Fast acrobatic maneuvers enable arboreal spiders to hunt dangerous prey.

Spiders, the most specious taxon of predators, have evolved an astounding range of predatory strategies, including group hunting, specialized silk traps, pheromone-loaded bolas, and aggressive mimicry. Spiders that hunt prey defended with behavioral, mechanical, or chemical means are under additional selection pressure to avoid injury and death. Ants are considered dangerous because they can harm or kill their predators, but some groups of spiders, such as the Theridiidae, have a very high diversification of ant-hunting species and strategies [J. Liu et al., Mol. Phylogenet. Evol. 94, 658-675 (2016)]. Here, we provide detailed behavioral analyses of the highly acrobatic Australian ant-slayer spider, Euryopis umbilicata (Theridiidae), that captures much larger and defended Camponotus ants on vertical tree trunks. The hunting sequence consists of ritualized steps performed within split seconds, resulting in an exceptionally high prey capture success rate.

Morphological ant mimics: constrained to imperfection?

Adaptive evolution relies on both heritable variation and selection. Variation is the raw material upon which selection acts, so any mechanism that limits or prevents the generation of heritable variation reduces the power of selection to lead to adaptation. Such limitations are termed evolutionary constraints. While it is widely accepted that constraints play an important role in shaping evolutionary outcomes, their relative importance, as opposed to adaptation, in determining evolutionary outcomes remains a subject of debate. Evolutionary constraints are often evoked as the reason behind the persistence of inaccurate mimicry. Here, we compared the variation and accuracy of body-shape mimicry in ant-mimicking spiders with that of ant-mimicking insects, predicting greater constraints, and hence inaccuracy, in spiders mimicking ants, due to their evolutionary distance from the ant model. We found high inter-species variation in mimetic accuracy, but dorsally, no overall difference in mimetic accuracy between spider and insect mimics, which is inconsistent with a constraint causing inaccurate mimicry. Our study provides empirical evidence suggesting that imperfect mimicry in spiders and insects is predominantly shaped by adaptive processes rather than constraints or chance. Our findings contribute to our understanding of the mechanisms underlying evolutionary diversity and the processes that shape phenotypic outcomes.

Building behavior does not drive rates of phenotypic evolution in spiders.

Do animals set the course for the evolution of their lineage when manipulating their environment? This heavily disputed question is empirically unexplored but critical to interpret phenotypic diversity. Here, we tested whether the macroevolutionary rates of body morphology correlate with the use of built artifacts in a megadiverse clade comprising builders and nonbuilders-spiders. By separating the inferred building-dependent rates from background effects, we found that variation in the evolution of morphology is poorly explained by artifact use. Thus natural selection acting directly on body morphology rather than indirectly via construction behavior is the dominant driver of phenotypic diversity.

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.

Stabilized Morphological Evolution of Spiders Despite Mosaic Changes in Foraging Ecology.

A prominent question in animal research is how the evolution of morphology and ecology interacts in the generation of phenotypic diversity. Spiders are some of the most abundant arthropod predators in terrestrial ecosystems and exhibit a diversity of foraging styles. It remains unclear how spider body size and proportions relate to foraging style, and if the use of webs as prey capture devices correlates with changes in body characteristics. Here, we present the most extensive data set to date of morphometric and ecological traits in spiders. We used this data set to estimate the change in spider body sizes and shapes over deep time and to test if and how spider phenotypes are correlated with their behavioral ecology. We found that phylogenetic variation of most traits best fitted an Ornstein-Uhlenbeck model, which is a model of stabilizing selection. A prominent exception was body length, whose evolutionary dynamics were best explained with a Brownian Motion (free trait diffusion) model. This was most expressed in the araneoid clade (ecribellate orb-weaving spiders and allies) that showed bimodal trends toward either miniaturization or gigantism. Only few traits differed significantly between ecological guilds, most prominently leg length and thickness, and although a multivariate framework found general differences in traits among ecological guilds, it was not possible to unequivocally associate a set of morphometric traits with the relative ecological mode. Long, thin legs have often evolved with aerial webs and a hanging (suspended) locomotion style, but this trend is not general. Eye size and fang length did not differ between ecological guilds, rejecting the hypothesis that webs reduce the need for visual cue recognition and prey immobilization. For the inference of the ecology of species with unknown behaviors, we propose not to use morphometric traits, but rather consult (micro-)morphological characters, such as the presence of certain podal structures. These results suggest that, in contrast to insects, the evolution of body proportions in spiders is unusually stabilized and ecological adaptations are dominantly realized by behavioral traits and extended phenotypes in this group of predators. This work demonstrates the power of combining recent advances in phylogenomics with trait-based approaches to better understand global functional diversity patterns through space and time. [Animal architecture; Arachnida; Araneae; extended phenotype; functional traits; macroevolution; stabilizing selection.].

