Showing papers by "John A. Endler published in 2018"

25 Years of sensory drive: the evidence and its watery bias.

Abstract: It has been 25 years since the formalization of the Sensory Drive hypothesis was published in the American Naturalist (1992). Since then, there has been an explosion of research identifying its utility in contributing to our understanding of inter- and intra-specific variation in sensory systems and signaling properties. The main tenet of Sensory Drive is that environmental characteristics will influence the evolutionary trajectory of both sensory (detecting capabilities) and signaling (detectable features and behaviors) traits in predictable directions. We review the accumulating evidence in 154 studies addressing these questions and categorized their approach in terms of testing for environmental influence on sensory tuning, signal characteristics, or both. For the subset of studies that examined sensory tuning, there was greater support for Sensory Drive processes shaping visual than auditory tuning, and it was more prevalent in aquatic than terrestrial habitats. Terrestrial habitats and visual traits were the prevalent habitat and sensory modality in the 104 studies showing support for environmental influence on signaling properties. An additional 19 studies that found no supporting evidence for environmental influence on signaling traits were all based in terrestrial ecosystems and almost exclusively involved auditory signals. Only 29 studies examined the complete coevolutionary process between sensory and signaling traits and were dominated by fish visual communication. We discuss biophysical factors that may contribute to the visual and aquatic bias for Sensory Drive evidence, as well as biotic factors that may contribute to the lack of Sensory Drive processes in terrestrial acoustic signaling systems.

Boundary strength analysis: Combining colour pattern geometry and coloured patch visual properties for use in predicting behaviour and fitness

Abstract: Author(s): Endler, John; Cole, Gemma; Kranz, Alexandrea | Abstract: Abstract Colour patterns are used by many species to make decisions that ultimately affect their Darwinian fitness. Colour patterns consist of a mosaic of patches that differ in geometry and visual properties. Although traditionally pattern geometry and colour patch visual properties are analysed separately, these components are likely to work together as a functional unit. Despite this, the combined effect of patch visual properties, patch geometry, and the effects of the patch boundaries on animal visual systems, behaviour and fitness are relatively unexplored. Here we describe Boundary Strength Analysis (BSA), a novel way to combine the geometry of the edges (boundaries among the patch classes) with the receptor noise estimate ( ΔS ) of the intensity of the edges. The method is based upon known properties of vertebrate and invertebrate retinas. The mean and SD of ΔS (m ΔS , s ΔS ) of a colour pattern can be obtained by weighting each edge class ΔS by its length, separately for chromatic and achromatic ΔS . This assumes those colour patterns, or parts of the patterns used in signalling, with larger m ΔS and s ΔS are more stimulating and hence more salient to the viewers. BSA can be used to examine both colour patterns and visual backgrounds. BSA was successful in assessing the estimated conspicuousness of colour pattern variants in two species, guppies ( Poecilia reticulata ) and Gouldian finches ( Erythrura gouldiae ), both polymorphic for patch colour, luminance and geometry. The pattern difference between chromatic and achromatic edges in both species reveals the possibility that chromatic and achromatic edges could function differently. BSA can be applied to any colour pattern used in intraspecific and interspecific behaviour. Seven predictions and four questions about colour patterns are presented.

Toxicity and taste: unequal chemical defences in a mimicry ring.

Abstract: Mimicry of warning signals is common, and can be mutualistic when mimetic species harbour equal levels of defence (Mullerian), or parasitic when mimics are undefended but still gain protection from their resemblance to the model (Batesian). However, whether chemically defended mimics should be similar in terms of toxicity (i.e. causing damage to the consumer) and/or unpalatability (i.e. distasteful to consumer) is unclear and in many studies remains undifferentiated. In this study, we investigated the evolution of visual signals and chemical defences in a putative mimicry ring of nudibranch molluscs. First, we demonstrated that the appearance of a group of red spotted nudibranchs molluscs was similar from the perspective of potential fish predators using visual modelling and pattern analysis. Second, using phylogenetic reconstruction, we demonstrated that this colour pattern has evolved multiple times in distantly related individuals. Third, we showed that these nudibranchs contained different chemical profiles used for defensive purposes. Finally, we demonstrated that although levels of distastefulness towards Palaemon shrimp remained relatively constant between species, toxicity levels towards brine shrimp varied significantly. We highlight the need to disentangle toxicity and taste when considering chemical defences in aposematic and mimetic species, and discuss the implications for aposematic and mimicry signal evolution.

