Computer vision for plant pathology: A review with examples from cocoa agriculture.

Plant pathogens can decimate crops and render the local cultivation of a species unprofitable. In extreme cases this has caused famine and economic collapse. Timing is vital in treating crop diseases, and the use of computer vision for precise disease detection and timing of pesticide application is gaining popularity. Computer vision can reduce labour costs, prevent misdiagnosis of disease, and prevent misapplication of pesticides. Pesticide misapplication is both financially costly and can exacerbate pesticide resistance and pollution. Here, we review the application and development of computer vision and machine learning methods for the detection of plant disease. This review goes beyond the scope of previous works to discuss important technical concepts and considerations when applying computer vision to plant pathology. We present new case studies on adapting standard computer vision methods and review techniques for acquiring training data, the use of diagnostic tools from biology, and the inspection of informative features. In addition to an in-depth discussion of convolutional neural networks (CNNs) and transformers, we also highlight the strengths of methods such as support vector machines and evolved neural networks. We discuss the benefits of carefully curating training data and consider situations where less computationally expensive techniques are advantageous. This includes a comparison of popular model architectures and a guide to their implementation.

The evolution of menopause in toothed whales.

Understanding how and why menopause has evolved is a long-standing challenge across disciplines. Females can typically maximize their reproductive success by reproducing for the whole of their adult life. In humans, however, women cease reproduction several decades before the end of their natural lifespan1,2. Although progress has been made in understanding the adaptive value of menopause in humans3,4, the generality of these findings remains unclear. Toothed whales are the only mammal taxon in which menopause has evolved several times5, providing a unique opportunity to test the theories of how and why menopause evolves in a comparative context. Here, we assemble and analyse a comparative database to test competing evolutionary hypotheses. We find that menopause evolved in toothed whales by females extending their lifespan without increasing their reproductive lifespan, as predicted by the 'live-long' hypotheses. We further show that menopause results in females increasing their opportunity for intergenerational help by increasing their lifespan overlap with their grandoffspring and offspring without increasing their reproductive overlap with their daughters. Our results provide an informative comparison for the evolution of human life history and demonstrate that the same pathway that led to menopause in humans can also explain the evolution of menopause in toothed whales.

Postreproductive female killer whales reduce socially inflicted injuries in their male offspring.

Understanding the evolution of menopause presents a long-standing scientific challenge1,2,3-why should females cease ovulation prior to the end of their natural lifespan? In human societies, intergenerational resource transfers, for example, food sharing and caregiving, are thought to have played a key role in the evolution of menopause, providing a pathway by which postreproductive females can boost the fitness of their kin.4,5,6 To date however, other late-life contributions that postreproductive females may provide their kin have not been well studied. Here, we test the hypothesis that postreproductive female resident killer whales (Orcinus orca) provide social support to their offspring by reducing the socially inflicted injuries they experience. We found that socially inflicted injuries, as quantified by tooth rake marks, are lower for male offspring in the presence of their postreproductive mother. In contrast, we find no evidence that postreproductive mothers reduce rake marking in their daughters. Similarly, we find no evidence that either reproductive mothers or grandmothers (reproductive or postreproductive) reduce socially inflicted injuries in their offspring and grandoffspring, respectively. Moreover, we find that postreproductive females have no effect on reducing the rake marks for whales in their social unit who are not their offspring. Taken together, our results highlight that directing late-life support may be a key pathway by which postreproductive females transfer social benefits to their male offspring.

Temporal dynamics of mother-offspring relationships in Bigg's killer whales: opportunities for kin-directed help by post-reproductive females.

