The evolution and ecology of multiple antipredator defences.

Prey seldom rely on a single type of antipredator defence, often using multiple defences to avoid predation. In many cases, selection in different contexts may favour the evolution of multiple defences in a prey. However, a prey may use multiple defences to protect itself during a single predator encounter. Such "defence portfolios" that defend prey against a single instance of predation are distributed across and within successive stages of the predation sequence (encounter, detection, identification, approach (attack), subjugation and consumption). We contend that at present, our understanding of defence portfolio evolution is incomplete, and seen from the fragmentary perspective of specific sensory systems (e.g., visual) or specific types of defences (especially aposematism). In this review, we aim to build a comprehensive framework for conceptualizing the evolution of multiple prey defences, beginning with hypotheses for the evolution of multiple defences in general, and defence portfolios in particular. We then examine idealized models of resource trade-offs and functional interactions between traits, along with evidence supporting them. We find that defence portfolios are constrained by resource allocation to other aspects of life history, as well as functional incompatibilities between different defences. We also find that selection is likely to favour combinations of defences that have synergistic effects on predator behaviour and prey survival. Next, we examine specific aspects of prey ecology, genetics and development, and predator cognition that modify the predictions of current hypotheses or introduce competing hypotheses. We outline schema for gathering data on the distribution of prey defences across species and geography, determining how multiple defences are produced, and testing the proximate mechanisms by which multiple prey defences impact predator behaviour. Adopting these approaches will strengthen our understanding of multiple defensive strategies.

Fast life history traits promote invasion success in amphibians and reptiles.

Competing theoretical models make different predictions on which life history strategies facilitate growth of small populations. While 'fast' strategies allow for rapid increase in population size and limit vulnerability to stochastic events, 'slow' strategies and bet-hedging may reduce variance in vital rates in response to stochasticity. We test these predictions using biological invasions since founder alien populations start small, compiling the largest dataset yet of global herpetological introductions and life history traits. Using state-of-the-art phylogenetic comparative methods, we show that successful invaders have fast traits, such as large and frequent clutches, at both establishment and spread stages. These results, together with recent findings in mammals and plants, support 'fast advantage' models and the importance of high potential population growth rate. Conversely, successful alien birds are bet-hedgers. We propose that transient population dynamics and differences in longevity and behavioural flexibility can help reconcile apparently contrasting results across terrestrial vertebrate classes.

Experimental evidence that primate trichromacy is well suited for detecting primate social colour signals.

Primate trichromatic colour vision has been hypothesized to be well tuned for detecting variation in facial coloration, which could be due to selection on either signal wavelengths or the sensitivities of the photoreceptors themselves. We provide one of the first empirical tests of this idea by asking whether, when compared with other visual systems, the information obtained through primate trichromatic vision confers an improved ability to detect the changes in facial colour that female macaque monkeys exhibit when they are proceptive. We presented pairs of digital images of faces of the same monkey to human observers and asked them to select the proceptive face. We tested images that simulated what would be seen by common catarrhine trichromatic vision, two additional trichromatic conditions and three dichromatic conditions. Performance under conditions of common catarrhine trichromacy, and trichromacy with narrowly separated LM cone pigments (common in female platyrrhines), was better than for evenly spaced trichromacy or for any of the dichromatic conditions. These results suggest that primate trichromatic colour vision confers excellent ability to detect meaningful variation in primate face colour. This is consistent with the hypothesis that social information detection has acted on either primate signal spectral reflectance or photoreceptor spectral tuning, or both.

The role of life history traits in mammalian invasion success.

Why some organisms become invasive when introduced into novel regions while others fail to even establish is a fundamental question in ecology. Barriers to success are expected to filter species at each stage along the invasion pathway. No study to date, however, has investigated how species traits associate with success from introduction to spread at a large spatial scale in any group. Using the largest data set of mammalian introductions at the global scale and recently developed phylogenetic comparative methods, we show that human-mediated introductions considerably bias which species have the opportunity to become invasive, as highly productive mammals with longer reproductive lifespans are far more likely to be introduced. Subsequently, greater reproductive output and higher introduction effort are associated with success at both the establishment and spread stages. High productivity thus supports population growth and invasion success, with barriers at each invasion stage filtering species with progressively greater fecundity.

Assessing the potential information content of multicomponent visual signals: a machine learning approach.