Assassin bugs enhance prey capture with a sticky resin.

Tool-use in animals is a complex and rare phenomenon, particularly in insects. Tool-use in assassin bugs has been suggested as several species apply adhesive plant resins to their body, which has been hypothesized to function in enhancing prey capture. Here, we staged predatory interactions of resin-deprived and resin-equipped assassin bugs (Gorareduvius sp.) and discovered that applying resin as a tool conveys a clear predatory advantage to the assassin bugs. Gorareduvius sp. can thus be considered a tool-user, and since this behaviour was present in all individuals, including newly hatched nymphs, tool-use can be considered to be stereotyped. Our study, along with others, suggests that, when compared with other insects, tool-use is disproportionately common within the assassin bugs.

The Effect of Predator Population Dynamics on Batesian Mimicry Complexes.

AbstractUnderstanding Batesian mimicry is a classic problem in evolutionary biology. In Batesian mimicry, a defended species (the model) is mimicked by an undefended species (the mimic). Prior theories have emphasized the role of predator behavior and learning as well as evolution in model-mimic complexes but have not examined the role of population dynamics in potentially governing the relative abundances and even persistence of model-mimic systems. Here, we examined the effect of the population dynamics of predators and alternative prey on the prevalence of warning-signaling prey composed of models and mimics. Using optimal foraging theory and signal detection theory, we found that the inclusion of predator and alternative prey population dynamics could reverse traditional theoretical predictions: as alternative prey increase in numbers, mimics suffer because larger populations of predators are maintained, resulting in apparent competition. Under some circumstances, apparent competition affects model populations as well, although not as severely as it affects mimics. Our results bear on the intriguing puzzle that in nature warning signals are relatively scarce, yet experiments suggest that such signals can be highly advantageous. The availability of alternative prey and numerical responses by predators can overwhelm advantages observed in experiments to keep warning signals in model-mimic systems relatively scarce.

Mimicry in motion and morphology: do information limitation, trade-offs or compensation relax selection for mimetic accuracy?

Many animals mimic dangerous or undesirable prey as a defence from predators. We would expect predators to reliably avoid animals that closely resemble dangerous prey, yet imperfect mimics are common across a wide taxonomic range. There have been many hypotheses suggested to explain imperfect mimicry, but comparative tests across multiple mimicry systems are needed to determine which are applicable, and which-if any-represent general principles governing imperfect mimicry. We tested four hypotheses on Australian ant mimics and found support for only one of them: the information limitation hypothesis. A predator with incomplete information will be unable to discriminate some poor mimics from their models. We further present a simple model to show that predators are likely to operate with incomplete information because they forage and make decisions while they are learning, so might never learn to properly discriminate poor mimics from their models. We found no evidence that one accurate mimetic trait can compensate for, or constrain, another, or that rapid movement reduces selection pressure for good mimicry. We argue that information limitation may be a general principle behind imperfect mimicry of complex traits, while interactions between components of mimicry are unlikely to provide a general explanation for imperfect mimicry.

Limits of piriform silk adhesion-similar effects of substrate surface polarity on silk anchor performance in two spider species with disparate microhabitat use.

