Natural selection in novel environments: predation selects for background matching in the body colour of a land fish

The invasion of a novel habitat often results in a variety of new selective pressures on an individual. One pressure that can severely impact population establishment is predation. The strategies that animals use to minimize predation, especially the extent to which those strategies are habitat or predator specific, will subsequently affect individuals' dispersal abilities. The invasion of land by a fish, the Pacific leaping blenny, Alticus arnoldorum, offers a unique opportunity to study natural selection following the colonization of a novel habitat. Various studies have examined adaptations in respiration and locomotion, but how these fish have responded to the predation regime on land was unknown. We studied five replicate populations of this fish around the island of Guam and found their body coloration converged on the terrestrial rocky backgrounds on which the fish were most often found. Subsequent experiments confirmed that this background matching significantly reduced predation. Natural selection has therefore selected for background matching in the body coloration of the Pacific leaping blenny to minimize predation, but it is a strategy that is habitat specific. A subsequent comparative study of closely related blenny species suggested that the evolutionary ancestor of the Pacific leaping blenny might have resembled the rocky backgrounds on land prior to invasion. The ancestors of the Pacific leaping blenny may therefore have already been ideally suited for the predator regime on land. More generally our results imply that animals must either already possess antipredator strategies that will be effective in new environments, or must adapt very quickly to new predation pressures if successful establishment is to occur. Ó 2013 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. Adaptive divergence among taxa often arises when populations invade new environments (reviewed by Schluter 2001). This is because changes in the selection regime experienced by invaders can lead to changes in phenotype (adaptation). The colonization of novel environments has therefore been of special interest to evolutionary biologists because of the opportunity it brings to study natural selection in the wild (e.g. If an individual is indistinguishable from other aspects of the environment, it is less likely to be attacked than one that is not. Tactics used to reduce detection and recognition by predators in this way include masquerading as an unpalatable food item Contents lists available at ScienceDirect Animal Behaviour j o u r n a l h o me p a g e : w w w . e l s e v i e r . c o m / l o ca t e / a n b e h a v establishment does occur, animals may be restricted to certain areas within that habitat where individuals are less conspicuous. Predation may still be a problem, but selection has the opportunity to drive the evolution of greater crypsis or some other strategy to minimize predation. Species in this latter scenario offer a means to study how predation can affect the colonization process and provide a wonderful opportunity to study the process of natural selection more generally (e.g. The primary goal of our study was to test the general hypothesis that visually oriented predators on land have selected for a body coloration in the Pacific leaping blenny that matches the rocky backgrounds against which the fish are typically found. We tested this hypothesis in two ways. First, we examined five populations of blenny around Guam and determined the extent to which the body coloration of each population matched their environments (we measured both the hue (chromatic) and brightness (achromatic) properties of fish and backgrounds). We replicated our study across five populations because initial observations suggested habitat backgrounds varied subtly from location to location. Given this, we predicted that populations would converge on the colour properties specific to their location. To provide a suitable benchmark for this colour comparison, we also quantified the colour of the dorsal fin, which is an important signal in social interactions for both males and females (Ord & Hsieh 2011) and should therefore be conspicuous in the environment (e.g. To provide some resolution of the evolutionary history of body coloration, and whether it might have facilitated or challenged the invasion of land by the Pacific leaping blenny, we supplemented these two studies with an ad hoc examination of body coloration in representative specimens of several closely related marine species found around the island. This comparative study was not meant to provide a formal phylogenetic reconstruction of ancestor phenotype, which would require detailed and extensive sampling of species across the blenny phylogeny (as well as their environments). Rather, the goal was to reveal the extent to which the Pacific leaping blenny differed or resembled its marine relatives and, by extension, the likelihood that the fish has evolved its presentday body coloration prior to, or following, the colonization