Careful investigation of the form of animal signals can offer novel insights into their function. Here, we deconstruct the face patterns of a tribe of primates, the guenons (Cercopithecini), and examine the information that is potentially available in the perceptual dimensions of their multicomponent displays. Using standardized colour-calibrated images of guenon faces, we measure variation in appearance both within and between species. Overall face pattern was quantified using the computer vision 'eigenface' technique, and eyebrow and nose-spot focal traits were described using computational image segmentation and shape analysis. Discriminant function analyses established whether these perceptual dimensions could be used to reliably classify species identity, individual identity, age and sex, and, if so, identify the dimensions that carry this information. Across the 12 species studied, we found that both overall face pattern and focal trait differences could be used to categorize species and individuals reliably, whereas correct classification of age category and sex was not possible. This pattern makes sense, as guenons often form mixed-species groups in which familiar conspecifics develop complex differentiated social relationships but where the presence of heterospecifics creates hybridization risk. Our approach should be broadly applicable to the investigation of visual signal function across the animal kingdom.

Extraneous color affects female macaques' gaze preference for photographs of male conspecifics.

Humans find members of the opposite sex more attractive when their image is spatially associated with the color red. This effect even occurs when the red color is not on the skin or clothing (i.e. is extraneous). We hypothesize that this extraneous color effect could be at least partially explained by a low-level and biologically innate generalization process, and so similar extraneous color effects should be observed in non-humans. To test this possibility, we examined the influence of extraneous color in rhesus macaques (Macaca mulatta). Across two experiments, we determined the influence of extraneous red on viewing preferences (assessed by looking time) in free-ranging rhesus monkeys. We presented male and female monkeys with black and white photographs of the hindquarters of same and opposite sex conspecifics on either a red (experimental condition) or blue (control condition) background. As a secondary control, we also presented neutral stimuli (photographs of seashells) on red and blue backgrounds. We found that female monkeys looked longer at a picture of a male scrotum, but not a seashell, on a red background (Experiment 1), while males showed no bias. Neither male nor female monkeys showed an effect of color on looking time for female hindquarters or seashells (Experiment 2). The finding for females viewing males suggests that extraneous color affects preferences among rhesus macaques. Further, it raises the possibility that evolutionary processes gave rise to extraneous color effects during human evolution.

Proceedings of the Second Annual Deep Brain Stimulation Think Tank: What's in the Pipeline.

The proceedings of the 2nd Annual Deep Brain Stimulation Think Tank summarize the most contemporary clinical, electrophysiological, and computational work on DBS for the treatment of neurological and neuropsychiatric disease and represent the insights of a unique multidisciplinary ensemble of expert neurologists, neurosurgeons, neuropsychologists, psychiatrists, scientists, engineers and members of industry. Presentations and discussions covered a broad range of topics, including advocacy for DBS, improving clinical outcomes, innovations in computational models of DBS, understanding of the neurophysiology of Parkinson's disease (PD) and Tourette syndrome (TS) and evolving sensor and device technologies.

Sexually selected skin colour is heritable and related to fecundity in a non-human primate.

Sexual selection promotes the prevalence of heritable traits that increase an individual's reproductive rate. Despite theoretically strong directional selection, sexually selected traits can show inter-individual variation. Here, we investigate whether red skin ornamentation, a rare example of a male mammalian trait involved in mate attraction, influences fecundity and is heritable in rhesus macaques (Macaca mulatta), and explore the mechanisms that are involved in maintaining trait variation. Interestingly, the trait is expressed by and is attractive to both sexes. We collected facial images of 266 free-ranging individuals and modelled skin redness and darkness to rhesus macaque vision. We used 20 years of genetic parentage data to calculate selection gradients on the trait and perform heritability analyses. Results show that males who were both darkly coloured and high-ranking enjoyed higher fecundity. Female skin redness was positively linked to fecundity, although it remains unclear whether this influences male selectiveness. Heritability explained 10-15% of the variation in redness and darkness, and up to 30% for skin darkness when sexes are considered separately, suggesting sex-influenced inheritance. Our results suggest that inter-individual variation is maintained through condition-dependence, with an added effect of balancing selection on male skin darkness, providing rare evidence for a mammalian trait selected through inter-sexual selection.

Optimising the colour of traps requires an insect's eye view.

Colour is a critical property of many traps used to control or monitor insect pests, and applied entomologists continue to devote time and effort to improving colour for greater trapping efficiency. This work has often been guided by human colour perceptions, which differ greatly from those of the pests being studied. As a result, trap development can be a laborious process that is heavily reliant on trial and error. However, the responses of an insect's photoreceptors to a given trap colour can be calculated using well-established procedures. Photoreceptor responses represent sensory inputs that drive insect behaviour, and if their relationship to insect attraction can be determined or hypothesised, they provide metrics that can guide the rational optimisation of trap colour. This approach has recently been used successfully in separate studies of tsetse flies and thrips, but could be applied to a wide diversity of pest insects. Here we describe this approach to facilitate its use by applied entomologists. © 2023 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Analyzing visual signals as visual scenes.