Temperature-induced colour change varies seasonally in bearded dragon lizards

Abstract: The benefits of colour change are expected to vary seasonally because of changes in reproductive activity, temperature and, potentially, predation risk; yet temporal variation in colour change has seldom been examined. We measured colour change in spring and autumn using captive individuals from two differently coloured populations of the central bearded dragon lizard, Pogona vitticeps. We predicted that colour change should be greater in spring than autumn because of the added requirements of reproductive and territorial activity. To elicit colour change in a standardized way, we placed lizards inside temperature-controlled chambers and measured colour at 15, 25, 35 and 40 °C, repeating experiments in spring and autumn. Lizards from both populations changed from dark grey to light yellowish or orange-brown (increasing luminance and saturation) with increasing temperature in both seasons, and both populations changed colour to a similar extent. As predicted, the maximal extent of temperature-induced colour change (in particular, luminance change) was greater in spring than autumn. Our results confirm that temperatureinduced colour change is greater in the peak activity season, probably an adaptation to the greater thermal and/or signalling needs of that time of year.

Light environment change induces differential expression of guppy opsins in a multi-generational evolution experiment.

Abstract: Light environments critically impact species that rely on vision to survive and reproduce. Animal visual systems must accommodate changes in light that occur from minutes to years, yet the mechanistic basis of their response to spectral (color) changes is largely unknown. Here, we used a laboratory experiment where replicate guppy populations were kept under three different light environments for up to 8-12 generations to explore possible differences in the expression levels of nine guppy opsin genes. Previous evidence for opsin expression-light environment "tuning" has been either correlative or focused exclusively on the relationship between the light environment and opsin expression over one or two generations. In our multigeneration experiment, the relative expression levels of nine different guppy opsin genes responded differently to light environment changes: some did not respond, while others differed due to phenotypic plasticity. Moreover, for the LWS-1 opsin we found that, while we observed a wide range of plastic responses under different light conditions, common plastic responses (where the population replicates all followed the same trajectory) occurred only after multigenerational exposure to different light environments. Taken together this suggests that opsin expression plasticity plays an important role in light environment "tuning" in different light environments on different time scales, and, in turn, has important implications for both visual system function and evolution.

Boundary Strength Analysis: Combining colour pattern geometry and coloured patch visual properties for use in predicting behaviour and fitness

Abstract: Colour patterns are used by many species to make decisions that ultimately affect their Darwinian fitness. Colour patterns consist of a mosaic of patches that differ in geometry and visual properties. Although traditionally pattern geometry and colour patch visual properties are analysed separately, these components are likely to work together as a functional unit. Despite this, the combined effect of patch visual properties, patch geometry, and the effects of the patch boundaries on animal visual systems, behaviour and fitness are relatively unexplored. Here we describe Boundary Strength Analysis (BSA), a novel way to combine the geometry of the edges (boundaries among the patch classes) with the receptor noise estimate (ΔS) of the intensity of the edges. The method is based upon known properties of vertebrate and invertebrate retinas. The mean and SD of ΔS of a colour pattern can be obtained by weighting each edge class ΔS by its length, separately for chromatic and achromatic ΔS. This assumes those colour patterns, or parts of the patterns used in signalling, with larger ΔS are more stimulating and hence more salient to the viewers. BSA can be used to examine both colour patterns and visual backgrounds. Examples of the kinds of analysis and insights that BSA are given using guppies and Gouldian finches. The pattern difference between chromatic and achromatic edges in both species reveals the possibility that chromatic and achromatic edges could function differently. In species which are convex rather than flat, both chromatic and luminance contrasts change with viewing angle; geometry of signalling is as important as signal geometry.

Individuals Among the Pots: How Do Traditional Ceramic Shapes Vary Between Potters?

Abstract: At the crossroad of archeology and experimental psychology, we addressed the issue of interindividual variability in traditional ceramic shapes. The goal was to explore whether such variability cou...

A perspective on sensory drive.

