalls of using this methodology. C_LIO_LIOur simulations show that utilizing common datastream permutations to test the coefficients of regression models can lead to extremely high type I (false-positive) error rates (> 30%) in the presence of non-random social structure. The magnitude of this problem is primarily dependent on the degree of non-randomness within the social structure and the intensity of sampling C_LIO_LIWe strongly recommend against utilizing datastream permutations to test regression models in animal social networks. We suggest that a potential solution may be found in regarding the problems of non-independence of network data and unreliability of observations as separate problems with distinct solutions. C_LI

animal behavior and cognition↗