Visual signals in the wing display of a tephritid fly deter jumping spider attacks.

Visual animal communication, whether to the same or to other species, is largely conducted through dynamic and colourful signals. For a signal to be effective, the signaller must capture and retain the attention of the receiver. Signal efficacy is also dependent on the sensory limitations of the receiver. However, most signalling studies consider movement and colour separately, resulting in a partial understanding of the signal in question. We explored the structure and function of predator-prey signalling in the jumping spider-tephritid fly system, where the prey performs a wing waving display that deters an attack from the predator. Using a custom-built spider retinal tracker combined with visual modelling, as well as behavioural assays, we studied the effect of fly wing movement and colour on the jumping spider's visual system. We show that jumping spiders track their prey less effectively during wing display and this can be attributed to a series of fluctuations in chromatic and achromatic contrasts arising from the wing movements. These results suggest that displaying flies deter spider attacks by manipulating the movement biases of the spider's visual system. Our results emphasise the importance of receiver attention on the evolution of interspecific communication.

Attention and distraction in the modular visual system of a jumping spider.

Animals must selectively attend to relevant stimuli and avoid being distracted by unimportant stimuli. Jumping spiders (Salticidae) do this by coordinating eyes with different capabilities. Objects are examined by a pair of high-acuity principal eyes, whose narrow field of view is compensated for by retinal movements. The principal eyes overlap in field of view with motion-sensitive anterior-lateral eyes (ALEs), which direct their gaze to new stimuli. Using a salticid-specific eyetracker, we monitored the gaze direction of the principal eyes as they examined a primary stimulus. We then presented a distractor stimulus visible only to the ALEs and observed whether the principal eyes reflexively shifted their gaze to it or whether this response was flexible. Whether spiders redirected their gaze to the distractor depended on properties of both the primary and distractor stimuli. This flexibility suggests that higher-order processing occurs in the management of the attention of the principal eyes.

Variations on a theme: Morphological variation in the secondary eye visual pathway across the order of Araneae.

Spiders possess a wide array of sensory-driven behaviors and therefore provide rich models for studying evolutionary hypotheses about the relationship between brain morphology, sensory systems, and behavior. Despite this, only a handful of studies have examined brain variation across the order of Araneae. In this study, I present descriptions of the gross brain morphology for 19 families of spiders that vary in eye morphology. Spiders showed the most variation in the secondary eye visual pathway. Based on this variation, spiders could be categorized into four groups. Group 1 spiders had small, underdeveloped laminae, no medullae, and no mushroom bodies. Group 2 spiders had large laminae, no medullae and large mushroom bodies. Group 3 spiders had laminae and some evidence of reduced medullae and mushroom bodies. Group 4 spiders had the most complex systems, with large laminae, medullae formed from optical glomeruli, and robust mushroom bodies. Within groups, there was large variation in the shape and size of individual regions, indicating possible variation in neuronal organization. The possible evolutionary implications of the loss of a dedicated olfactory organ in spiders and its effects on the mushroom body are also discussed.

The central nervous system of whip spiders (Amblypygi): Large mushroom bodies receive olfactory and visual input.

Whip spiders (Amblypygi) are known for their nocturnal navigational abilities, which rely on chemosensory and tactile cues and, to a lesser degree, on vision. Unlike true spiders, the first pair of legs in whip spiders is modified into extraordinarily long sensory organs (antenniform legs) covered with thousands of mechanosensory, olfactory, and gustatory sensilla. Olfactory neurons send their axons through the leg nerve into the corresponding neuromere of the central nervous system, where they terminate on a particularly large number (about 460) of primary olfactory glomeruli, suggesting an advanced sense of smell. From the primary glomeruli, olfactory projection neurons ascend to the brain and terminate in the mushroom body calyx on a set of secondary olfactory glomeruli, a feature that is not known from olfactory pathways of other animals. Another part of the calyx receives visual input from the secondary visual neuropil (the medulla). This calyx region is composed of much smaller glomeruli ("microglomeruli"). The bimodal input and the exceptional size of their mushroom bodies may support the navigational capabilities of whip spiders. In addition to input to the mushroom body, we describe other general anatomical features of the whip spiders' central nervous system.

Lateral eyes direct principal eyes as jumping spiders track objects.

One way of circumventing the functional tradeoffs on eye design [1,2] is to have different eyes for different tasks. For example, jumping spiders (Salticidae), known for elaborate, visually guided courtship and predatory behavior [3], view the same object simultaneously with two of their four pairs of eyes: the antero-lateral eyes (ALEs) and the principal eyes (reviewed in [2]; Figure 1A). The ALEs, with immobile lenses and retinas, wide fields of view, and hyperacute sensitivity to moving stimuli [4], are structurally distinct from the principal eyes, which have the best spatial acuity known for terrestrial invertebrates and can discern fine details of stationary objects [5]. Behind the immobile corneal lenses of the principal eyes are miniature, boomerang-shaped retinas with correspondingly small fields of view (Figure 1B). The principal-eye visual fields are greatly expanded and overlap because of eye movements: these retinas are at the proximal ends of long, moveable tubes within the spider's cephalothorax [6]. By designing and using a specialized eyetracker, we tested whether principal-eye gaze direction is influenced by what the ALEs see. The principal eyes scanned stationary objects regardless of whether the ALEs were masked, but only when the ALEs were unmasked did the principal eyes smoothly track moving disks. The principal eyes, with high acuity but a narrow field of view, can thus precisely target moving stimuli, but only with the guidance of the secondary eyes.

A novel protocol for generating intact, whole-head spider cephalothorax tissue sections.

The diversity of spider behavior and sensory systems provides an excellent opportunity for comparative studies of the relationship between the brain and behavior. However, the morphology of spiders poses a challenge for histologists since the spider cephalothorax contains heterogeneous tissues and has both tough external and internal sclerotized regions. Unlike the heads of insects, the cephalothorax is highly pressurized, which can cause tissues to shift during processing and can reduce tissue cohesion in thick sections. This work describes a novel protocol for producing thick whole-head sections for morphological study by softening the exoskeleton and stabilizing friable tissue, without freezing or dehydration. It also presents an effective whole-head DiI staining method that uses minimal dehydration and highlights neural structures.

Secondary eyes mediate the response to looming objects in jumping spiders (Phidippus audax, Salticidae).

Some species have sensory systems divided into subsystems with morphologically different sense organs that acquire different types of information within the same modality. Jumping spiders (family Salticidae) have eight eyes. Four eyes are directed anteriorly to view objects in front of the spider: a pair of principal eyes track targets with their movable retinae, while the immobile anterior lateral (AL) eyes have a larger field of view and lower resolution. To test whether the principal eyes, the AL eyes, or both together mediate the response to looming stimuli, we presented spiders with a video of a solid black circle that rapidly expanded (loomed) or contracted (receded). Control spiders and spiders with their principal eyes masked were significantly more likely to back away from the looming stimulus than were spiders with their AL eyes masked. Almost no individuals backed away from the receding stimulus. Our results show that the AL eyes alone mediate the loom response to objects anterior to the spider.