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Caldart, M. V., M. B. dos SantosG. Machado (2021). Function of a multimodal signal: a multiple hypothesis test using a robot frog Journal of Animal Ecology, https://doi.org/10.1111/1365-2656.13620. Animals can communicate using signals perceived by different sensory systems, and many combine multiple sensory modalities in their display repertoires. Why these multimodal displays evolve and how they function to transmit information between individuals are crucial questions in behavioural and evolutionary research. Most empirical studies addressing these questions assume, even if implicitly, that signals of different modalities have independent effects on receiver responses. Nonetheless, the potential for interactions between signals as an explanation for the function of multimodal displays has been recognized for over two decades. Caldart et al. (2021) use a robotic frog and a receiver-based approach to test four alternative hypotheses for the function of multimodal (acoustic + visual) displays in the stream-dwelling frog Crossodactylus schmidti. Their results lend support to an inter-signal interaction mechanism, whereby inclusion of visual signals modifies the context in which an acoustic display is interpreted. In contrast, the results in Caldart et al. (2021) are less consistent with the hypotheses that emphasize the quality-related information encoded in different signal modalities and a hypothesis that focuses on signal transmission across heterogeneous environments. These results showcase how experimental manipulation of different signal modalities and tests of multiple alternative hypotheses are key to clarifying the function of multimodal displays.

Human activities have increased the intensity and frequency of natural stressors and created novel stressors, altering host-pathogen interactions, and changing the risk of emerging infectious diseases. Despite the ubiquity of such anthropogenic impacts, predicting the directionality of outcomes has proven challenging. Here, we conduct a systematic review and meta-analysis to determine the primary mechanisms through which stressors affect host-pathogen interactions and to evaluate the impacts stress has on host fitness (survival and fecundity) and pathogen infectivity (prevalence and intensity). We assessed 893 effect sizes from 71 host species (representing seven taxonomic groups) and 78 parasite taxa from 98 studies. We found that infected and uninfected hosts had similar sensitivity to stressors and that responses varied according to stressor type. Specifically, limited resources compromised host fecundity and decreased pathogen intensity, while abiotic environmental stressors (e.g., temperature and salinity) decreased host survivorship and increased pathogen intensity, and pollution increased mortality but decreased pathogen prevalence. We then used our meta-analysis results to develop Susceptible-Infected theoretical models to illustrate scenarios where infection rates are expected to increase or decrease in response to resource limitation or environmental stress gradients. Our results carry implications for conservation and disease emergence and reveal areas for future work.

Research Highlight: Delhey, K., Valcu, M., Dale, J.,Kempenaers, B. (2022). The evolution of carotenoid-based plumage colours in passerine birds. Journal of Animal Ecology, https://doi.org/10.1111/1365-2656.13791. Carotenoids, a class of colour pigments, are responsible for red, yellow and orange hues in nature. They play an important role in visual animals, and specially birds, where dietary carotenoids can act as honest sexual signals. Long-standing interest in the function of carotenoid-based colours has led to different hypotheses for their evolutionary drivers. Yet, comparative studies testing the generality of these hypotheses have been previously limited in phylogenetic scope or resolution. In a recent study, Delhey et al. (2022) combined sexual dichromatism, life history and environmental data to investigate the evolution of carotenoid-based colouration in the largest avian radiation, the passerines (Order: Passeriformes). The authors show that the expression of carotenoid-based colours depends on environmental availability, dietary content and body size. They also show that red carotenoids are more often evolutionarily and metabolically derived, and suggest different colours are favoured by natural and sexual selection. These findings shine new light on commonly held hypotheses of carotenoid-colour evolution and contribute to our understanding of how phenotypic diversity evolves.