Age-related changes in the patterns of local relatedness (kinship dynamics) can be a significant selective force shaping the evolution of life history and social behaviour. In humans and some species of toothed whales, average female relatedness increases with age, which can select for a prolonged post-reproductive lifespan in older females due to both costs of reproductive conflict and benefits of late-life helping of kin. Killer whales (Orcinus orca) provide a valuable system for exploring social dynamics related to such costs and benefits in a mammal with an extended post-reproductive female lifespan. We use more than 40 years of demographic and association data on the mammal-eating Bigg's killer whale to quantify how mother-offspring social relationships change with offspring age and identify opportunities for late-life helping and the potential for an intergenerational reproductive conflict. Our results suggest a high degree of male philopatry and female-biased budding dispersal in Bigg's killer whales, with some variability in the dispersal rate for both sexes. These patterns of dispersal provide opportunities for late-life helping particularly between mothers and their adult sons, while partly mitigating the costs of mother-daughter reproductive conflict. Our results provide an important step towards understanding why and how menopause has evolved in Bigg's killer whales.

Costly lifetime maternal investment in killer whales.

Parents often sacrifice their own future reproductive success to boost the survival of their offspring, a phenomenon referred to as parental investment. In several social mammals, mothers continue to improve the survival of their offspring well into adulthood;1,2,3,4,5 however, whether this extended care comes at a reproductive costs to mothers, and therefore represents maternal investment, is not well understood. We tested whether lifetime maternal care is a form of parental investment in fish-eating "resident" killer whales. Adult killer whales, particularly males, are known to receive survival benefits from their mothers;3 however, whether this comes at a cost to mothers' reproductive success is not known. Using multiple decades of complete census data from the "southern resident" population, we found a strong negative correlation between females' number of surviving weaned sons and their annual probability of producing a viable calf. This negative effect did not attenuate as sons grew older, and the cost of sons could not be explained by long-term costs of lactation or group composition effects, supporting the hypothesis that caring for adult sons is reproductively costly. This is the first direct evidence of lifetime maternal investment in an iteroparous animal, revealing a previously unknown life history strategy.

BISoN: A Bayesian Framework for Inference of Social Networks.

Animal social networks are often constructed from point estimates of edge weights. In many contexts, edge weights are inferred from observational data, and the uncertainty around estimates can be affected by various factors. Though this has been acknowledged in previous work, methods that explicitly quantify uncertainty in edge weights have not yet been widely adopted, and remain undeveloped for many common types of data. Furthermore, existing methods are unable to cope with some of the complexities often found in observational data, and do not propagate uncertainty in edge weights to subsequent statistical analyses.We introduce a unified Bayesian framework for modelling social networks based on observational data. This framework, which we call BISoN, can accommodate many common types of observational social data, can capture confounds and model effects at the level of observations, and is fully compatible with popular methods used in social network analysis.We show how the framework can be applied to common types of data and how various types of downstream statistical analyses can be performed, including non-random association tests and regressions on network properties.Our framework opens up the opportunity to test new types of hypotheses, make full use of observational datasets, and increase the reliability of scientific inferences. We have made both an R package and example R scripts available to enable adoption of the framework.

Common permutation methods in animal social network analysis do not control for non-independence.

The non-independence of social network data is a cause for concern among behavioural ecologists conducting social network analysis. This has led to the adoption of several permutation-based methods for testing common hypotheses. One of the most common types of analysis is nodal regression, where the relationships between node-level network metrics and nodal covariates are analysed using a permutation technique known as node-label permutations. We show that, contrary to accepted wisdom, node-label permutations do not automatically account for the non-independences assumed to exist in network data, because regression-based permutation tests still assume exchangeability of residuals. The same assumption also applies to the quadratic assignment procedure (QAP), a permutation-based method often used for conducting dyadic regression. We highlight that node-label permutations produce the same p-values as equivalent parametric regression models, but that in the presence of non-independence, parametric regression models can also produce accurate effect size estimates. We also note that QAP only controls for a specific type of non-independence between edges that are connected to the same nodes, and that appropriate parametric regression models are also able to account for this type of non-independence. Based on this, we suggest that standard parametric models could be used in the place of permutation-based methods. Moving away from permutation-based methods could have several benefits, including reducing over-reliance on p-values, generating more reliable effect size estimates, and facilitating the adoption of causal inference methods and alternative types of statistical analysis. Supplementary Information: The online version contains supplementary material available at 10.1007/s00265-022-03254-x.

