The Evolution of Simplifying Heuristics in Visual Cognition: Categorization, Specialization, and Visual Illusions.

Animals live in visually complex environments. As a result, visual systems have evolved mechanisms that simplify visual processing and allow animals to focus on the information that is most relevant to adaptive decision making. This review explores two key mechanisms that animals use to efficiently process visual information: categorization and specialization. Categorization occurs when an animal's perceptual system sorts continuously varying stimuli into a set of discrete categories. Specialization occurs when particular classes of stimuli are processed using distinct cognitive operations that are not used for other classes of stimuli. We also describe a nonadaptive consequence of simplifying heuristics: visual illusions, where visual perception consistently misleads the viewer about the state of the external world or objects within it. We take an explicitly comparative approach by exploring similarities and differences in visual cognition across human and nonhuman taxa. Considering areas of convergence and divergence across taxa provides insight into the evolution and function of visual systems and associated perceptual strategies.

Secondary not subordinate: Opsin localization suggests possibility for color sensitivity in salticid secondary eyes.

The principal eyes of jumping spiders (Salticidae) integrate a dual-lens system, a tiered retinal matrix with multiple photoreceptor classes and muscular control of retinal movements to form high resolution images, extract color information, and dynamically evaluate visual scenes. While much work has been done to characterize these more complex principal anterior eyes, little work has investigated the three other pairs of simpler secondary eyes: the anterior lateral eye pair and two posterior (lateral and median) pairs of eyes. We investigated the opsin protein component of visual pigments in the eyes of three species of salticid using transcriptomics and immunohistochemistry. Based on characterization and localization of a set of three conserved opsins (Rh1 - green sensitive, Rh2 - blue sensitive, and Rh3 - ultraviolet sensitive) we have identified potential photoreceptors for blue light detection in the eyes of two out of three species: Menemerus bivittatus (Chrysillini) and Habrocestum africanum (Hasarinii). Additionally, the photoreceptor diversity of the secondary eyes exhibits more variation than previous estimates, particularly for the small, posterior median eyes previously considered vestigial in some species. In all three species investigated the lateral eyes were dominated by green-sensitive visual pigments (RH1 opsins), while the posterior median retinas were dominated by opsins forming short-wavelength sensitive visual pigments (e.g. RH2 and/or RH3/RH4). There was also variation among secondary eye types and among species in the distribution of opsins in retinal photoreceptors, particularly for the putatively blue-sensitive visual pigment formed from RH2. Our findings suggest secondary eyes have the potential for color vision, with observed differences between species likely associated with different ecologies and visual tasks.

Nutrition-induced macular-degeneration-like photoreceptor damage in jumping spider eyes.

Age-related macular degeneration (AMD) is a leading cause of vision loss in humans. Despite its prevalence and medical significance, many aspects of AMD remain elusive and treatment options are limited. Here, we present data that suggest jumping spiders offer a unique opportunity for understanding the fundamentals underlying retinal degeneration, thereby shedding light on a process that impacts millions of people globally. Using a micro-ophthalmoscope and histological evidence, we demonstrate that significant photoreceptor damage can occur during development in the image-forming anterior lateral eyes of the jumping spider Phidippus audax. Furthermore, we find that this photoreceptor degeneration is exacerbated by inadequate nutrition and is most prevalent in the high-density region of the retina, like AMD in humans. This suggests that similar to those in vertebrates, the retinas in P. audax are challenged to meet high-energy cellular demands.

Spectral sensitivities of the orchid bee Euglossa dilemma.