The study of visual signal design is gaining momentum as techniques for studying signals become more sophisticated and more freely available. In this paper we discuss methods for analyzing the color and form of visual signals, for integrating signal components into visual scenes, and for producing visual signal stimuli for use in psychophysical experiments. Our recommended methods aim to be rigorous, detailed, quantitative, objective, and where possible based on the perceptual representation of the intended signal receiver(s). As methods for analyzing signal color and luminance have been outlined in previous publications we focus on analyzing form information by discussing how statistical shape analysis (SSA) methods can be used to analyze signal shape, and spatial filtering to analyze repetitive patterns. We also suggest the use of vector-based approaches for integrating multiple signal components. In our opinion elliptical Fourier analysis (EFA) is the most promising technique for shape quantification but we await the results of empirical comparison of techniques and the development of new shape analysis methods based on the cognitive and perceptual representations of receivers. Our manuscript should serve as an introductory guide to those interested in measuring visual signals, and while our examples focus on primate signals, the methods are applicable to quantifying visual signals in most taxa.

Human activities favour prolific life histories in both traded and introduced vertebrates.

Species' life histories determine population demographics and thus the probability that introduced populations establish and spread. Life histories also influence which species are most likely to be introduced, but how such 'introduction biases' arise remains unclear. Here, we investigate how life histories affect the probability of trade and introduction in phylogenetic comparative analyses across three vertebrate classes: mammals, reptiles and amphibians. We find that traded species have relatively high reproductive rates and long reproductive lifespans. Within traded species, introduced species have a more extreme version of this same life history profile. Species in the pet trade also have long reproductive lifespans but lack 'fast' traits, likely reflecting demand for rare species which tend to have slow life histories. We identify multiple species not yet traded or introduced but with life histories indicative of high risk of future trade, introduction and potentially invasion. Our findings suggest that species with high invasion potential are favoured in the wildlife trade and therefore that trade regulation is crucial for preventing future invasions.

Body size and life history shape the historical biogeography of tetrapods.

Dispersal across biogeographic barriers is a key process determining global patterns of biodiversity as it allows lineages to colonize and diversify in new realms. Here we demonstrate that past biogeographic dispersal events often depended on species' traits, by analysing 7,009 tetrapod species in 56 clades. Biogeographic models incorporating body size or life history accrued more statistical support than trait-independent models in 91% of clades. In these clades, dispersal rates increased by 28-32% for lineages with traits favouring successful biogeographic dispersal. Differences between clades in the effect magnitude of life history on dispersal rates are linked to the strength and type of biogeographic barriers and intra-clade trait variability. In many cases, large body sizes and fast life histories facilitate dispersal success. However, species with small bodies and/or slow life histories, or those with average traits, have an advantage in a minority of clades. Body size-dispersal relationships were related to a clade's average body size and life history strategy. These results provide important new insight into how traits have shaped the historical biogeography of tetrapod lineages and may impact present-day and future biogeographic dispersal.

A quantitative test of the predicted relationship between countershading and lighting environment.

Countershading, a vertical luminance gradient from a dark back to a light belly, is perhaps the most common coloration phenotype in the animal kingdom. Why? We investigated whether countershading functions as self-shadow concealment (SSC) in ruminants. We calculated "optimal" countershading for SSC by measuring illumination falling onto a model ruminant as a function of time of day and lighting environment. Calibrated images of 114 species of ruminant were compared to the countershading model, and phylogenetic analyses were used to find the best predictors of coats' countershading characteristics. In many species, countershading was close to the model's prediction of "optimal" countershading for SSC. Stronger countershading was associated with increased use of open lighting environments, living closer to the equator, and small body size. Abrupt transitions from dark to light tones were more common in open lighting environments but unassociated with group size or antipredator behavior. Though the SSC hypothesis prediction for stronger countershading in diurnal species was not supported and noncountershaded or reverse-countershaded species were unexpectedly common, this basic pattern of associations is explained only by the SSC hypothesis. Despite extreme variation in lighting conditions, many terrestrial animals still find protection from predation by compensating for their own shadows.

Inferring Phenotypic Trait Evolution on Large Trees With Many Incomplete Measurements.

Comparative biologists are often interested in inferring covariation between multiple biological traits sampled across numerous related taxa. To properly study these relationships, we must control for the shared evolutionary history of the taxa to avoid spurious inference. An additional challenge arises as obtaining a full suite of measurements becomes increasingly difficult with increasing taxa. This generally necessitates data imputation or integration, and existing control techniques typically scale poorly as the number of taxa increases. We propose an inference technique that integrates out missing measurements analytically and scales linearly with the number of taxa by using a post-order traversal algorithm under a multivariate Brownian diffusion (MBD) model to characterize trait evolution. We further exploit this technique to extend the MBD model to account for sampling error or non-heritable residual variance. We test these methods to examine mammalian life history traits, prokaryotic genomic and phenotypic traits, and HIV infection traits. We find computational efficiency increases that top two orders-of-magnitude over current best practices. While we focus on the utility of this algorithm in phylogenetic comparative methods, our approach generalizes to solve long-standing challenges in computing the likelihood for matrix-normal and multivariate normal distributions with missing data at scale.