Patterns and consequences of age-linked change in local relatedness in animal societies.

The ultimate payoff of behaviours depends not only on their direct impact on an individual, but also on the impact on their relatives. Local relatedness-the average relatedness of an individual to their social environment-therefore has profound effects on social and life history evolution. Recent work has begun to show that local relatedness has the potential to change systematically over an individual's lifetime, a process called kinship dynamics. However, it is unclear how general these kinship dynamics are, whether they are predictable in real systems and their effects on behaviour and life history evolution. In this study, we combine modelling with data from real systems to explore the extent and impact of kinship dynamics. We use data from seven group-living mammals with diverse social and mating systems to demonstrate not only that kinship dynamics occur in animal systems, but also that the direction and magnitude of kinship dynamics can be accurately predicted using a simple model. We use a theoretical model to demonstrate that kinship dynamics can profoundly affect lifetime patterns of behaviour and can drive sex differences in helping and harming behaviour across the lifespan in social species. Taken together, this work demonstrates that kinship dynamics are likely to be a fundamental dimension of social evolution, especially when considering age-linked changes and sex differences in behaviour and life history.

Kinship dynamics: patterns and consequences of changes in local relatedness.

Mounting evidence suggests that patterns of local relatedness can change over time in predictable ways, a process termed kinship dynamics. Kinship dynamics may occur at the level of the population or social group, where the mean relatedness across all members of the population or group changes over time, or at the level of the individual, where an individual's relatedness to its local group changes with age. Kinship dynamics are likely to have fundamental consequences for the evolution of social behaviour and life history because they alter the inclusive fitness payoffs to actions taken at different points in time. For instance, growing evidence suggests that individual kinship dynamics have shaped the evolution of menopause and age-specific patterns of helping and harming. To date, however, the consequences of kinship dynamics for social evolution have not been widely explored. Here we review the patterns of kinship dynamics that can occur in natural populations and highlight how taking a kinship dynamics approach has yielded new insights into behaviour and life-history evolution. We discuss areas where analysing kinship dynamics could provide new insight into social evolution, and we outline some of the challenges in predicting and quantifying kinship dynamics in natural populations.

A long postreproductive life span is a shared trait among genetically distinct killer whale populations.

The extended female postreproductive life span found in humans and some toothed whales remains an evolutionary puzzle. Theory predicts demographic patterns resulting in increased female relatedness with age (kinship dynamics) can select for a prolonged postreproductive life span due to the combined costs of intergenerational reproductive conflict and benefits of late-life helping. Here, we test this prediction using >40 years of longitudinal demographic data from the sympatric yet genetically distinct killer whale ecotypes: resident and Bigg's killer whales. The female relatedness with age is predicted to increase in both ecotypes, but with a less steep increase in Bigg's due to their different social structure. Here, we show that there is a significant postreproductive life span in both ecotypes with >30% of adult female years being lived as postreproductive, supporting the general prediction that an increase in local relatedness with age predisposes the evolution of a postreproductive life span. Differences in the magnitude of kinship dynamics however did not influence the timing or duration of the postreproductive life span with females in both ecotypes terminating reproduction before their mid-40s followed by an expected postreproductive period of about 20 years. Our results highlight the important role of kinship dynamics in the evolution of a long postreproductive life span in long-lived mammals, while further implying that the timing of menopause may be a robust trait that is persistent despite substantial variation in demographic patterns among populations.

Age and sex influence social interactions, but not associations, within a killer whale pod.