Diurnal pollinators often rely on color cues to make decisions when visiting flowers. Orchid bees are major tropical pollinators, with most studies of their pollination behavior to date focusing on scent collection and chemical ecology. The objective of this study was to measure their spectral sensitivities to preliminarily characterize color vision in the orchid bee Euglossa dilemma and compare it to the known spectral sensitivity of other closely related bees. We compared E. dilemma's spectral sensitivities and opsin protein sequences to four closely related corbiculate bees. E. dilemma appears to have trichromatic vision, with spectral sensitivity peaks in the ultraviolet, blue, and green wavelengths (347 ± 0.957 (SE) nm, 429 ± 6.570 nm, and 537 ± 1.183 nm, respectively), similar to other measured bees. We found no differences between male and female E. dilemma visual systems despite neuroanatomical and behavioral differences reported in the literature. The lambda maxes of the ultraviolet-sensitive photoreceptors appeared to be the most conserved among the bees we compared. Meanwhile, both the lambda maxes of the blue photoreceptors and the blue opsin proteins sequences were the least conserved. Our results open up new possibilities for the study of color vision and color-mediated pollination behaviors in orchid bees.

The jumping spider Saitis barbipes lacks a red photoreceptor to see its own sexually dimorphic red coloration.

Examining the role of color in mate choice without testing what colors the study animal is capable of seeing can lead to ill-posed hypotheses and erroneous conclusions. Here, we test the seemingly reasonable assumption that the sexually dimorphic red coloration of the male jumping spider Saitis barbipes is distinguishable, by females, from adjacent black color patches. Using microspectrophotometry, we find clear evidence for photoreceptor classes with maximal sensitivity in the UV (359 nm) and green (526 nm), inconclusive evidence for a photoreceptor maximally sensitive in the blue (451 nm), and no evidence for a red photoreceptor. No colored filters within the lens or retina could be found to shift green sensitivity to red. To quantify and visualize whether females may nevertheless be capable of discriminating red from black color patches, we take multispectral images of males and calculate photoreceptor excitations and color contrasts between color patches. Red patches would be, at best, barely discriminable from black, and not discriminable from a low-luminance green. Some color patches that appear achromatic to human eyes, such as beige and white, strongly absorb UV wavelengths and would appear as brighter "spider-greens" to S. barbipes than the red color patches. Unexpectedly, we discover an iridescent UV patch that contrasts strongly with the UV-absorbing surfaces dominating the rest of the spider. We propose that red and black coloration may serve identical purposes in sexual signaling, functioning to generate strong achromatic contrast with the visual background. The potential functional significance of red coloration outside of sexual signaling is discussed.

Spatio-temporal Dynamics in Animal Communication: A Special Issue Arising from a Unique Workshop-Symposium Model.

Investigating how animals navigate space and time is key to understanding communication. Small differences in spatial positioning or timing can mean the difference between a message received and a missed connection. However, these spatio-temporal dynamics are often overlooked or are subject to simplifying assumptions in investigations of animal signaling. This special issue addresses this significant knowledge gap by integrating work from researchers with disciplinary backgrounds in neuroscience, cognitive ecology, sensory ecology, computer science, evolutionary biology, animal behavior, and philosophy. This introduction to the special issue outlines the novel questions and approaches that will advance our understanding of spatio-temporal dynamics of animal communication. We highlight papers that consider the evolution of spatio-temporal dynamics of behavior across sensory modalities and social contexts. We summarize contributions that address the neural and physiological mechanisms in senders and receivers that shape communication. We then turn to papers that introduce cutting edge technologies that will revolutionize our ability to track spatio-temporal dynamics of individuals during social encounters. The interdisciplinary collaborations that gave rise to these papers emerged in part from a novel workshop-symposium model, which we briefly summarize for those interested in fostering syntheses across disciplines.

Beyond Cognitive Templates: Re-Examining Template Metaphors Used for Animal Recognition and Navigation.