Abstract: In 1992, The American Naturalist published a special supplement entitled: “Sensory Drive. Does Sensory Drive Biology Bias or Constrain the Direction of Evolution?” organized by John Endler. The supplement contained a seminal paper on “sensory drive” by Endler (1992a) as well as several other well-cited papers on sensory exploitation (Ryan and Keddy-Hector 1992), background matching with respect to motion (Fleishman 1992), chemical cues in mammals and amphibians (Alberts 1992; Roth et al. 1992), and the relationship between auditory processing and call properties in frogs (Narins 1992). The paper by Endler was especially important; it has been cited over 1,200 times and has inspired research at many levels of ecology and evolution across diverse taxa and sensory modalities. In this paper and associated ones, Endler laid out the primary components that influence the evolution of signaling systems, placing a large emphasis on the environmental conditions under which signaling occurs (Endler 1992a, 1992b, 1993). Twenty-five years later, the American Society of Naturalists held a symposium on “25 Years of Sensory Drive” at the 2017 Evolution meetings in Portland, Oregon, organized by Becky Fuller. This special column in Current Zoology summarizes the work presented there as well as other contributions made for the column. In this editorial, we first review sensory drive and the state of the field when it emerged. We then summarize the work in this special column and suggest fruitful ways forward. Figure 1 shows the sensory drive framework. In order for signaling to occur between a signaler and a receiver the following must happen: The signaler gives off signal(s) using one or more signal modalities, and those signals have particular properties (e.g., reflectance, pitch, degree of polarization, chemical structure, etc.). The signals are given off in particular times and places. In order for the signal to be successful, the signal must travel through the environmental conditions under which signaling takes place and be detected by the receiver against a background of other potential stimuli. The signal is then detected (or not) by the sensory system of the receiver and processed by the brain, which influences the perception of the signals and the resulting behavior (i.e., decision criteria). Of course, there are other things can influence the evolution of the signaler and the receiver, which are indicated in Figure 1. The receiver must do many things with its sensory systems other than merely detect signals used in communication. It must also find food, avoid predators, and find proper habitat, all of which can exert natural selection on sensory system properties. In Figure 1, this is exemplified by “Detectability of food” and foraging success (fs). In addition, the act of signaling may make signalers more conspicuous to predators and other actors that would exploit signals. The environmental conditions under which signaling takes place can affect the roles of predators and eavesdroppers just as it can with signalers and intended receivers. Open in a separate window Figure 1 Diagram of the main processes in sensory drive, modified and revised from Endler (1992). Solid arrows indicate evolutionary processes. Dashed arrows with upper case symbols indicate immediate or functional effects: Eo: immediate effects of ecological and optical conditions on signalling conditions. V: immediate effect of microenvironment on the visibility of prey. P: immediate effect of microenvironment on visibility to predators, and also natural selection caused by microenvironmental conditions acting on predator senses and behaviour. Lower Case Symbols: Fs: feeding success that directly affects the evolution of the senses. Ms: mating success that affects sensory evolution directly. Ss: sexual selection (Good Genes, Fisher Process, etc.) That influences mate-choice criteria evolution directly. The asterisks identify the three components of sensory exploitation, a well-studied subset of sensory drive.

Colour pattern component phenotypic divergence can be predicted by the light environment.

Abstract: The sensory drive hypothesis predicts that across different light environments sexually selected colour patterns will change to increase an animal's visual communication efficiency within different habitats. This is because individuals with more efficient signal components are likely to have more successful matings and hence produce more offspring. However, how colour pattern signals change over multiple generations under different light environmental conditions has not been tested experimentally. Here, we manipulated colour pattern signal efficiency by providing different ambient light environments over multiple generations to examine whether male colour pattern components change within large replicated populations of guppies (Poecilia reticulata). We report that colour patches change within populations over time and are phenotypically different among our three different light environments. Visual modelling suggests that the majority of these changes can be understood by considering the chroma, hue and luminance of each colour patch as seen by female guppies under each light environment. Taken together, our results support the hypothesis that different environmental conditions during signal reception can directly or indirectly drive the phenotypic diversification of visual signals within species.

pavo 2.0: new tools for the spectral and spatial analysis of colour in R

Abstract: Biological colouration presents a canvas for the study of ecological and evolutionary processes. Enduring interest in colour-based phenotypes has driven, and been driven by, improved techniques for quantifying colour patterns in ever-more relevant ways, yet the need for flexible, open frameworks for data processing and analysis persists. Here we introduce pavo 2.0, the latest iteration of the R package pavo. This release represents the extensive refinement and expansion of existing methods, as well as a suite of new tools for the cohesive analysis of the spectral and (now) spatial structure of colour patterns and perception. At its core, the package retains a broad focus on (a) the organisation and processing of spectral and spatial data, and tools for the alternating (b) visualisation, and (c) analysis of data. Significantly, pavo 2.0 introduces image-analysis capabilities, providing a cohesive workflow for the comprehensive analysis of colour patterns. We demonstrate the utility of pavo with a brief example centred on mimicry in Heliconius butterflies. Drawing on visual modelling, adjacency, and boundary strength analyses, we show that the combined spectral (colour and luminance) and spatial (pattern element distribution and boundary salience) features of putative models and mimics are closely aligned. pavo 2.0 offers a flexible and reproducible environment for the analysis of colour, with renewed potential to assist researchers in answering fundamental questions in sensory ecology and evolution.

