How hot is too hot? Metabolic responses to temperature across life stages of a small ectotherm.

To understand how global warming will impact biodiversity, we need to pay attention to those species with higher vulnerability. However, to assess vulnerability we also need to consider the thermoregulatory mechanisms, body size and thermal tolerance of species. Studies addressing thermal tolerance on small ectotherms have mostly focused on insects, while other arthropods such as arachnids remain understudied. Here, we quantified the physiological thermal sensitivity of the pseudoscorpion Dactylochelifer silvestris using a respirometry setup with a ramping temperature increase. Overall, we found that D. silvestris has a much lower metabolic rate than other organisms of similar size. As expected, metabolic rate increased with body size, with adults having larger metabolic rates, but the overall metabolic scaling exponent was low. Both the temperature at which metabolism peaked and the critical thermal maxima were high (above 44°C) and comparable to those of other arachnids. The activation energy, which characterizes the rising portion of the thermal sensitivity curve, was 0.66 eV, consistent with predictions for insects and other taxa in general. Heat tolerances and activation energy did not differ across life stages. We conclude that D. silvestris has low metabolic rates and a high thermal tolerance, which would likely influence how all stages and sexes of this species could endure climate change.

Influence of ambient water coloration on habitat and conspecific choice in the female Lake Malawi cichlid, Metriaclima zebra.

Female cichlid fish living in African great lakes are known to have sensory systems that are adapted to ambient light environments. These sensory system adaptations are hypothesized to have influenced the evolution of the diverse male nuptial coloration. In rock-dwelling Lake Malawi mbuna cichlids, however, the extent to which ambient light environments influence female sensory systems and potentially associated male nuptial coloration remains unknown. Yet, the ubiquitous blue flank coloration and UV reflection of male mbuna cichlids suggest the potential impacts of the blue-shifted ambient light environment on these cichlid's visual perception and male nuptial coloration in the shallow water depth in Lake Malawi. In the present study, we explored whether and how the sensory bias of females influences intersexual communication in the mbuna cichlid, Metriaclima zebra. A series of choice experiments in various light environments showed that M. zebra females 1) have a preference for the blue-shifted light environment, 2) prefer to interact with males in blue-shifted light environments, 3) do not show a preference between dominant and subordinate males in full-spectrum, long-wavelength filtered, and short-wavelength filtered light environments, and 4) show a "reversed" preference for subordinate males in the UV-filtered light environment. These results suggest that the visual perception of M. zebra females may be biased to the ambient light spectra in their natural habitat by local adaptation and that this sensory bias may influence the evolution of blue and UV reflective patterns in male nuptial coloration.

Vibroscape analysis reveals acoustic niche overlap and plastic alteration of vibratory courtship signals in ground-dwelling wolf spiders.

To expand the scope of soundscape ecology to encompass substrate-borne vibrations (i.e. vibroscapes), we analyzed the vibroscape of a deciduous forest floor using contact microphone arrays followed by automated processing of large audio datasets. We then focused on vibratory signaling of ground-dwelling Schizocosa wolf spiders to test for (i) acoustic niche partitioning and (ii) plastic behavioral responses that might reduce the risk of signal interference from substrate-borne noise and conspecific/heterospecific signaling. Two closely related species - S. stridulans and S. uetzi - showed high acoustic niche overlap across space, time, and dominant frequency. Both species show plastic behavioral responses - S. uetzi males shorten their courtship in higher abundance of substrate-borne noise, S. stridulans males increased the duration of their vibratory courtship signals in a higher abundance of conspecific signals, and S. stridulans males decreased vibratory signal complexity in a higher abundance of S. uetzi signals.

Could sexual selection be driven by the mistaken inferences of young females?

A new evolutionary model of mate choice copying, published in PLOS Biology, aims to reconcile mismatches between theory and data by proposing that juvenile females mistakenly imprint on male phenotypes that were not in fact preferred by the female they copied.

Investigating boundary-geometry use by whip spiders (Phrynus marginemaculatus) during goal-directed navigation.