The term "cognitive template" originated from work in human-based cognitive science to describe a literal, stored, neural representation used in recognition tasks. As the study of cognition has expanded to nonhuman animals, the term has diffused to describe a wider range of animal cognitive tools and strategies that guide action through the recognition of and discrimination between external states. One potential reason for this nonstandardized meaning and variable employment is that researchers interested in the broad range of animal recognition tasks enjoy the simplicity of the cognitive template concept and have allowed it to become shorthand for many dissimilar or unknown neural processes without deep scrutiny of how this metaphor might comport with underlying neurophysiology. We review the functional evidence for cognitive templates in fields such as perception, navigation, communication, and learning, highlighting any neural correlates identified by these studies. We find that the concept of cognitive templates has facilitated valuable exploration at the interface between animal behavior and cognition, but the quest for a literal template has failed to attain mechanistic support at the level of neurophysiology. This may be the result of a misled search for a single physical locus for the "template" itself. We argue that recognition and discrimination processes are best treated as emergent and, as such, may not be physically localized within single structures of the brain. Rather, current evidence suggests that such tasks are accomplished through synergies between multiple distributed processes in animal nervous systems. We thus advocate for researchers to move toward a more ecological, process-oriented conception, especially when discussing the neural underpinnings of recognition-based cognitive tasks.

How Signaling Geometry Shapes the Efficacy and Evolution of Animal Communication Systems.

Animal communication is inherently spatial. Both signal transmission and signal reception have spatial biases-involving direction, distance, and position-that interact to determine signaling efficacy. Signals, be they visual, acoustic, or chemical, are often highly directional. Likewise, receivers may only be able to detect signals if they arrive from certain directions. Alignment between these directional biases is therefore critical for effective communication, with even slight misalignments disrupting perception of signaled information. In addition, signals often degrade as they travel from signaler to receiver, and environmental conditions that impact transmission can vary over even small spatiotemporal scales. Thus, how animals position themselves during communication is likely to be under strong selection. Despite this, our knowledge regarding the spatial arrangements of signalers and receivers during communication remains surprisingly coarse for most systems. We know even less about how signaler and receiver behaviors contribute to effective signaling alignment over time, or how signals themselves may have evolved to influence and/or respond to these aspects of animal communication. Here, we first describe why researchers should adopt a more explicitly geometric view of animal signaling, including issues of location, direction, and distance. We then describe how environmental and social influences introduce further complexities to the geometry of signaling. We discuss how multimodality offers new challenges and opportunities for signalers and receivers. We conclude with recommendations and future directions made visible by attention to the geometry of signaling.

Floral Color Properties of Serpentine Seep Assemblages Depend on Community Size and Species Richness.

Functional traits, particularly those that impact fitness, can shape the ecological and evolutionary relationships among coexisting species of the same trophic level. Thus, examining these traits and properties of their distributions (underdispersion, overdispersion) within communities can provide insights into key ecological interactions (e.g., competition, facilitation) involved in community assembly. For instance, the distribution of floral colors in a community may reflect pollinator-mediated interactions between sympatric plant species, and the phylogenetic distribution of color can inform how evolutionary contingencies can continue to shape extant community assemblages. Additionally, the abundance and species richness of the local habitat may influence the type or strength of ecological interactions among co-occurring species. To evaluate the impact of community size and species richness on mechanisms shaping the distribution of ecologically relevant traits, we examined how floral color (defined by pollinator color vision models) is distributed within co-flowering assemblages. We modeled floral reflectance spectra of 55 co-flowering species using honeybee (Apis mellifera) and syrphid fly (Eristalis tenax) visual systems to assess the distributions of flower color across 14 serpentine seep communities in California. We found that phylogenetic relatedness had little impact on the observed color assemblages. However, smaller seep communities with lower species richness were more overdispersed for flower color than larger, more species-rich communities. Results support that competitive exclusion could be a dominant process shaping the species richness of flower color in smaller-sized communities with lower species richness, but this is less detectable or overwhelmed by other processes at larger, more speciose communities.

Characterization of Female Reproductive Proteases in a Butterfly from Functional and Evolutionary Perspectives.