Change in male coloration associated with artificial selection on foraging colour preference.

Abstract: Sensory drive proposes that natural selection on nonmating behaviours (e.g. foraging preferences) alters sensory system properties and results in a correlated effect on mating preferences and subsequently sexual traits. In colour-based systems, we can test this by selecting on nonmating colour preferences and testing for responses in colour-based female preferences and male sexual coloration. In guppies (Poecilia reticulata), individual functional links of sensory drive have been demonstrated providing an opportunity to test the process over more than one link. We measured male coloration and female preferences in populations previously artificially selected for colour-based foraging behaviour towards two colours, red and blue. We found associated changes in male coloration in the expected direction as well as weak changes in female preferences. Our results can be explained by a correlated response in female preferences due to artificial selection on foraging preferences that are mediated by a shared sensory system or by other mechanisms such as colour avoidance, pleiotropy or social experiences. This is the first experimental evidence that selection on a nonmating behaviour can affect male coloration and, more weakly, female preferences.

Effects of female preference intensity on the permissiveness of sexual trait polymorphisms

Abstract: Recent developments in sexual selection theory suggest that on their own, mate preferences can promote the maintenance of sexual trait diversity. However, how mate preferences constrain the permissiveness of sexual trait diversity in different environmental regimes remains an open question. Here, we examine how a range of mate choice parameters affect the permissiveness of sexual trait polymorphism under several selection regimes. We use the null model of sexual selection and show that environments with strong assortative mating significantly increase the permissiveness of sexual trait polymorphism. We show that for a given change in mate choice parameters, the permissiveness of polymorphism changes more in environments with strong natural selection on sexual traits than in environments with weak selection. Sets of nearly stable polymorphic populations with weak assortative mating are more likely to show accidental divergence in sexual traits than sets of populations with strong assortative mating. The permissiveness of sexual trait polymorphism critically depends upon particular combinations of natural selection and mate choice parameters.

An Ishihara-style test of animal colour vision

Abstract: Colour vision mediates ecologically relevant tasks for many animals, such as mate choice, foraging and predator avoidance. However, our understanding of animal colour perception is largely derived from human psychophysics, even though animal visual systems differ from our own. Behavioural tests of non-human animals are required to understand how colour signals are perceived by them. Here we introduce a novel test of colour vision in animals inspired by the Ishihara colour charts, which are widely used to identify human colour deficiencies. These charts consist of dots that vary in colour, brightness and size, and are designed so that a numeral or letter is distinguishable from distractor dots for humans with normal colour vision. In our method, distractor dots have a fixed chromaticity (hue and saturation) but vary in luminance. Animals can be trained to find single target dots that differ from distractor dots in chromaticity. We provide Matlab code for creating these stimuli, which can be modified for use with different animals. We demonstrate the success of this method with triggerfish, Rhinecanthus aculeatus, and highlight behavioural parameters that can be measured, including success of finding the target dot, time to detect dot and error rate. Triggerfish quickly learnt to select target dots that differed from distractors dots regardless of the particular hue or saturation, and proved to use acute colour vision. We measured discrimination thresholds by testing the detection of target colours that were of increasing colour distances (ΔS) from distractor dots in different directions of colour space. At least for some colours, thresholds indicated better discrimination than expected from the Receptor Noise Limited (RNL) model assuming 5% Weber fraction for the long-wavelength cone. This methodology seems to be highly effective because it resembles natural foraging behavior for the triggerfish and may well be adaptable to a range of other animals, including mammals, birds, bees and freshwater fish. Other questions may be addressed using this methodology, including luminance thresholds, sensory bias, effects of sensory noise in detection tasks, colour categorization and saliency.

Evolution and learning in artificial ecosystems

Abstract: A generic model is presented for ecosystems inhabited by artificial animals, or animats, that develop over time. The individual animats develop continuously by means of generic mechanisms for learning, forgetting, and decisionmaking. At the same time, the animat populations develop in an evolutionary process based on fixed mechanisms for sexual and asexual reproduction, mutation, and death. The animats of the ecosystems move, eat, learn, make decisions, interact with other animats, reproduce, and die. Each animat has its individual sets of homeostatic variables, sensors, and motors. It also has its own memory graph that forms the basis of its decision-making. This memory graph has an architecture (i.e. graph topology) that changes over time via mechanisms for adding and removing nodes. Our approach combines genetic algorithms, reinforcement learning, homeostatic decision-making, and dynamic concept formation. To illustrate the generality of the model, five examples of ecosystems are given, ranging from a simple world inhabited by a single frog to a more complex world in which grass, sheep, and wolves interact.