Social structure is a fundamental aspect of animal populations. In order to understand the function and evolution of animal societies, it is important to quantify how individual attributes, such as age and sex, shape social relationships. Detecting these influences in wild populations under natural conditions can be challenging, especially when social interactions are difficult to observe and broad-scale measures of association are used as a proxy. In this study, we use unoccupied aerial systems to observe association, synchronous surfacing, and physical contact within a pod of southern resident killer whales (Orcinus orca). We show that interactions do not occur randomly between associated individuals, and that interaction types are not interchangeable. While age and sex did not detectably influence association network structure, both interaction networks showed significant social homophily by age and sex, and centrality within the contact network was higher among females and young individuals. These results suggest killer whales exhibit interesting parallels in social bond formation and social life histories with primates and other terrestrial social mammals, and demonstrate how important patterns can be missed when using associations as a proxy for interactions in animal social network studies.

Fine-scale genetic structure reflects limited and coordinated dispersal in the colonial monk parakeet, Myiopsitta monachus.

The genetic structure of animal populations has considerable behavioural, ecological and evolutionary implications and may arise from various demographic traits. Here, we use observational field data and molecular genetics to determine the genetic structure of an invasive population of monk parakeets, Myiopsitta monachus, at a range of spatial scales, and investigate the demographic processes that generate the observed structure. Monk parakeets construct large nests that can house several pairs occupying separate chambers; these nests are often aggregated within nesting trees. We determined patterns of relatedness within compound nests, within nesting trees and between trees. Spatial autocorrelation analyses of pairwise genetic relatedness revealed fine-scale genetic structure with relatives of both sexes spatially clustered within, but not beyond, nesting trees. In addition, males were more related to males sharing their compound nests than to other males occupying the same nesting tree. By contrast, males and females within compound nests were not significantly more closely related than elsewhere in the same tree, and we found no evidence for inbreeding. Adults showed high breeding site fidelity between years despite considerable disturbance of nest sites. Natal dispersal was female-biased, but dispersal distances were relatively short with some natal philopatry observed in both sexes. Sibling coalitions, typically of males, were observed amongst both philopatric and dispersing birds. Our results show significant clustering of kin within compound nests and nesting trees resulting from limited and coordinated natal dispersal, with subsequent breeding site fidelity. The resulting genetic structure has implications for social behaviour in this unusual parrot species.

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

1. Social 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 animal social networks. In particular, they have been used to test whether exogenous factors are related to network structure by interfacing these permutations with regression models. 2. Here, 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. 3. Our simulations show that, if used to indicate whether a relationship exists between network structure and a covariate, datastream permutations can result in extremely high type I error rates, in some cases approaching 50%. In the same set of simulations, traditional node-label permutations produced appropriate type I error rates (~ 5%). 4. Our analysis shows that datastream permutations do not represent the appropriate null hypothesis for these analyses. We suggest that potential alternatives to this procedure may be found in regarding the problems of non-independence of network data and unreliability of observations separately. If biases introduced during data collection can be corrected, either prior to model fitting or within the model itself, node-label permutations then serve as a useful test for interfacing animal social network analysis with regression modelling.

Ant colony nest networks adapt to resource disruption.

Animal social structure is shaped by environmental conditions, such as food availability. This is important as conditions are likely to change in the future and changes to social structure can have cascading ecological effects. Wood ants are a useful taxon for the study of the relationship between social structure and environmental conditions, as some populations form large nest networks and they are ecologically dominant in many northern hemisphere woodlands. Nest networks are formed when a colony inhabits more than one nest, known as polydomy. Polydomous colonies are composed of distinct sub-colonies that inhabit spatially distinct nests and that share resources with each other. In this study, we performed a controlled experiment on 10 polydomous wood ant (Formica lugubris) colonies to test how changing the resource environment affects the social structure of a polydomous colony. We took network maps of all colonies for 5 years before the experiment to assess how the networks changes under natural conditions. After this period, we prevented ants from accessing an important food source for a year in five colonies and left the other five colonies undisturbed. We found that preventing access to an important food source causes polydomous wood ant colony networks to fragment into smaller components and begin foraging on previously unused food sources. These changes were not associated with a reduction in the growth of populations inhabiting individual nests (sub-colonies), foundation of new nests or survival, when compared with control colonies. Colony splitting likely occurred as the availability of food in each nest changed causing sub-colonies to change their inter-nest connections. Consequently, our results demonstrate that polydomous colonies can adjust to environmental changes by altering their social network.