It has been suggested that physical interactions between biological and environmental surfaces may constrain ecological niche spaces. However, the mechanistic understanding of niche formation is frequently limited by the lack of information on the function and variation of these interactions. Here, we hypothesised that two closely related species of orb-web spiders have evolved different adhesion performance of web attachment (i.e. piriform silk) facilitating the occupation of contrasting microhabitats: plants versus rocks. Contrary to our prediction, we found that piriform silk adhesion was equally affected by surface chemistry in both species, with maximal adhesion on surfaces with high surface polarity and an average adhesion loss of 70-75% on low polar surfaces. Spiders did not respond to adhesion losses by increasing the anchor size, despite the repeated failure to attach their web to low polar surfaces. In a natural setting, poor adhesion on low polar surfaces may be mitigated by behavioural means, like the preference to place anchors on corrugated surface features such as leaf edges, or the spinning of multiple anchorages and formation of a bundled anchor line. Thus, microhabitat choice for web-building spiders may be governed by structural properties rather than surface chemistry. These results suggest that the repeatedly demonstrated effects of surface chemistry on bio-adhesion may be ecologically less important than assumed and that the role of behaviour in the evolution of bio-adhesion performance has been underestimated.

Predator chemical cues decrease attack time and increase metabolic rate in an orb-web spider.

Animals are able to assess the risk of predation and respond accordingly via behavioural and physiological changes. Web-building spiders are in the unique situation where they reside in the middle of their web and are therefore relatively exposed to predators. Thus, these spiders might moderate either their web-building behaviour or their behaviour on the web when exposed to the threat of predation. In this study, we experimentally explored how chemical cues from a predator influence foraging behaviour and metabolic rate in females of the orb-web spider Argiope keyserlingi We found that female spiders restricted their foraging time budget when exposed to the predator cues from a praying mantid: they responded 11% and 17% quicker to a vibratory stimulus compared with control and non-predator cues, respectively, and spent less time handling the prey. Moreover, spiders were less likely to rebuild the web under predator cues. Female A. keyserlingi exposed to the praying mantid cue significantly elevated their metabolic rate compared with the control group. Our findings revealed short-term modifications over the 2 week trials in foraging behaviour and the physiology of female spiders in response to predator cues. This study suggests that under predator cues the spiders move quicker and this could be facilitated by elevation in metabolic rate. Reduced foraging activity and less frequent web repair/rebuilding would also reduce the spiders' exposure to praying mantid predators.

Distinct spinning patterns gain differentiated loading tolerance of silk thread anchorages in spiders with different ecology.

Building behaviour in animals extends biological functions beyond bodies. Many studies have emphasized the role of behavioural programmes, physiology and extrinsic factors for the structure and function of buildings. Structure attachments associated with animal constructions offer yet unrealized research opportunities. Spiders build a variety of one- to three-dimensional structures from silk fibres. The evolution of economic web shapes as a key for ecological success in spiders has been related to the emergence of high performance silks and thread coating glues. However, the role of thread anchorages has been widely neglected in those models. Here, we show that orb-web (Araneidae) and hunting spiders (Sparassidae) use different silk application patterns that determine the structure and robustness of the joint in silk thread anchorages. Silk anchorages of orb-web spiders show a greater robustness against different loading situations, whereas the silk anchorages of hunting spiders have their highest pull-off resistance when loaded parallel to the substrate along the direction of dragline spinning. This suggests that the behavioural 'printing' of silk into attachment discs along with spinneret morphology was a prerequisite for the evolution of extended silk use in a three-dimensional space. This highlights the ecological role of attachments in the evolution of animal architectures.

Genital evolution: why are females still understudied?

The diversity, variability, and apparent rapid evolution of animal genitalia are a vivid focus of research in evolutionary biology, and studies exploring genitalia have dramatically increased over the past decade. These studies, however, exhibit a strong male bias, which has worsened since 2000, despite the fact that this bias has been explicitly pointed out in the past. Early critics argued that previous investigators too often considered only males and their genitalia, while overlooking female genitalia or physiology. Our analysis of the literature shows that overall this male bias has worsened with time. The degree of bias is not consistent between subdisciplines: studies of the lock-and-key hypothesis have been the most male focused, while studies of cryptic female choice usually consider both sexes. The degree of bias also differed across taxonomic groups, but did not associate with the ease of study of male and female genital characteristics. We argue that the persisting male bias in this field cannot solely be explained by anatomical sex differences influencing accessibility. Rather the bias reflects enduring assumptions about the dominant role of males in sex, and invariant female genitalia. New research highlights how rapidly female genital traits can evolve, and how complex coevolutionary dynamics between males and females can shape genital structures. We argue that understanding genital evolution is hampered by an outdated single-sex bias.

Short and fast vs long and slow: age changes courtship in male orb-web spiders (Argiope keyserlingi).