Previous studies have shown that whip spiders (Amblypygi) can use a variety of cues to navigate to and recognize a home refuge. The current study aimed to determine whether whip spiders were capable of using the boundary geometry of an experimental space (geometric information) to guide goal-directed navigation and to investigate any preferential use of geometric or feature (visual) information. Animals were first trained to find a goal location situated in one corner of a rectangular arena (geometric information) fronting a dark-green-colored wall, which created a brightness contrast with the other three white walls (feature information). Various probe trials were then implemented to determine cue use. It was found that animals were capable of directing their choice behavior towards geometrically correct corners at a rate significantly higher than chance, even when the feature cue was removed. By contrast, choice behavior dropped to random chance when geometric information was removed (test in a square arena) and only feature information remained. Choice behavior was also reduced to chance when geometric and feature information were set in conflict (by moving the feature cue to one of the longer walls in the rectangular arena). The data thus suggest that whip spiders are capable of using geometric information to guide goal-directed navigation and that geometric information is preferred over feature guidance, although a feature cue may set the context for activating geometry-guided navigation. Experimental design limitations and future directions are discussed.

Light Environment Interacts with Visual Displays in a Species-Specific Manner in Multimodal-Signaling Wolf Spiders.

AbstractLight availability is highly variable, yet predictable, over various timescales and is expected to play an important role in the evolution of visual signals. Courtship displays of the wolf spider genus Schizocosa always involve the use of substrate-borne vibrations; however, there is substantial variation in the presence and complexity of visual displays among species. To gain insight into the role the light environment plays in the evolution of courtship displays, we tested the function of visual courtship signaling across distinct light environments in four species of Schizocosa that vary in their degree of ornamentation and dynamic visual signals. We ran mating and courtship trials at three light intensities (bright, dim, and dark) and tested the hypothesis that ornamentation interacts with light environment. We also examined each species' circadian activity patterns. The effects of the light environment on courtship and mating varied between species, as did circadian activity patterns. Our results suggest that femur pigmentation may have evolved for diurnal signaling, whereas tibial brushes may function to increase signal efficacy under dim light. Additionally, we found evidence for light-dependent changes in selection on male traits, illustrating that short-term changes in light intensity have the potential for strong effects on the dynamics of sexual selection.

Comparative biology of spatial navigation in three arachnid orders (Amblypygi, Araneae, and Scorpiones).

From both comparative biology and translational research perspectives, there is escalating interest in understanding how animals navigate their environments. Considerable work is being directed towards understanding the sensory transduction and neural processing of environmental stimuli that guide animals to, for example, food and shelter. While much has been learned about the spatial orientation behavior, sensory cues, and neurophysiology of champion navigators such as bees and ants, many other, often overlooked animal species possess extraordinary sensory and spatial capabilities that can broaden our understanding of the behavioral and neural mechanisms of animal navigation. For example, arachnids are predators that often return to retreats after hunting excursions. Many of these arachnid central-place foragers are large and highly conducive to scientific investigation. In this review we highlight research on three orders within the Class Arachnida: Amblypygi (whip spiders), Araneae (spiders), and Scorpiones (scorpions). For each, we describe (I) their natural history and spatial navigation, (II) how they sense the world, (III) what information they use to navigate, and (IV) how they process information for navigation. We discuss similarities and differences among the groups and highlight potential avenues for future research.

Mate Sampling Behavior Determines the Density Dependence of Sexual Selection.

AbstractTheory predicts that the strength of sexual selection (i.e., how well a trait predicts mating or fertilization success) should increase with population density, yet empirical support remains mixed. We explore how this discrepancy might reflect a disconnect between current theory and our understanding of the strategies individuals use to choose mates. We demonstrate that the density dependence of sexual selection predicted by previous theory arises from the assumption that individuals automatically sample more potential mates at higher densities. We provide an updated theoretical framework for the density dependence of sexual selection by (1) developing models that clarify the mechanisms through which density-dependent mate sampling strategies might be favored by selection and (2) using simulations to determine how sexual selection changes with population density when individuals use those strategies. We find that sexual selection may increase strongly with density if sampling strategies change adaptively in response to density-dependent sampling costs, whereas within-individual plasticity in sampling over time (e.g., due to adaptation to increasing sampling costs as the breeding season progresses) produces weaker density-dependent sexual selection. Our findings suggest that density dependence of sexual selection depends on the ecological context in which mate sampling has evolved.

Increased signal complexity is associated with increased mating success.

The evolution of complex signals has often been explored by testing multiple functional hypotheses regarding how independent signal components provide selective benefits to offset the costs of their production. In the present study, we take a different approach by exploring the function of complexity per se. We test the hypothesis that increased vibratory signal complexity-based on both proportional and temporal patterning-provides selective benefits to courting male Schizocosa stridulans wolf spiders. In support of this hypothesis, all of our quantified metrics of vibratory signal complexity predicted the mating success of male S. stridulans. The rate of visual signalling, which is mechanistically tied to vibratory signal production, was also associated with mating success. We additionally found evidence that males can dynamically adjust the complexity of their vibratory signalling. Together, our results suggest that complexity per se may be a target of female choice.