Pleiotropy (multiple phenotypic effects of single genes) and epistasis (gene interaction) have key roles in the development of complex phenotypes, especially in polymorphic taxa. The development of discrete and heritable phenotypic polymorphisms often emerges from major-effect genes that interact with other loci and have pleiotropic effects on multiple traits. We quantified gene expression changes during ontogenetic color development in a polymorphic insect (damselfly: Ischnura elegans), with three heritable female morphs, one being a male mimic. This female color polymorphism is maintained by male mating harassment and sexual conflict. Using transcriptome sequencing and de novo assembly, we demonstrate that all three morphs downregulate gene expression during early color development. The morphs become increasingly differentiated during sexual maturation and when developing adult coloration. These different ontogenetic trajectories arise because the male-mimic shows accelerated (heterochronic) development, compared to the other female morphs. Many loci with regulatory functions in reproductive development are differentially regulated in the male-mimic, including upstream and downstream regulators of ecdysone signaling and transcription factors potentially influencing sexual differentiation. Our results suggest that long-term sexual conflict does not only maintain this polymorphism, but has also modulated the evolution of gene expression profiles during color development of these sympatric female morphs.

Frogs in the genus Phyllobates are known for the presence of batrachotoxin, a highly toxic alkaloid, in their skin. Nevertheless, Phyllobates frogs from Costa Rica and Panama (P. lugubris and P. vittatus) are considered non-toxic, as they have been reported to harbor low concentrations of this alkaloid. However, the potential toxicity of Central American Phyllobates has not been assessed experimentally. Our goal was to determine the toxicity of the whole skin of P. vittatus, an endemic species from the Southeastern Pacific region of Costa Rica. We performed median lethal dose (LD50) tests in mice to determine general toxicity, and an irritant assay based on the behavioral responses of mice to subcutaneous injection, to determine differences in irritability, as a measure of toxicity, among three study localities. Using UPLC-ESI-QTOF, we obtained chemical profiles of the methanolic extract of frog skins. Due to the absence of mortality at the studied doses, we were unable to estimate LD50. However, we recorded a list of toxicity symptoms in mice that are consistent with cardiotoxic effects, and found that mice presented more symptoms at higher concentrations of skin extracts during the first hour of the LD50 assays, recovering completely at all doses by the end of the assay. On the other hand, we did not detect differences in irritability among studied localities. Additionally, we putatively identified three toxic alkaloids (Batrachotoxinin A, DHQ 251A and Lehm 275A). This study provides the first experimental data on the toxicity and associated symptoms in mice, as well as the chemical profile of the skin of P. vittatus. We suggest that the skin alkaloids of P. vitattus may confer a chemical defense towards predators.

Intersexual signals that reveal developmental or mating status in females have evolved repeatedly in many animal lineages. Such signals have functions in sexual conflict over mating and can therefore influence sexually antagonistic coevolution. However, we know little about how female signal development modifies male mating harassment and thereby sexual conflict. Here, we combine phylogenetic comparative analyses of a color polymorphic damselfly genus (Ischnura) with behavioral experiments in one target species to investigate the evolutionary origin and current adaptive function of a developmental female color signal. Many Ischnura species have multiple female color morphs, which include a male-colored morph (male mimics) and one or two female morphs that differ markedly from males (heterochrome females). In Ischnura elegans, males and male-mimicking females express a blue abdominal patch throughout postemergence life. Using phenotypic manipulations, we show that the developmental expression of this signaling trait in heterochrome females reduces premating harassment prior to sexual maturity. Across species this signal evolved repeatedly, but in heterochrome females its origin is contingent on the signal expressed by co-occurring male-mimicking females. Our results suggest that the co-option of a male-like trait to a novel female antiharassment function plays a key role in sexual conflict driven by premating interactions.

1. Geographically widespread species provide excellent opportunities to investigate how phenotypes change across large-scale environmental gradients. Temperature is a fundamental environmental variable and an important determinant of insect fitness. However, field research is often geographically restricted, and typically concentrated in northern latitudes. Basic population biology and phenotypic clines in relation to temperature therefore remain poorly known across the entire geographic range, even in otherwise well-studied taxa. 2. We surveyed populations of the trimorphic damselfly Ischnura elegans in Cyprus, which is the southern range limit in Europe of this widespread insect species. Females of I. elegans occur in three discrete and heritable colour morphs, which vary in suites of phenotypic traits. One of these female morphs is a male-mimic that avoids excessive male-mating harassment by its male-like appearance, and which is more cold-tolerant than the two other morphs. 3. In contrast to the situation in northern Europe, these male-mimicking females are the minority morph in Cyprus, representing only about 5% of all females. Male mimics also have lower mating rates than alternative female morphs. 4. Individuals in Cyprus are relatively small in comparison to the reported European range for body size, consistent with Bergman's rule. 5. Finally, populations of I. elegans on the island have the longest flight period known in Europe, and there is only partial evidence for seasonality in flight activity. 6. These results underscore the benefits of considering the entire range of environmental conditions encountered by insect species when conducting evolutionary ecology research. (Less)

