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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

A Probable Case of Incipient Speciation in Schizocosa Wolf Spiders Driven by Allochrony, Habitat Use, and Female Mate Choice.

There is growing evidence that speciation can occur between populations that are not geographically isolated. The emergence of assortative mating is believed to be critical to this process, but how assortative mating arises in diverging populations is poorly understood. The wolf spider genus Schizocosa has become a model system for studying mechanisms of assortative mating. We conducted a series of experiments to identify the factors that control mate pair formation in a Schizocosa population that includes both ornamented and nonornamented males. We show that the population also includes two previously unrecognized female phenotypes. One female phenotype mates mostly or exclusively with ornamented males, and the other mates mostly or exclusively with unornamented males. Assortative mating within these groups is maintained by differences in maturation time, microhabitat use, and female mate preference. We conclude that the population is not a single species, as previously believed, but rather an incipient species pair with multiple overlapping mechanisms of reproductive isolation. The identification of a new incipient species pair in the well-studied and rapidly speciating Schizocosa clade presents new opportunities for the study of speciation without geographic isolation.

Using cross-disciplinary knowledge to facilitate advancements in animal communication and science communication research.

Although humans may have more nuanced reasons for communicating - e.g. to teach or inform, to share or change opinions or attitudes - all animals engage in communication with members of their own as well as other species, and there are more similarities than differences between non-human and human communication. All communication systems are composed of the same basic elements and all face comparable challenges. In this Commentary, we explore the extent to which research investigating how non-human animals communicate with each other (animal communication) overlaps in questions and approaches with research focused on how humans communicate with each other. We place a special focus on human communication involving scientific content, i.e. science communication. We begin with a brief review of the fields of animal communication and science communication. We next synthesize literature from each field to examine the roles, impacts and potential interactions of communication system elements - signaling environments, signalers, signal form and receivers - on effective communication. We find that research examining animal and human communication, including science communication, often has different emphases. Animal communication research, for example, tends to focus more on the role of the signaling environment through quantification of receiver responses. In contrast, science communication research currently emphasizes relationship building between signalers and receivers, and quantifies aspects of the receiver's psychology. Informed by our cross-disciplinary assessment, we propose potentially productive avenues of future research in both animal communication and science communication.

Development of site fidelity in the nocturnal amblypygid, Phrynus marginemaculatus.

Amblypygids are capable of navigation in the complex terrain of rainforests in near complete darkness. Path integration is unnecessary for successful homing, and the alternative mechanisms by which they navigate have yet to be elucidated. Here, our aims were to determine whether the amblypygid Phrynus marginemaculatus could be trained to reliably return to a target shelter in a laboratory arena-indicating goal recognition-and to document changes in behavior associated with the development of fidelity. We recorded nocturnal movements and space use by individuals over five nights in an arena in which subjects were provided with two shelters that differed in quality. The target shelter, unlike the alternative shelter, shielded subjects from light in daylight hours. Individuals consistently exited and returned to a shelter each night and from the third night onward chose the target shelter more often than the alternative shelter. Indeed, on the fifth night, every subject chose the target shelter. This transition was associated with changes in movement and space use in the arena. Notably, the movement features of outbound and inbound paths differed but did not change across nights. Individuals were also characterized by distinct behavioral strategies reflecting candidate homing mechanisms.

Importance of the antenniform legs, but not vision, for homing by the neotropical whip spider Paraphrynus laevifrons.

Amblypygids, or whip spiders, are nocturnal, predatory arthropods that display a robust ability to navigate to their home refuge. Prior field observations and displacement studies in amblypygids demonstrated an ability to home from distances as far away as 10 m. In the current study, micro-transmitters were used to take morning position fixes of individual Paraphrynus laevifrons following an experimental displacement of 10 m from their home refuge. The intention was to assess the relative importance of vision compared with sensory input acquired from the antenniform legs for navigation as well as other aspects of their spatial behavior. Displaced individuals were randomly assigned to three treatment groups: (i) control individuals; (ii) vision-deprived individuals, VD; and (iii) individuals with sensory input from the tips of their antenniform legs compromised, AD. Control and VD subjects were generally successful in returning home, and the direction of their movement on the first night following displacement was homeward oriented. By contrast, AD subjects experienced a complete loss of navigational ability, and movement on the first night indicated no hint of homeward orientation. The data strongly support the hypothesis that sensory input from the tips of the antenniform legs is necessary for successful homing in amblypygids following displacement to an unfamiliar location, and we hypothesize an essential role of olfaction for this navigational ability.