Alarm communication networks as a driver of community structure in African savannah herbivores.

Social information networks have the potential to shape the spatial structure of ecological communities by promoting the formation of mixed-species groups. However, what actually drives social affinity between species in the wild will depend on the characteristics of the species available to group. Here we first present an agent-based model that predicts trait-related survival benefits from mixed-species group formation in a multi-species community and we then test the model predictions in a community-wide field study of African savannah herbivores using multi-layered network analysis. We reveal benefits from information transfer about predators as a key determinant of mixed-species group formation, and that dilution benefits alone are not enough to explain patterns in interspecific sociality. The findings highlight the limitations of classical ecological approaches focusing only on direct trophic interactions when analysing community structure and suggest that declines in species occupying central social network positions, such as key informants, can have significant repercussions throughout communities.

Postreproductive killer whale grandmothers improve the survival of their grandoffspring.

Understanding why females of some mammalian species cease ovulation prior to the end of life is a long-standing interdisciplinary and evolutionary challenge. In humans and some species of toothed whales, females can live for decades after stopping reproduction. This unusual life history trait is thought to have evolved, in part, due to the inclusive fitness benefits that postreproductive females gain by helping kin. In humans, grandmothers gain inclusive fitness benefits by increasing their number of surviving grandoffspring, referred to as the grandmother effect. Among toothed whales, the grandmother effect has not been rigorously tested. Here, we test for the grandmother effect in killer whales, by quantifying grandoffspring survival with living or recently deceased reproductive and postreproductive grandmothers, and show that postreproductive grandmothers provide significant survival benefits to their grandoffspring above that provided by reproductive grandmothers. This provides evidence of the grandmother effect in a nonhuman menopausal species. By stopping reproduction, grandmothers avoid reproductive conflict with their daughters, and offer increased benefits to their grandoffspring. The benefits postreproductive grandmothers provide to their grandoffspring are shown to be most important in difficult times where the salmon abundance is low to moderate. The postreproductive grandmother effect we report, together with the known costs of late-life reproduction in killer whales, can help explain the long postreproductive life spans of resident killer whales.

The costs and benefits of decentralization and centralization of ant colonies.

A challenge faced by individuals and groups of many species is determining how resources and activities should be spatially distributed: centralized or decentralized. This distribution problem is hard to understand due to the many costs and benefits of each strategy in different settings. Ant colonies are faced by this problem and demonstrate two solutions: 1) centralizing resources in a single nest (monodomy) and 2) decentralizing by spreading resources across many nests (polydomy). Despite the possibilities for using this system to study the centralization/decentralization problem, the trade-offs associated with using either polydomy or monodomy are poorly understood due to a lack of empirical data and cohesive theory. Here, we present a dynamic network model of a population of ant nests which is based on observations of a facultatively polydomous ant species (Formica lugubris). We use the model to test several key hypotheses for costs and benefits of polydomy and monodomy and show that decentralization is advantageous when resource acquisition costs are high, nest size is limited, resources are clustered, and there is a risk of nest destruction, but centralization prevails when resource availability fluctuates and nest size is limited. Our model explains the phylogenetic and ecological diversity of polydomous ants, demonstrates several trade-offs of decentralization and centralization, and provides testable predictions for empirical work on ants and in other systems.

Using social network analysis of mixed-species groups in African savannah herbivores to assess how community structure responds to environmental change.