Colour polymorphisms are popular study systems among biologists interested in evolutionary dynamics, genomics, sexual selection and sexual conflict. In many damselfly groups, such as in the globally distributed genus Ischnura (forktails), sex-limited female colour polymorphisms occur in multiple species. Female-polymorphic species contain two or three female morphs, one of which phenotypically matches the male (androchrome or male mimic) and the other(s) which are phenotypically distinct from the male (heterochrome). These female colour polymorphisms are thought to be maintained by frequency-dependent sexual conflict, but their macroevolutionary histories are unknown, due to the lack of a robust molecular phylogeny. Here, we present the first time-calibrated phylogeny of Ischnura, using a multispecies coalescent approach (StarBEAST2) and incorporating both molecular and fossil data for 41 extant species (55% of the genus). We estimate the age of Ischnura to be between 13.8 and 23.4 millions of years, i.e. Miocene. We infer the ancestral state of this genus as female monomorphism with heterochrome females, with multiple gains and losses of female polymorphisms, evidence of trans-species female polymorphisms and a significant positive relationship between female polymorphism incidence and current geographic range size. Our study provides a robust phylogenetic framework for future research on the dynamic macroevolutionary history of this clade with its extraordinary diversity of sex-limited female polymorphisms.

We present The Odonate Phenotypic Database (OPD): an online data resource of dragonfly and damselfly phenotypes (Insecta: Odonata). Odonata is a relatively small insect order that currently consists of about 6400 species belonging to 32 families. The database consists of multiple morphological, life-history and behavioral traits, and biogeographical information collected from literature sources. We see taxon-specific phenotypic databases from Odonata and other organismal groups as becoming an increasing valuable resource in comparative studies. Our database has phenotypic records for 1011 of all 6400 known odonate species. The database is accessible at http://www.odonatephenotypicdatabase.org/, and a static version with an information file about the variables in the database is archived at Dryad., Measurement(s)Invertebrate Taxonomy • body length • wing • appendage morphology trait • mating behavior • flight behavior • habitat • ecozone • climate • sexual dimorphism • size • color • biological pigmentTechnology Type(s)digital curationFactor Type(s)phenotypesSample Characteristic - OrganismZygoptera • AnisopteraSample Characteristic - Environmentstream • pond • wetland ecosystem • lake • river • ephemeral springSample Characteristic - LocationSouth America • North America • Africa • Asia • Europe • Australia Machine-accessible metadata file describing the reported data: 10.6084/m9.figshare.10321595

Conflicts of interests between males and females over reproduction is a universal feature of sexually reproducing organisms and has driven the evolution of intersexual mimicry, mating behaviours and reproductive polymorphisms. Here, we show how temperature drives pre-reproductive selection in a female colour polymorphic insect that is subject to strong sexual conflict. These species have three female colour morphs, one of which is a male mimic. This polymorphism is maintained by frequency-dependent sexual conflict caused by male mating harassment. The frequency of female morphs varies geographically, with higher frequency of the male mimic at higher latitudes. We show that differential temperature sensitivity of the female morphs and faster sexual maturation of the male mimic increases the frequency of this morph in the north. These results suggest that sexual conflict during the adult stage is shaped by abiotic factors and frequency-independent pre-reproductive selection that operate earlier during ontogeny of these female morphs.

Pleiotropy (multiple phenotypic effects of single genes) and epistasis (gene interaction) have key roles in the development of complex phenotypes, especially in polymorphic taxa. The development of discrete and heritable phenotypic polymorphisms often emerges from major-effect genes that interact with other loci and have pleiotropic effects on multiple traits. We quantified gene expression changes during ontogenetic colour development in a polymorphic insect (damselfly:Ischnura elegans), with three heritable female morphs, one being a male mimic. This female colour polymorphism is maintained by male mating harassment and sexual conflict. Using transcriptome sequencing andde novoassembly, we demonstrate that all three morphs downregulate gene expression during early colour development. The morphs become increasingly differentiated during sexual maturation and when developing adult colouration. These different ontogenetic trajectories arise because the male-mimic shows accelerated (heterochronic) development, compared to the other female morphs. Many loci with regulatory functions in reproductive development are differentially regulated in the male-mimic, including upstream and downstream regulators of ecdysone signalling and transcription factors potentially influencing sexual differentiation. Our results suggest that long-term sexual conflict does not only maintain this polymorphism, but has also modulated the evolution of gene expression profiles during colour development of these sympatric female morphs.