Exploring Higher-Order Conceptual Learning in an Arthropod with a Large Multisensory Processing Center.

Comparative cognition aims to understand the evolutionary history and current function of cognitive abilities in a variety of species with diverse natural histories. One characteristic often attributed to higher cognitive abilities is higher-order conceptual learning, such as the ability to learn concepts independent of stimuli-e.g., 'same' or 'different'. Conceptual learning has been documented in honeybees and a number of vertebrates. Amblypygids, nocturnal enigmatic arachnids, are good candidates for higher-order learning because they are excellent associational learners, exceptional navigators, and they have large, highly folded mushroom bodies, which are brain regions known to be involved in learning and memory in insects. In Experiment 1, we investigate if the amblypygid Phrynus marginimaculatus can learn the concept of same with a delayed odor matching task. In Experiment 2, we test if Paraphrynus laevifrons can learn same/different with delayed tactile matching and nonmatching tasks before testing if they can transfer this learning to a novel cross-modal odor stimulus. Our data provide no evidence of conceptual learning in amblypygids, but more solid conclusions will require the use of alternative experimental designs to ensure our negative results are not simply a consequence of the designs we employed.

Phylogeny and secondary sexual trait evolution in Schizocosa wolf spiders (Araneae, Lycosidae) shows evidence for multiple gains and losses of ornamentation and species delimitation uncertainty.

Members of the Nearctic spider genus Schizocosa Chamberlin, 1904 have garnered much attention in behavioral studies and over many decades, a number of species have developed as model systems for investigating patterns of sexual selection and multimodal communication. Many of these studies have employed a comparative approach using putative, but not rigorously tested, sister species pairs that have distinctive morphological traits and attendant behaviors. Despite past emphasis on the efficacy of these presumably comparative-based studies of closely related species, generating a robust phylogenetic hypothesis for Schizocosa has been an ongoing challenge. Here, we apply a phylogenomic approach using anchored hybrid enrichment to generate a data set comprising over 400 loci representing a comprehensive taxonomic sample of 23 Nearctic Schizocosa. Our sampling also includes numerous outgroup lycosid genera that allow for a robust evaluation of genus monophyly. Based on analyses using concatenation and coalescent-based methods, we recover a well-supported phylogeny that infers the following: 1) The New World Schizocosa do not form a monophyletic group; 2) Previous hypotheses of North American species require reconsideration along with the composition of species groups; 3) Multiple longstanding model species are not genealogically exclusive and thus are not "good" species; 4) This updated phylogenetic framework establishes a new working paradigm for studying the evolution of characters associated with reproductive communication and mating. Ancestral character state reconstructions show a complex pattern of homoplasy that has likely obfuscated previous attempts to reconstruct relationships and delimit species. Important characters presumably related to sexual selection, such as foreleg pigmentation and dense bristle formation, have undergone repeated gain and loss events, many of which have led to increased morphological divergence between sister-species. Evaluation of these traits in a comparative framework illuminates how sexual selection and natural selection influence character evolution and provides a model for future studies of multimodal communication evolution and function.

Identification and quantification of 11 airborne biochemicals emitted by the brown recluse and another primitive hunting spider using headspace solid-phase microextraction-GC/MS.

Loxosceles reclusa, or brown recluse spider, is a harmful household spider whose habitat extends throughout the Midwest in the USA and other regions in the world. The pheromones and other biomolecules that facilitate signaling for brown recluses and other spider species are poorly understood. A rapid and sensitive method is needed to analyze airborne spider signaling biomolecules to better understand the structure and function of these biochemicals in order to control the population of the spiders. In this study, we developed a novel headspace solid-phase microextraction (HS-SPME)-GC/MS method to analyze potential pheromones and biomolecules emitted by the brown recluse spider. The method is highly selective and sensitive for biomolecule identification and quantification from a single live spider. Using this novel non-destructive HS-SPME-GC/MS technique, we identified 11 airborne biomolecules, including 4-methylquinazoline, dimethyl sulfone, 2-methylpropanoic acid, butanoic acid, hexanal, 3-methylbutanoic acid, 2-methylbutanoic acid, 2,4-dimethylbenzaldehyde, 2-phenoxyethanol, and citral (contains both isomers of neral and geranial). Some of these airborne biomolecules were also reported as semiochemicals associated with biological functions of other spiders and insects. The method was also applied to study the airborne biochemicals of Plectreurys tristis, another primitive hunting spider with a poor web, enabling quantitation of the same compounds and demonstrating a difference in signaling molecule concentrations between the two species. This method has potential application in the study of pheromones and biological signaling in other species, which allows for the possibility of utilizing attractant or deterrent functions to limit household populations of harmful species.