A systems approach to animal communication.

Why animal communication displays are so complex and how they have evolved are active foci of research with a long and rich history. Progress towards an evolutionary analysis of signal complexity, however, has been constrained by a lack of hypotheses to explain similarities and/or differences in signalling systems across taxa. To address this, we advocate incorporating a systems approach into studies of animal communication--an approach that includes comprehensive experimental designs and data collection in combination with the implementation of systems concepts and tools. A systems approach evaluates overall display architecture, including how components interact to alter function, and how function varies in different states of the system. We provide a brief overview of the current state of the field, including a focus on select studies that highlight the dynamic nature of animal signalling. We then introduce core concepts from systems biology (redundancy, degeneracy, pluripotentiality, and modularity) and discuss their relationships with system properties (e.g. robustness, flexibility, evolvability). We translate systems concepts into an animal communication framework and accentuate their utility through a case study. Finally, we demonstrate how consideration of the system-level organization of animal communication poses new practical research questions that will aid our understanding of how and why animal displays are so complex.

Benefits of size dimorphism and copulatory silk wrapping in the sexually cannibalistic nursery web spider, Pisaurina mira.

In sexually cannibalistic animals, male fitness is influenced not only by successful mate acquisition and egg fertilization, but also by avoiding being eaten. In the cannibalistic nursery web spider, Pisaurina mira, the legs of mature males are longer in relation to their body size than those of females, and males use these legs to aid in wrapping a female's legs with silk prior to and during copulation. We hypothesized that elongated male legs and silk wrapping provide benefits to males, in part through a reduced likelihood of sexual cannibalism. To test this, we paired females of random size with males from one of two treatment groups-those capable of silk wrapping versus those incapable of silk wrapping. We found that males with relatively longer legs and larger body size were more likely to mate and were less likely to be cannibalized prior to copulation. Regardless of relative size, males capable of silk wrapping were less likely to be cannibalized during or following copulation and had more opportunities for sperm transfer (i.e. pedipalpal insertions). Our results suggest that male size and copulatory silk wrapping are sexually selected traits benefiting male reproductive success.

Nocturnal foraging enhanced by enlarged secondary eyes in a net-casting spider.

Animals that possess extreme sensory structures are predicted to have a related extreme behavioural function. This study focuses on one such extreme sensory structure-the posterior median eyes of the net-casting spider Deinopis spinosa. Although past research has implicated the importance of vision in the nocturnal foraging habits of Deinopis, no direct link between vision in the enlarged eyes and nocturnal foraging has yet been made. To directly test the hypothesis that the enlarged posterior median eyes facilitate visually based nocturnal prey capture, we conducted repeated-measures, visual occlusion trials in both natural and laboratory settings. Our results indicate that D. spinosa relies heavily on visual cues detected by the posterior median eyes to capture cursorial prey items. We suggest that the enlarged posterior median eyes benefit D. spinosa not only through increased diet breadth, but also by allowing spiders to remain active solely at night, thus evading predation by diurnal animals.

Costly learning: preference for familiar food persists despite negative impact on survival.

Animals often rely on events in their environment that provide information (i.e. experience) to alter their future decision-making in ways that are presumed to be beneficial. Such experience-based learning, however, does not always lead to adaptive decision-making. In this study, we use the omnivorous harvestman Heteromitobates discolor to explore the role of past diet on subsequent food choice and survival. We first tested whether a short-term homogeneous diet (rotten crickets, fresh crickets or dog food) influenced subsequent food choice (rotten cricket versus fresh cricket). We next examine the impact of diet on survival. We found that following experience with a homogeneous cricket diet, adult harvestmen displayed a learned preference for familiar food, regardless of whether it was rotten or fresh crickets; individuals experiencing dog food were equally likely to choose rotten versus fresh crickets. We additionally found that individuals that ate rotten crickets suffered shorter survival than those that ate fresh crickets. Together, our results suggest that the diet an individual experiences can lead to maladaptive food preferences-preferences that ultimately result in reduced longevity.