Male reproductive performance can vary with condition, age and future reproductive opportunities. Web-building spiders are ideal models to examine the effects of senescence on fitness-related behaviours due to strong selection on male courtship to reduce pre-copulatory sexual cannibalism. Argiope keyserlingi spiders generate courtship vibrations, or 'shudders', that reduce female aggression. We found that male A. keyserlingi courtship slowed with chronological age. Older males took longer to travel across the courtship thread, and overall number of shudders increased. Males retained some ability to modulate courtship quality (shudder duration and number of rocks within each shudder) in response to female quality. A change in courtship performance over time, despite strong selection for repeatability, indicates that ageing in male A. keyserlingi may have direct impacts on reproductive performance.

Producers and scroungers: feeding-type composition changes with group size in a socially foraging spider.

In groups of socially foraging animals, feeding behaviour may change with group size in response to varying cost-benefit trade-offs. Numerous studies have described group-size effects on group-average feeding behaviour, particularly emphasizing an increase in scrounging incidence for larger groups, where individuals (scroungers) feed from the food sources others (producers) discovered. However, individual variation in feeding behaviour remains unconsidered in the vast majority of these studies even though theoretical models predict individuals to specialize in feeding tactic and anticipate higher scrounger-type frequencies in larger groups. We combined group-level and individual-level analyses of group-size effects on social foraging in the subsocial spider Australomisidia ergandros Lending novel experimental support to model predictions, we found that individuals specialize in feeding tactic and that higher scrounging and lower producing incidence in larger groups were mediated through shifts in the ratio of feeding types. Further, feeding-type specialization was not explained by innate individual differences in hunting ability as all feeding types were equally efficient in prey capture when foraging alone. Context adaptivity of feeding behaviour might allow this subsocial species to succeed under varying socioecological conditions.

The role of ultraviolet colour in the assessment of mimetic accuracy between Batesian mimics and their models: a case study using ant-mimicking spiders.

The use of ultraviolet (UV) cues for intra- and inter-specific communication is common in many animal species. Still, the role of UV signals under some predator-prey contexts, such as Batesian mimicry, is not clear. Batesian mimicry is a defensive strategy by which a palatable species (the mimic) resembles an unpalatable or noxious species (the model) to avoid predation. This strategy has evolved independently in many different taxa that are predated by species capable of UV perception. Moreover, there is considerable variation in how accurately Batesian mimics resemble their models across species. Our aim was to investigate how UV colour contributed to mimetic accuracy using several ant-mimicking spider species as a case study. We measured the reflectance spectrum (300-700 nm) for several species of mimics and models, and we tested whether they differ in visible and UV colour. We modelled whether two different predators could discriminate between mimics and models using colour information. We found that generally, ant-mimicking spiders differed significantly from their ant models in UV colour and that information from the visible range of light cannot be extrapolated into the UV. Our modelling suggested that wasps should be able to discriminate between mimics and models combining information from visible and the UV light, whereas birds may not discriminate between them. Thus, we show that UV colour can influence mimic accuracy and we discuss its potential role in Batesian mimicry. We conclude that colour, especially in the UV range, should be taken into account when measuring mimetic accuracy.

An integrative framework for the appraisal of coloration in nature.

The world in color presents a dazzling dimension of phenotypic variation. Biological interest in this variation has burgeoned, due to both increased means for quantifying spectral information and heightened appreciation for how animals view the world differently than humans. Effective study of color traits is challenged by how to best quantify visual perception in nonhuman species. This requires consideration of at least visual physiology but ultimately also the neural processes underlying perception. Our knowledge of color perception is founded largely on the principles gained from human psychophysics that have proven generalizable based on comparative studies in select animal models. Appreciation of these principles, their empirical foundation, and the reasonable limits to their applicability is crucial to reaching informed conclusions in color research. In this article, we seek a common intellectual basis for the study of color in nature. We first discuss the key perceptual principles, namely, retinal photoreception, sensory channels, opponent processing, color constancy, and receptor noise. We then draw on this basis to inform an analytical framework driven by the research question in relation to identifiable viewers and visual tasks of interest. Consideration of the limits to perceptual inference guides two primary decisions: first, whether a sensory-based approach is necessary and justified and, second, whether the visual task refers to perceptual distance or discriminability. We outline informed approaches in each situation and discuss key challenges for future progress, focusing particularly on how animals perceive color. Given that animal behavior serves as both the basic unit of psychophysics and the ultimate driver of color ecology/evolution, behavioral data are critical to reconciling knowledge across the schools of color research.