of land. METHODS Population Colour Analysis Adult male and female Pacific leaping blennies and specimens of closely related species were captured using hand nets at five locations around Guam between June and August 2011 (overlapping with the probable breeding season of this genus; see Full body photographs were taken of individuals positioned side-on to the camera with the dorsal fin raised against a white standard background (X-Rite ColorChecker White Balance Card) and beside a ruler and a Munsell colour chart (X-Rite mini ColorChecker; Colour analysis was performed using the inCamera plug-in for Photoshop CS4. The images that were analysed for a given individual were those photographs that exhibited the lowest standard deviation for the red, green and blue (RGB) colour channels of the colour squares of the Munsell colour chart (i.e. those photographs with the least amount of within-image variance in lighting). The colour and brightness of these images were then standardized using the known RGB values of the colour squares in the Munsell chart with the inCamera plug-in (see To quantify achromatic properties or the brightness of colour, we took the average value of all three colour channels and divided this number by 255 to compute a value between 0 (corresponding to black or zero brightness) and 1 (corresponding to white or maximum brightness; NB: white has a value of 255 for the R, G and B channels, whereas black has a value of 0 for all three channels). We quantified the colour of fish for a common section of the dorsal fin and a representative, similarly sized area of the body This type of standardized colour analysis makes several assumptions about the spectral properties of the object being measured and, subsequently, the most relevant spectral sensitivities of the visual system of the organism viewing the object. Like most digital cameras, the one we used relied on image sensors that captured reflected light over a wavelength range of 400 to 700 nm, which is designed to match the wavelengths visible to humans. Actual data on the spectral sensitivity of these sensors for the make and model of the camera we used was not available. However, peak sensitivities of the sensors most likely occur at (or close to) 475, 550 and 625 nm, with sensitivity curves around these peaks overlapping extensively to ensure consistent colour representation across the visible spectrum in captured images (this is based on specifications published by Canon, the colour processing tests of DxO Image Science for the same make and model of camera (www. dxo.com), and the spectral sensitivities of other digital cameras that have been reported by Whether or not UV reflectance is relevant is dependent on the visual system of the predator viewing the blenny. We anticipated most predation occurred from birds, land crabs or lizards. Many birds and lizards do see into the UV To compare body, fin and background colour and brightness, we used the degree of overlap between the 95% confidence intervals of means and the magnitude of effect sizes (R/G and brightness ratios were normally distributed for all populations). Means with 95% confidence intervals that did not overlap were considered statistically different from one another (equivalent to P < 0.05). For effect size magnitude, we computed effects for two sample comparisons (body versus background colour or brightness; fin versus background colour or brightness) as a standardized mean difference (Cohen's d). This value and its 95% confidence interval were then converted into an r value. A biological effect was interpreted if the confidence intervals of r did not overlap zero. Equations for effect size computations are given in Predation Experiment We used highly realistic plasticine models made from casts of euthanized male and female Pacific leaping blennies to test the relative predation pressure between two environments: intertidal rocks and sandy beach. We chose Taga'chang to perform the experiment because it was a site where both habitat types occurred immediately adjacent to each other and were infrequently used by people. The blenny was found in both habitats, but densities were heavily skewed towards the rocky environment. Observations of blennies on the beach were generally limited to areas of wet sand within several metres of isolated rock outcrops that were within the intertidal zone. As a method of quantifying predation, the use of plasticine or clay models has been successfully used in a variety of taxa (e.g. Note that we assumed that predators were equally abundant in both environments. We had no reason to believe that this assumption was not correct prior to conducting the experiment: models and controls were positioned in rocky and beach habitat that were immediately adjacent to each other (e.g. within several metres of each other) and observations of birds, land crabs and lizards (likely predators) were made in both habitats. If anything, predator density may have been slightly skewed towards the rocky habitat: while birds were frequently observed in both habitats, we often observed large land crabs and lizards on the rocks but less so