Molecules that mediate reproductive interactions are some of the most rapidly evolving traits. Researchers have often suggested that this is due to coevolution at key physiological interfaces. However, very few of these interfaces are well understood at the functional level. One such interface is the digestion of the spermatophore in Lepidoptera. Female Lepidoptera have a specialized reproductive organ called the bursa copulatrix that receives and processes the male spermatophore, a complex proteinaceous ejaculate. In the cabbage white butterfly, Pieris rapae, the bursa secretes a mixture of proteases hypothesized to digest the spermatophore. However, these proteases remain biochemically uncharacterized. Using a zymogram approach, we identified six proteases in bursal extracts at sufficiently high concentrations to characterize their in vitro activity. We assessed the modes of action of these bursal enzymes by quantifying their activity following exposure to diagnostic protease inhibitors. A serine protease-specific inhibitor failed to reduce bursal protease digestion of casein. However, a cysteine protease-specific inhibitor did decrease the activity of some proteases. To explore the possible molecular mechanisms responsible for these responses, we created protease homology models. The models mirrored the results of our in vitro experiments, indicating that protease homology models may offer insight into underlying functional mechanisms. Whether the observed bursal protease resistance to known inhibitors is important in the context of spermatophore digestion remains to be tested. However, our results suggest the exciting possibility that bursal protease specificity may have evolved in response to interactions with various proteins and inhibitors present within the female tract during the reproductive process.

Growing tiny eyes: How juvenile jumping spiders retain high visual performance in the face of size limitations and developmental constraints.

Adult jumping spiders are known for their extraordinary eyesight and complex, visually guided behaviors, including elaborate communicatory displays, navigational abilities, and prey-specific predatory strategies. Juvenile spiders also exhibit many of these behaviors, yet their visual systems are many times smaller. How do juveniles retain high visually guided performance despite severe size constraints on their visual systems? We investigated developmental changes in eye morphology and visual function in the jumping spider Phidippus audax using morphology, histology, ophthalmoscopy, and optical measurements. We find that juvenile spiders have proportionally larger lenses in relation to their body size than adults. This should alleviate some of the costs of small body size on visual function. However, photoreceptor number in the anterior lateral eyes (ALE) remains constant from early development onward, consistent with a developmental constraint on photoreceptor differentiation. To accommodate these photoreceptors within the diminutive volume of the spiderling cephalothorax, ALE rhabdoms in early life stages are more tightly packed and significantly smaller in diameter and length, properties that expand across development. Lens focal lengths increase as eyes and retinas grow, resulting in a remarkable maintenance of ALE spatial acuity and field-of-view across life stages. However, this maintenance of acuity comes at a sensitivity cost given the small rhabdomal volumes required by space constraints early in life. Taken together, our results indicate that young jumping spiders have eyes already equipped for high acuity vision, but these young spiders may struggle to perform visually demanding behaviors in low-light environments, a notion that warrants further testing.

The molecular genetic basis of herbivory between butterflies and their host plants.

Interactions between herbivorous insects and their host plants are a central component of terrestrial food webs and a critical topic in agriculture, where a substantial fraction of potential crop yield is lost annually to pests. Important insights into plant-insect interactions have come from research on specific plant defences and insect detoxification mechanisms. Yet, much remains unknown about the molecular mechanisms that mediate plant-insect interactions. Here we use multiple genome-wide approaches to map the molecular basis of herbivory from both plant and insect perspectives, focusing on butterflies and their larval host plants. Parallel genome-wide association studies in the cabbage white butterfly, Pieris rapae, and its host plant, Arabidopsis thaliana, pinpointed a small number of butterfly and plant genes that influenced herbivory. These genes, along with much of the genome, were regulated in a dynamic way over the time course of the feeding interaction. Comparative analyses, including diverse butterfly/plant systems, showed a variety of genome-wide responses to herbivory, as well as a core set of highly conserved genes in butterflies as well as their host plants. These results greatly expand our understanding of the genomic causes and evolutionary consequences of ecological interactions across two of nature's most diverse taxa, butterflies and flowering plants.

Rapid Divergence of Wing Volatile Profiles Between Subspecies of the Butterfly Pieris rapae (Lepidoptera: Pieridae).