Pollinator deception in the orchid mantis.

Mimicry has evolved in contexts such as camouflage, predator deterrence, luring of prey, and pollinator attraction. Mimicry of flowers has until now been demonstrated only in angiosperms, yet it has been hypothesized that the Malaysian orchid mantis Hymenopus coronatus mimics a flower to attract pollinators as prey. Despite the popularity of this charismatic insect, this long-discussed hypothesis has never been experimentally investigated. We found that, as predicted for mimicry, the color of H. coronatus is indistinguishable from the color of sympatric flowers for hymenopteran pollinators. Field experiments show that isolated mantises attract wild pollinators at a rate even higher than flowers and capture these pollinators as prey items. After more than a century of conjecture, we provide the first experimental evidence of pollinator deception in the orchid mantis and the first description of a unique predatory strategy that has not been documented in any other animal species.

Offspring dynamics affect food provisioning, growth and mortality in a brood-caring spider.

In brood-caring species, family members are faced with a conflict over resource distribution. While parents are selected to adapt the amount of care according to their offspring's needs, offspring might be selected to demand more care than optimal for parents. Recent studies on birds have shown that the social network structure of offspring affects the amount of care and thus the fitness of families. Such a network structure of repeated interactions is probably influenced by within-brood relatedness. We experimentally manipulated the group composition in a brood-caring spider to test how the presence of unrelated spiderlings affects the dynamics between female and brood as well as within broods. Broods consisting of siblings grew better and had a lower mortality compared with mixed broods, no matter whether the caring female was a genetic or foster mother. Interestingly, we found that foster mothers lost weight when caring for sibling broods, whereas females caring for mixed broods gained weight. This indicates that females may be willing to share more prey when the brood contains exclusively siblings even if the entire brood is unrelated to the female. Resource distribution may thus be negotiated by offspring dynamics that could have a signalling function to females.

Current evidence of climate-driven colour change in insects and its impact on sexual signals.

The colours of insects function in intraspecific communication such as sexual signalling, interspecific communication such as protection from predators, and in physiological processes, such as thermoregulation. The expression of melanin-based colours is temperature-dependent and thus likely to be impacted by a changing climate. However, it is unclear how climate change drives changes in body and wing colour may impact insect physiology and their interactions with conspecifics (e.g. mates) or heterospecific (e.g. predators or prey). The aim of this review is to synthesise the current knowledge of the consequences of climate-driven colour change on insects. Here, we discuss the environmental factors that affect insect colours, and then we outline the adaptive mechanisms in terms of phenotypic plasticity and microevolutionary response. Throughout we discuss the impact of climate-related colour change on insect physiology, and interactions with con-and-heterospecifics.

Cooler and drier conditions increase parasitism in a subtropical damselfly population.

Host-parasite interactions are impacted by climate, which may result in variation of parasitism across landscapes and time. Understanding how parasitism varies across these spatio-temporal scales is crucial to predicting how organisms will respond to and cope under a rapidly changing climate. Empirical work on how parasitism varies across climates is limited. Here, we examine the variation of parasitism across seasons and identify the likely climatic factors that explain this variation using Agriocnemis femina damselflies and Arrenurus water mite ectoparasites as a host-parasite study system. We assessed parasitism in a natural population in Sylhet, Bangladesh which is located in subtropical climate between 2021 and 2023. We calculated prevalence (proportion of infected individuals) and intensity (the number of parasites on an infected individual) of parasitism across different seasons. Parasite prevalence and intensity were greater during cooler seasons (autumn and winter) compared to hotter seasons (spring and summer). Mean temperature and precipitation were negatively correlated with parasite prevalence, whereas only mean precipitation was negatively correlated with parasite intensity. Tropical, subtropical and mediterranean regions are predicted to experience extreme climatic events (extreme temperature, less precipitation and frequent drought) as a consequence of anthropogenic climate change, and our finding suggests that this might alter patterns of parasitism in aquatic insects.