on the beach. Nevertheless, the subsequent frequency of attack rates recorded during the experiment was generally consistent with the notion that predators were equally likely to target stimuli in both habitats (see Results). Both models and controls were of similar size; photos of both stimuli positioned in the environment are shown in Models and controls were placed alternately along transects parallel to the shoreline at intervals of approximately 1.5 m. In the rocky habitat, models and controls were attached to rocks using fishing line and in areas that were above the high tide waterline, but otherwise within the splash zone (i.e. areas frequented by blennies but where stimuli would not be washed away by the tide). In the beach habitat, models and controls were secured by lengths of fishing line to plastic lids that were buried in the sand and positioned above the high tide waterline. The integrity of stimuli was checked daily and evidence of predation was tallied after 3 days, following which all stimuli were removed from the environment. On occasion, unusually large swells buried stimuli on the beach and these were replaced daily. On day 3, stimuli were categorized on the following criteria: (1) no marks; (2) single or multiple small nicks; (3) large punctures or nicks; (4) entire portions missing; or (5) only the anchor point remaining. For our analyses, we focused on categories 3 and 4 as evidence of predation. Category 2 seemed to reflect the inspection of stimuli by small scavenging organisms rather than predator attacks (e.g. ants nibbling at stimuli). Category 5 was exempt from analysis as it was not possible to exclude wave action or human interference as reasons for model disappearance. To make monitoring manageable, the experiment was conducted in two halves. Consecutive batches of stimuli were dispatched in nonoverlapping areas of each environment, for a final total of 70 models and 70 controls. The experiment was run over 8 days (2 days were devoted to the removal and positioning of stimuli between batches). Our final tally based on the recovery rates of stimuli was 52 models and 63 controls in the rocky habitat and 58 models and 64 controls from the beach habitat. The experiment was conducted from 6 July to 12 August 2011. Differences in predation rate between models and controls, and between environments for a given stimulus type, were evaluated through a comparison of 95% CIs of the proportion of stimuli exhibiting predation and relevant effect sizes (see previous section, Population Colour Analysis). Confidence intervals for proportions were computed using formula presented in Zar (2010). Comparisons in which the 95% CIs of proportions did not overlap were considered to be statistical different from one another (i.e. equivalent to P < 0.05). We also calculated effect sizes by computing an odds ratio and its associated 95% CI, and then converting this value into an r value using formula presented in . Comparative Study To explore the extent to which body coloration might have changed following the colonization of land, we compared the colour morphology of the Pacific leaping blenny to 12 closely related blenny species. These 12 species covered the full diversity of intertidal blenny species around Guam. Species ranged from exclusively marine (seven species) to amphibious (five species). These behavioural categorizations were based on observations made of fish behaviour during collection. Marine species were always observed fully immersed in water (e.g. swimming about in open water), while amphibious species were observed immersed in water and above the waterline in rock holes or (more rarely) out in the open on rocks. The Pacific leaping blenny was the only species that remained exclusively out of the water at all times. The assessment of species colour morphology relied largely on a qualitative comparison of coloration among species, coupled with a single estimate of the chroma and brightness of the specimen examined for each species. This comparison was made with reference to a preliminary phylogeny created using maximum parsimony and based on two mitochondrial DNA genes (ATPase 6 and 8) and four nuclear DNA genes (RAG1, ZiC, Sreb2 and Ptr; G. M. Cooke & T. J. Ord, unpublished data). A formal ancestor state reconstruction of chroma and hue was inappropriate given that the species found on Guam were only a subset of the species found in the entire C. L. Morgans, T. J. Ord / Animal Behaviour 86 Nevertheless, a general comparison of the colour morphology among our subset of species still provides a reasonable picture of the probable history of colour evolution in the group. For example, if the Pacific leaping blenny appears very similar in colour to its marine and amphibious relatives, then it likely evolved from an ancestor that was also very similar in appearance. Otherwise, the extent to which the Pacific leaping blenny differs in colour morphology from its immediate relatives provides a general indication of the extent to which colour evolution has likely changed following, or in conjunction with, the colonization of land. RESULTS Background Matchin