Visual control of refuge recognition in the whip spider Phrynus marginemaculatus.

Amblypygids, or whip spiders, are nocturnally active arachnids which live in structurally complex environments. Whip spiders are excellent navigators that can re-locate a home refuge without relying on visual input. Therefore, an open question is whether visual input can control any aspect of whip spider spatial behavior. In the current study, Phrynus marginemaculatus were trained to locate an escape refuge by discriminating between differently oriented black and white stripes placed either on the walls of a testing arena (frontal discrimination) or on the ceiling of the same testing arena (overhead discrimination). Regardless of the placement of the visual stimuli, the whip spiders were successful in learning the location of the escape refuge. In a follow-up study of the overhead discrimination, occluding the median eyes was found to disrupt the ability of the whip spiders to locate the shelter. The data support the conclusion that whip spiders can rely on vision to learn and recognize an escape shelter. We suggest that visual inputs to the brain's mushroom bodies enable this ability.

Sister species diverge in modality-specific courtship signal form and function.

Understanding the relative importance of different sources of selection (e.g., the environment, social/sexual selection) on the divergence or convergence of reproductive communication can shed light on the origin, maintenance, or even disappearance of species boundaries. Using a multistep approach, we tested the hypothesis that two presumed sister species of wolf spider with overlapping ranges and microhabitat use, yet differing degrees of sexual dimorphism, have diverged in their reliance on modality-specific courtship signaling. We predicted that male Schizocosa crassipalpata (no ornamentation) rely predominantly on diet-dependent vibratory signaling for mating success. In contrast, we predicted that male S. bilineata (black foreleg brushes) rely on diet-dependent visual signaling. We first tested and corroborated the sister-species relationship between S. crassipalpata and S. bilineata using phylogenomic scale data. Next, we tested for species-specific, diet-dependent vibratory and visual signaling by manipulating subadult diet and subsequently quantifying adult morphology and mature male courtship signals. As predicted, vibratory signal form was diet-dependent in S. crassipalpata, while visual ornamentation (brush area) was diet-dependent in S. bilineata. We then compared the species-specific reliance on vibratory and visual signaling by recording mating across artificially manipulated signaling environments (presence/absence of each modality in a 2 × 2 full factorial design). In accordance with our diet dependence results for S. crassipalpata, the presence of vibratory signaling was important for mating success. In contrast, the light and vibratory environment interacted to influence mating success in S. bilineata, with vibratory signaling being important only in the absence of light. We found no differences in overall activity patterns. Given that these species overlap in much of their range and microhabitat use, we suggest that competition for signaling space may have led to the divergence and differential use of sensory modalities between these sister species.

Multisensory integration supports configural learning of a home refuge in the whip spider Phrynus marginemaculatus.

Whip spiders (Amblypygi) reside in structurally complex habitats and are nocturnally active yet display notable navigational abilities. From the theory that uncertainty in sensory inputs should promote multisensory representations to guide behavior, we hypothesized that their navigation is supported by a multisensory and perhaps configural representation of navigational inputs, an ability documented in a few insects and never reported in arachnids. We trained Phrynus marginemaculatus to recognize a home shelter characterized by both discriminative olfactory and tactile stimuli. In tests, subjects readily discriminated between shelters based on the paired stimuli. However, subjects failed to recognize the shelter in tests with either of the component stimuli alone. This result is consistent with the hypothesis that the terminal phase of their navigational behavior, shelter recognition, can be supported by the integration of multisensory stimuli as an enduring, configural representation. We hypothesize that multisensory learning occurs in the whip spiders' extraordinarily large mushroom bodies, which may functionally resemble the hippocampus of vertebrates.

Ogre-Faced, Net-Casting Spiders Use Auditory Cues to Detect Airborne Prey.