Principled, practical, flexible, fast: a new approach to phylogenetic factor analysis.

Biological phenotypes are products of complex evolutionary processes in which selective forces influence multiple biological trait measurements in unknown ways. Phylogenetic comparative methods seek to disentangle these relationships across the evolutionary history of a group of organisms. Unfortunately, most existing methods fail to accommodate high-dimensional data with dozens or even thousands of observations per taxon. Phylogenetic factor analysis offers a solution to the challenge of dimensionality. However, scientists seeking to employ this modeling framework confront numerous modeling and implementation decisions, the details of which pose computational and replicability challenges.We develop new inference techniques that increase both the computational efficiency and modeling flexibility of phylogenetic factor analysis. To facilitate adoption of these new methods, we present a practical analysis plan that guides researchers through the web of complex modeling decisions. We codify this analysis plan in an automated pipeline that distills the potentially overwhelming array of decisions into a small handful of (typically binary) choices.We demonstrate the utility of these methods and analysis plan in four real-world problems of varying scales. Specifically, we study floral phenotype and pollination in columbines, domestication in industrial yeast, life history in mammals, and brain morphology in New World monkeys.General and impactful community employment of these methods requires a data scientific analysis plan that balances flexibility, speed and ease of use, while minimizing model and algorithm tuning. Even in the presence of non-trivial phylogenetic model constraints, we show that one may analytically address latent factor uncertainty in a way that (a) aids model flexibility, (b) accelerates computation (by as much as 500-fold) and (c) decreases required tuning. These efforts coalesce to create an accessible Bayesian approach to high-dimensional phylogenetic comparative methods on large trees.

A synthesis of deimatic behaviour.

Deimatic behaviours, also referred to as startle behaviours, are used against predators and rivals. Although many are spectacular, their proximate and ultimate causes remain unclear. In this review we aim to synthesise what is known about deimatic behaviour and identify knowledge gaps. We propose a working hypothesis for deimatic behaviour, and discuss the available evidence for the evolution, ontogeny, causation, and survival value of deimatic behaviour using Tinbergen's Four Questions as a framework. Our overarching aim is to direct future research by suggesting ways to address the most pressing questions in this field.

Why the leopard got its spots: relating pattern development to ecology in felids.

A complete explanation of the diversity of animal colour patterns requires an understanding of both the developmental mechanisms generating them and their adaptive value. However, only two previous studies, which involved computer-generated evolving prey, have attempted to make this link. This study examines variation in the camouflage patterns displayed on the flanks of many felids. After controlling for the effects of shared ancestry using a fully resolved molecular phylogeny, this study shows how phenotypes from plausible felid coat pattern generation mechanisms relate to ecology. We found that likelihood of patterning and pattern attributes, such as complexity and irregularity, were related to felids' habitats, arboreality and nocturnality. Our analysis also indicates that disruptive selection is a likely explanation for the prevalence of melanistic forms in Felidae. Furthermore, we show that there is little phylogenetic signal in the visual appearance of felid patterning, indicating that camouflage adapts to ecology over relatively short time scales. Our method could be applied to any taxon with colour patterns that can reasonably be matched to reaction-diffusion and similar models, where the kinetics of the reaction between two or more initially randomly dispersed morphogens determines the outcome of pattern development.

Tail autotomy works as a pre-capture defense by deflecting attacks.

Caudal autotomy is a dramatic antipredator adaptation where prey shed their tail in order to escape capture by a predator. The mechanism underlying the effectiveness of caudal autotomy as a pre-capture defense has not been thoroughly investigated. We tested two nonexclusive hypotheses, that caudal autotomy works by providing the predator with a "consolation prize" that makes it break off the hunt to consume the shed tail, and the deflection hypothesis, where the autotomy event directs predator attacks to the autotomized tail enabling prey escape. Our experiment utilized domestic dogs Canis familiaris as model predator engaged to chase a snake-like stimulus with a detachable tail. The tail was manipulated to vary in length (long versus short) and conspicuousness (green versus blue), with the prediction that dog attacks on the tail should increase with length under the consolation-prize hypothesis and conspicuous color under the deflection hypothesis. The tail was attacked on 35% of trials, supporting the potential for pre-capture autotomy to offer antipredator benefits. Dogs were attracted to the tail when it was conspicuously colored, but not when it was longer. This supports the idea that deflection of predator attacks through visual effects is the prime antipredator mechanism underlying the effectiveness of caudal autotomy as opposed to provision of a consolation prize meal.