Evolutionary loss of complexity in animal signals: cause and consequence

We identified hypotheses for the cause and consequences of the loss of complexity in animal signals and tested these using a genus of visually communicating lizards, the Southeast Asian Draco lizards. Males of some species have lost the headbob component from their display, which is otherwise central to the communication of this genus. These males instead display a large, colorful dewlap to defend territories and attract mates. This dewlap initially evolved to augment the headbob component of the display, but has become the exclusive system of communication. We tested whether the loss of headbobs was caused by relaxed selection, habitat-dependent constraints, or size-specific energetic constraints on display movement. We then examined whether the consequences of this loss have been mitigated by increased signaling effort or com- plexity in the color of the dewlap. It appears the increased cost of display movement resulting from the evolution of large body size might have contributed to the loss of headbobs and has been somewhat compensated for by the evolution of greater complexity in dewlap color. However, this evolutionary shift is unlikely to have maintained the complexity previously present in the communication system, resulting in an apparent detrimental loss of information potential

Evolutionary predictors of mammalian home range size: body mass, diet and the environment

ABSTRACT Aim Mammalian home range patterns provide information on spatial behaviour and ecological patterns, such as resource use, that is often used by conservation managers in a variety of contexts. However, there has been little research on home range patterns outside of the terrestrial environment, potentially limiting the relevance of current home range models for marine mammals, a group of particular conservation concern. To address this gap, we investigated how variation in mammalian home range size among marine and terrestrial species was related to diet, environment and body mass. Location Global. Methods We compiled data on home range size, environment (marine and terrestrial), diet and body mass from the literature and empirical studies to obtain a dataset covering 462 mammalian species. We then used phylogenetic regression analyses (to address non-independence between species) to examine the relative contribution of these factors to variation of home range size among species. Results Body size explained the majority of the difference in home range size among species (53-85%), with larger species occupying larger home ranges. The type of food exploited by species was also an important predictor of home range size (an additional 15% of variation), as was the environment, but to a much lesser degree (1.7%). Main conclusions The factors contributing to the evolution of home ranges are more complex than has been assumed. We demonstrate that diet and body size both influence home range patterns but differ in their relative contribution, and show that colonization of the marine environment has resulted in the expansion of home range size. Broad-scale models are often used to inform conservation strategies. We propose that future integrative models should incorporate the possibility of phylogenetic effects and a range of ecological variables, and that they should include species representative of the diversity within a group

Deep-time convergent evolution in animal communication presented by shared adaptations for coping with noise in lizards and other animals animals

Convergence in communication appears rare compared with other forms of adaptation. This is puzzling, given communication is acutely dependent on the environment and expected to converge in form when animals communicate in similar habitats. We uncover deep-time convergence in territorial communication between two groups of tropical lizards separated by over 140 million years of evolution: the Southeast Asian Draco and Caribbean Anolis. These groups have repeatedly converged in multiple aspects of display along common environmental gradients. Robot playbacks to free-ranging lizards confirmed that the most prominent convergence in display is adaptive, as it improves signal detection. We then provide evidence from a sample of the literature to further show that convergent adaptation among highly divergent animal groups is almost certainly widespread in nature. Signal evolution is therefore curbed towards the same set of adaptive solutions, especially when animals are challenged with the problem of communicating effectively in noisy environments

Antiinflammatory Therapy with Canakinumab for Atherosclerotic Disease

Background: Experimental and clinical data suggest that reducing inflammation without affecting lipid levels may reduce the risk of cardiovascular disease. Yet, the inflammatory hypothesis of atherothrombosis has remained unproved. Methods: We conducted a randomized, double-blind trial of canakinumab, a therapeutic monoclonal antibody targeting interleukin-1β, involving 10,061 patients with previous myocardial infarction and a high-sensitivity C-reactive protein level of 2 mg or more per liter. The trial compared three doses of canakinumab (50 mg, 150 mg, and 300 mg, administered subcutaneously every 3 months) with placebo. The primary efficacy end point was nonfatal myocardial infarction, nonfatal stroke, or cardiovascular death. RESULTS: At 48 months, the median reduction from baseline in the high-sensitivity C-reactive protein level was 26 percentage points greater in the group that received the 50-mg dose of canakinumab, 37 percentage points greater in the 150-mg group, and 41 percentage points greater in the 300-mg group than in the placebo group. Canakinumab did not reduce lipid levels from baseline. At a median follow-up of 3.7 years, the incidence rate for the primary end point was 4.50 events per 100 person-years in the placebo group, 4.11 events per 100 person-years in the 50-mg group, 3.86 events per 100 person-years in the 150-mg group, and 3.90 events per 100 person-years in the 300-mg group. The hazard ratios as compared with placebo were as follows: in the 50-mg group, 0.93 (95% confidence interval [CI], 0.80 to 1.07; P = 0.30); in the 150-mg group, 0.85 (95% CI, 0.74 to 0.98; P = 0.021); and in the 300-mg group, 0.86 (95% CI, 0.75 to 0.99; P = 0.031). The 150-mg dose, but not the other doses, met the prespecified multiplicity-adjusted threshold for statistical significance for the primary end point and the secondary end point that additionally included hospitalization for unstable angina that led to urgent revascularization (hazard ratio vs. placebo, 0.83; 95% CI, 0.73 to 0.95; P = 0.005). Canakinumab was associated with a higher incidence of fatal infection than was placebo. There was no significant difference in all-cause mortality (hazard ratio for all canakinumab doses vs. placebo, 0.94; 95% CI, 0.83 to 1.06; P = 0.31). Conclusions: Antiinflammatory therapy targeting the interleukin-1β innate immunity pathway with canakinumab at a dose of 150 mg every 3 months led to a significantly lower rate of recurrent cardiovascular events than placebo, independent of lipid-level lowering. (Funded by Novartis; CANTOS ClinicalTrials.gov number, NCT01327846.