Prey capture behavior among spiders varies greatly from passive entrapment in webs to running down prey items on foot. Somewhere in the middle are the ogre-faced, net-casting spiders [1] (Deinopidae: Deinopis) that actively capture prey while being suspended within a frame web [2-5]. Using a net held between their front four legs, these spiders lunge downward to ensnare prey from off the ground beneath them. This "forward strike" is sensorially mediated by a massive pair of hypersensitive, night-vision eyes [5-7]. Deinopids can also intercept flying insects with a "backward strike," a ballistically rapid, overhead back-twist, that seems not to rely on visual cues [4, 5, 8]. Past reports have hypothesized a role of acoustic detection in backward strike behavior [4, 5, 8]. Here, we report that the net-casting spider, Deinopis spinosa, can detect auditory stimuli from at least 2 m from the sound source, at or above 60 dB SPL, and that this acoustic sensitivity is sufficient to trigger backward strike behavior. We present neurophysiological recordings in response to acoustic stimulation, both from sound-sensitive areas in the brain and isolated forelegs, which demonstrate a broad range of auditory sensitivity (100-10,000 Hz). Moreover, we conducted behavioral assays of acoustic stimulation that confirm acoustic triggering of backward net-casting by frequencies in harmony with flight tones of known prey. However, acoustic stimulation using higher frequency sounds did not elicit predatory responses in D. spinosa. We hypothesize higher frequencies are emitted by avian predators and that detecting these auditory cues may aid in anti-predator behavior. VIDEO ABSTRACT.

Vertical-surface navigation in the Neotropical whip spider Paraphrynus laevifrons (Arachnida: Amblypygi).

Studies on whip spider navigation have focused on their ability to locate goal locations in the horizontal plane (e.g., when moving along the ground). However, many species of tropical whip spiders reside and move along surfaces in the vertical plane (e.g., trees). Under controlled laboratory conditions, the current study investigated the ability of the tropical whip spider, Paraphrynus laevifrons, to return to a home shelter on a vertical surface in the presence of numerous, similar and competing refuge sites, as well as the distribution of navigational errors in the vertical, horizontal and diagonal plane. We also assessed the relative importance of sensory cues originating from a previously occupied home shelter compared to the position of a previously occupied shelter in guiding shelter choice. It was found that P. laevifrons displays robust fidelity in re-locating a home shelter on a vertical surface. When navigational errors did occur, they were not significantly different in all three directions. Additionally, cue-conflict test trials revealed that cues associated with an original home shelter, likely self-deposited chemical signals, were more important than sources of positional information in guiding the shelter choice of P. laevifrons.

Ecophysiological determinants of sexual size dimorphism: integrating growth trajectories, environmental conditions, and metabolic rates.

Sexual size dimorphism (SSD) often results in dramatic differences in body size between females and males. Despite its ecological importance, little is known about the relationship between developmental, physiological, and energetic mechanisms underlying SSD. We take an integrative approach to understand the relationship between developmental trajectories, metabolism, and environmental conditions resulting in extreme female-biased SSD in the crab spider Mecaphesa celer (Thomisidae). We tested for sexual differences in growth trajectories, as well as in the energetics of growth, hypothesizing that female M. celer have lower metabolic rates than males or higher energy assimilation. We also hypothesized that the environment in which spiderlings develop influences the degree of SSD of a population. We tracked growth and resting metabolic rates of female and male spiderlings throughout their ontogeny and quantified the adult size of individuals raised in a combination of two diet and two temperature treatments. We show that M. celer's SSD results from differences in the shape of female and male growth trajectories. While female and male resting metabolic rates did not differ, diet, temperature, and their interaction influenced body size through an interactive effect with sex, with females being more sensitive to the environment than males. We demonstrate that the shape of the growth curve is an important but often overlooked determinant of SSD and that females may achieve larger sizes through a combination of high food ingestion and low activity levels. Our results highlight the need for new models of SSD based on ontogeny, ecology, and behavior.

Contemporary sexual selection does not explain variation in male display traits among populations.

Sexual selection is widely hypothesized to facilitate the evolution of reproductive isolation through divergence in sexual traits and sexual trait preferences among populations. However, direct evidence of divergent sexual selection causing intraspecific trait divergence remains limited. Using the wolf spider Schizocosa crassipes, we characterized patterns of female mate choice within and among geographic locations and related those patterns to geographic variation in male display traits to test whether divergent sexual selection caused by mate choice explains intraspecific trait variation. We found evidence of phenotypic selection on male behavior arising from female mate choice, but no evidence that selection varied among locations. Only those suites of morphological and behavioral traits that did not influence mate choice varied geographically. These results are inconsistent with ongoing divergent sexual selection underlying the observed intraspecific divergence in male display traits. These findings align with theory on the potentially restrictive conditions under which divergent sexual selection may persist, and suggest that long-term studies capable of detecting periodic or transient divergent sexual selection will be critical to rigorously assess the relative importance of divergent sexual selection in intraspecific trait divergence.