Complex signaling traits such as pheromone profiles can play an important role in the early stages of reproductive isolation between populations. These signals can diverge along multiple trait axes, and signal receivers are often sensitive to subtle differences in signal properties. In the Lepidoptera, prior research has highlighted that natural selection can drive rapid chemical signal divergence, for instance via mate recognition to maintain species boundaries. Much less is known about the occurrence of such changes for predominantly sexually selected chemical signals, such as those released by many male lepidopterans. We evaluated the divergence in male and female wing volatile profiles between two recently isolated subspecies of the pierid butterfly Pieris rapae Linnaeus (Lepidoptera: Pieridae): P. rapae rapae and P. rapae crucivora. In laboratory settings, these subspecies exhibit strong premating isolation, with females rejecting males of the opposite subspecies despite the fact that males direct equivalent courtship effort toward females of either subspecies. Using gas chromatography-mass spectrometry, we analyzed the volatile chemical profiles of individual males and females of each subspecies. We find that males of each subspecies differ in their wing volatile profiles, including quantitative differences in a male sex pheromone, ferrulactone. In contrast, female wing volatiles profiles have diverged significantly less. These sex-specific patterns suggest that male chemical profiles may play a role in the observed premating isolation between these two subspecies, providing support for future investigations of sexually selected chemical traits in population divergence.

Molecular Evolution of Spider Vision: New Opportunities, Familiar Players.

Spiders are among the world's most species-rich animal lineages, and their visual systems are likewise highly diverse. These modular visual systems, composed of four pairs of image-forming "camera" eyes, have taken on a huge variety of forms, exhibiting variation in eye size, eye placement, image resolution, and field of view, as well as sensitivity to color, polarization, light levels, and motion cues. However, despite this conspicuous diversity, our understanding of the genetic underpinnings of these visual systems remains shallow. Here, we review the current literature, analyze publicly available transcriptomic data, and discuss hypotheses about the origins and development of spider eyes. Our efforts highlight that there are many new things to discover from spider eyes, and yet these opportunities are set against a backdrop of deep homology with other arthropod lineages. For example, many (but not all) of the genes that appear important for early eye development in spiders are familiar players known from the developmental networks of other model systems (e.g., Drosophila). Similarly, our analyses of opsins and related phototransduction genes suggest that spider photoreceptors employ many of the same genes and molecular mechanisms known from other arthropods, with a hypothesized ancestral spider set of four visual and four nonvisual opsins. This deep homology provides a number of useful footholds into new work on spider vision and the molecular basis of its extant variety. We therefore discuss what some of these first steps might be in the hopes of convincing others to join us in studying the vision of these fascinating creatures.

Structural complexity and molecular heterogeneity of a butterfly ejaculate reflect a complex history of selection.

Male ejaculates are often structurally complex, and this complexity is likely to influence key reproductive interactions between males and females. However, despite its potential evolutionary significance, the molecular underpinnings of ejaculate structural complexity have received little empirical attention. To address this knowledge gap, we sought to understand the biochemical and functional properties of the structurally complex ejaculates of Pieris rapae butterflies. Males in this species produce large ejaculates called spermatophores composed of an outer envelope, an inner matrix, and a bolus of sperm. Females are thought to benefit from the nutrition contained in the soluble inner matrix through increases in longevity and fecundity. However, the indigestible outer envelope of the spermatophore delays female remating, allowing males to monopolize paternity for longer. Here, we show that these two nonsperm-containing spermatophore regions, the inner matrix and the outer envelope, differ in their protein composition and functional properties. We also reveal how these divergent protein mixtures are separately stored in the male reproductive tract and sequentially transferred to the female reproductive tract during spermatophore assembly. Intriguingly, we discovered large quantities of female-derived proteases in both spermatophore regions shortly after mating, which may contribute to spermatophore digestion and hence, female control over remating rate. Finally, we report evidence of past selection on these spermatophore proteins and female proteases, indicating a complex evolutionary history. Our findings illustrate how structural complexity of ejaculates may allow functionally and/or spatially associated suites of proteins to respond rapidly to divergent selective pressures, such as sexual conflict or reproductive cooperation.

Life-history evolution in the anthropocene: effects of increasing nutrients on traits and trade-offs.