Is sociality required for the evolution of communicative complexity? Evidence weighed against alternative hypotheses in diverse taxonomic groups

All data used in this study have been archived in the Dryad Digital Repository: http://dx.doi.org/10.5061/dryad.nf7697j6Complex social communication is expected to evolve whenever animals engage in many and varied social interactions; that is, sociality should promote communicative complexity. Yet, informal comparisons among phylogenetically independent taxonomic groups seem to cast doubt on the putative role of social factors in the evolution of complex communication. Here, we provide a formal test of the sociality hypothesis alongside alternative explanations for the evolution of communicative complexity. We compiled data documenting variations in signal complexity among closely related species for several case study groups-ants, frogs, lizards and birds-and used new phylogenetic methods to investigate the factors underlying communication evolution. Social factors were only implicated in the evolution of complex visual signals in lizards. Ecology, and to some degree allometry, were most likely explanations for complexity in the vocal signals of frogs (ecology) and birds (ecology and allometry). There was some evidence for adaptive evolution in the pheromone complexity of ants, although no compelling selection pressure was identified. For most taxa, phylogenetic null models were consistently ranked above adaptive models and, for some taxa, signal complexity seems to have accumulated in species via incremental or random changes over long periods of evolutionary time. Becoming social presumably leads to the origin of social communication in animals, but its subsequent influence on the trajectory of signal evolution has been neither clear-cut nor general among taxonomic groups. © 2012 The Royal Society.J.G.P. was supported by a pre-doctoral research fellowship (JAE) from the CSIC.Peer Reviewe

Data from: Receiver perception predicts species divergence in long-range communication

The design of animal signals is believed to reflect the combined effect of the sensory system of receivers, the type of environment in which communication is being conducted, and the distance signals must travel in that environment. While empirical studies have examined how each of these factors might separately explain the structure of signals used by animals within species, comparative evidence supporting the predicted interaction of the sensory system, environment and transmission range in the generation of species differences in communication is lacking. I studied the long-range visual displays used by male Caribbean Anolis lizards to advertise territory ownership. The type of movements included in advertisement displays was closely predicted by the motion detection capabilities of the visual system for a given distance and the compounding affects of environmental conditions at the time of display production. Furthermore, the motion detection of Anolis receivers predicted almost precisely the type of movements included in advertisement displays among closely related species from two separate island radiations. My study provides rare comparative evidence illustrating how the sensory system of receivers sets the minimum requirements for what constitutes an effective signal, given the transmission distance of signals, with further variance in signal structure resulting from the environmental conditions occurring at the time of communication

Data from: Historical contingency and behavioural divergence in territorial Anolis lizards

The extent that evolution—including adaptation—is historically contingent (dependent on past events) has often been hotly debated, but is still poorly understood. In particular, there is little data on the degree that behaviour, an aspect of the phenotype that is strongly linked to contemporary environments (social or physical), retains the imprint of evolutionary history. In this study, I examined whether differences in the design of the territorial displays among species of Caribbean Anolis lizards reflect island specific selection regimes, or historically contingent predispositions associated with different clade histories. Adult males advertise territory ownership using a series of headbobs and dewlap extensions, bouts of which vary in duration among species. When display durations were mapped onto the Anolis phylogeny, prominent differences between species belonging to the Western and Eastern Caribbean radiations were apparent. Statistical analyses confirmed that species differences in the duration of headbob displays, and to some extent the duration of dewlap extensions, were historically contingent. The unique evolutionary histories of each clade have seemingly had a profound effect on the subsequent direction of display evolution among descendent taxa. These results combined with those from previous studies on these lizards show that past history can have an important impact on the type of behaviour exhibited by species today, to the point that adaptive evolution can proceed quite differently in lineages originating from different evolutionary starting points

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