The dynamics of wildlife populations often depend heavily on interspecific interactions and understanding the underlying principles can be an important step in designing conservation strategies. Behavioural ecological studies can here provide useful insights into the structure and function of communities and their likely response to environmental changes. In this study of the Masai Mara herbivore community, we use a social network approach to investigate social affinities between species and how these change over the year in response to seasonal changes in ecological conditions. We find that even though social networks were correlated across different ecological conditions, for half the species dyads in the community, the strength of social affinities responded to changes in rainfall and/or the presence of migratory wildebeest. Several species consequentially adopted more or less central positions in the network depending on the ecological conditions. The findings point out interspecific social links that are likely to be attenuated or strengthened as a consequence of human-induced environmental changes and therefore call for particular attention from conservation managers. The eco-evolutionary ramifications of the perturbations of social affinities still require further study. This article is part of the theme issue 'Linking behaviour to dynamics of populations and communities: application of novel approaches in behavioural ecology to conservation'.

Linking behaviour to dynamics of populations and communities: application of novel approaches in behavioural ecology to conservation.

The impact of environmental change on the reproduction and survival of wildlife is often behaviourally mediated, placing behavioural ecology in a central position to quantify population- and community-level consequences of anthropogenic threats to biodiversity. This theme issue demonstrates how recent conceptual and methodological advances in the discipline are applied to inform conservation. The issue highlights how the focus in behavioural ecology on understanding variation in behaviour between individuals, rather than just measuring the population mean, is critical to explaining demographic stochasticity and thereby reducing fuzziness of population models. The contributions also show the importance of knowing the mechanisms by which behaviour is achieved, i.e. the role of learning, reasoning and instincts, in order to understand how behaviours change in human-modified environments, where their function is less likely to be adaptive. More recent work has thus abandoned the 'adaptationist' paradigm of early behavioural ecology and increasingly measures evolutionary processes directly by quantifying selection gradients and phenotypic plasticity. To support quantitative predictions at the population and community levels, a rich arsenal of modelling techniques has developed, and interdisciplinary approaches show promising prospects for predicting the effectiveness of alternative management options, with the social sciences, movement ecology and epidemiology particularly pertinent. The theme issue furthermore explores the relevance of behaviour for global threat assessment, and practical advice is given as to how behavioural ecologists can augment their conservation impact by carefully selecting and promoting their study systems, and increasing their engagement with local communities, natural resource managers and policy-makers. Its aim to uncover the nuts and bolts of how natural systems work positions behavioural ecology squarely in the heart of conservation biology, where its perspective offers an all-important complement to more descriptive 'big-picture' approaches to priority setting. This article is part of the theme issue 'Linking behaviour to dynamics of populations and communities: application of novel approaches in behavioural ecology to conservation'.

Analyses of ovarian activity reveal repeated evolution of post-reproductive lifespans in toothed whales.

In most species the reproductive system ages at the same rate as somatic tissue and individuals continue reproducing until death. However, females of three species - humans, killer whales and short-finned pilot whales - have been shown to display a markedly increased rate of reproductive senescence relative to somatic ageing. In these species, a significant proportion of females live beyond their reproductive lifespan: they have a post-reproductive lifespan. Research into this puzzling life-history strategy is hindered by the difficulties of quantifying the rate of reproductive senescence in wild populations. Here we present a method for measuring the relative rate of reproductive senescence in toothed whales using published physiological data. Of the sixteen species for which data are available (which does not include killer whales), we find that three have a significant post-reproductive lifespan: short-finned pilot whales, beluga whales and narwhals. Phylogenetic reconstruction suggests that female post-reproductive lifespans have evolved several times independently in toothed whales. Our study is the first evidence of a significant post-reproductive lifespan in beluga whales and narwhals which, when taken together with the evidence for post-reproductive lifespan in killer whales, doubles the number of non-human mammals known to exhibit post-reproductive lifespans in the wild.