Variation in life-history traits can have major impacts on the ecological and evolutionary responses of populations to environmental change. Life-history variation often results from trade-offs that arise because individuals have a limited pool of resources to allocate among traits. However, human activities are increasing the availability of many once-limited resources, such as nitrogen and phosphorus, with potentially major implications for the expression and evolution of life-history trade-offs. In this review, we synthesize contemporary life history and sexual selection literature with current research on ecosystem nutrient cycling to highlight novel opportunities presented by anthropogenic environmental change for investigating life-history trait development and evolution. Specifically, we review four areas where nutrition plays a pivotal role in life-history evolution and explore possible implications in the face of rapid, human-induced change in nutrient availability. For example, increases in the availability of nutrients may relax historical life-history trade-offs and reduce the honesty of signaling systems. We argue that ecosystems experiencing anthropogenic nutrient inputs present a powerful yet underexplored arena for testing novel and longstanding questions in organismal life-history evolution.

Dynamic digestive physiology of a female reproductive organ in a polyandrous butterfly.

Reproductive traits experience high levels of selection because of their direct ties to fitness, often resulting in rapid adaptive evolution. Much of the work in this area has focused on male reproductive traits. However, a more comprehensive understanding of female reproductive adaptations and their relationship to male characters is crucial to uncover the relative roles of sexual cooperation and conflict in driving co-evolutionary dynamics between the sexes. We focus on the physiology of a complex female reproductive adaptation in butterflies and moths: a stomach-like organ in the female reproductive tract called the bursa copulatrix that digests the male ejaculate (spermatophore). Little is known about how the bursa digests the spermatophore. We characterized bursa proteolytic capacity in relation to female state in the polyandrous butterfly Pieris rapae. We found that the virgin bursa exhibits extremely high levels of proteolytic activity. Furthermore, in virgin females, bursal proteolytic capacity increases with time since eclosion and ambient temperature, but is not sensitive to the pre-mating social environment. Post copulation, bursal proteolytic activity decreases rapidly before rebounding toward the end of a mating cycle, suggesting active female regulation of proteolysis and/or potential quenching of proteolysis by male ejaculate constituents. Using transcriptomic and proteomic approaches, we report identities for nine proteases actively transcribed by bursal tissue and/or expressed in the bursal lumen that may contribute to observed bursal proteolysis. We discuss how these dynamic physiological characteristics may function as female adaptations resulting from sexual conflict over female remating rate in this polyandrous butterfly.

Digestive organ in the female reproductive tract borrows genes from multiple organ systems to adopt critical functions.

Persistent adaptive challenges are often met with the evolution of novel physiological traits. Although there are specific examples of single genes providing new physiological functions, studies on the origin of complex organ functions are lacking. One such derived set of complex functions is found in the Lepidopteran bursa copulatrix, an organ within the female reproductive tract that digests nutrients from the male ejaculate or spermatophore. Here, we characterized bursa physiology and the evolutionary mechanisms by which it was equipped with digestive and absorptive functionality. By studying the transcriptome of the bursa and eight other tissues, we revealed a suite of highly expressed and secreted gene products providing the bursa with a combination of stomach-like traits for mechanical and enzymatic digestion of the male spermatophore. By subsequently placing these bursa genes in an evolutionary framework, we found that the vast majority of their novel digestive functions were co-opted by borrowing genes that continue to be expressed in nonreproductive tissues. However, a number of bursa-specific genes have also arisen, some of which represent unique gene families restricted to Lepidoptera and may provide novel bursa-specific functions. This pattern of promiscuous gene borrowing and relatively infrequent evolution of tissue-specific duplicates stands in contrast to studies of the evolution of novelty via single gene co-option. Our results suggest that the evolution of complex organ-level phenotypes may often be enabled (and subsequently constrained) by changes in tissue specificity that allow expression of existing genes in novel contexts, such as reproduction. The extent to which the selective pressures encountered in these novel roles require resolution via duplication and sub/neofunctionalization is likely to be determined by the need for specialized reproductive functionality. Thus, complex physiological phenotypes such as that found in the bursa offer important opportunities for understanding the relative role of pleiotropy and specialization in adaptive evolution.