Colour polymorphisms are popular study systems among biologists interested in evolutionary dynamics, genomics, sexual selection and sexual conflict. In many damselfly groups, such as in the globally distributed genus Ischnura (forktails), sex-limited female colour polymorphisms occur in multiple species. Female-polymorphic species contain two or three female morphs, one of which phenotypically matches the male (androchrome or male mimic) and the other(s) which are phenotypically distinct from the male (heterochrome). These female colour polymorphisms are thought to be maintained by frequency-dependent sexual conflict, but their macroevolutionary histories are unknown, due to the lack of a robust molecular phylogeny. Here, we present the first time-calibrated phylogeny of Ischnura, using a multispecies coalescent approach (StarBEAST2) and incorporating both molecular and fossil data for 41 extant species (55% of the genus). We estimate the age of Ischnura to be between 13.8 and 23.4 millions of years, i.e. Miocene. We infer the ancestral state of this genus as female monomorphism with heterochrome females, with multiple gains and losses of female polymorphisms, evidence of trans-species female polymorphisms and a significant positive relationship between female polymorphism incidence and current geographic range size. Our study provides a robust phylogenetic framework for future research on the dynamic macroevolutionary history of this clade with its extraordinary diversity of sex-limited female polymorphisms.

Extreme climatic events such as the El Nino Southern Oscillation profoundly affect many plants and animals, including amphibians, which are strongly negatively affected by drought conditions. How amphibians respond to exceptionally high precipitation as observed in La Nina events, however, remains unclear. We document the correlation between the exceedingly wet 2010–2012 La Nina and community-level changes in a leaf litter frog assemblage in Costa Rica. Relative abundances of species shifted, diversity and plot occupancy decreased, and community composition became homogenized with the onset of La Nina. These aspects remained altered for over 20 months but rebounded to pre-La Nina levels after approximately 12 months. We hypothesize that complex ecological cascades associated with excess moisture caused short-term declines in abundances of species and associated changes in community structure. If additional stressors such as disease or habitat loss are not co-occurring, frog communities can rapidly recover to pre-disturbance levels following severe climatic events.

Evolutionary divergence in the coloration of toxic prey is expected when geographic variation in predator composition and behavior favours shifts in prey conspicuousness. A fundamental prediction of predator-driven colour divergence is that the local coloration should experience lower predation risk than novel prey phenotypes. The dorsal coloration of the granular poison frog varies gradually from populations of conspicuous bright red frogs to populations of dull green and relatively cryptic frogs. We conducted experiments with clay models in four populations to examine the geographic patterns of taxon-specific predation. Birds avoided the local phenotype while lizards consistently selected for decreased conspicuousness and crab predation did not depend on frog coloration. Importantly, birds and lizards favoured low conspicuousness in populations where relatively cryptic green morphs have evolved. This study provides evidence for the interplay among distinct selective pressures, from multiple-predator taxa, acting on the divergence in protective coloration of prey species.(c) 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113, 580-589.

The evolution of aposematism is linked to increased opportunities for conspicuous sexual displays since detection by potential predators is no longer disadvantageous. Therefore, phenotypic divergence in aposematic species leading to relatively cryptic forms is expected to constrain such opportunities, by restoring the trade-off between natural and sexual selection on the boldness of sexual displays. We asked if and how a derived phenotype of the poison-dart frog Oophaga granulifera that appears relatively cryptic to potential predators exhibits conspicuous sexual displays for potential mates. We used visual modeling of frog contrasts against their natural backgrounds to test if for conspecifics green frogs appear less conspicuous than red frogs as they do for birds. We conducted behavioral observations of focal red and green males to determine if green frogs adjust their display behavior to the availability of potential mates. Dorsal brightness is known to influence female preferences in at least one poison frog species. We found that, despite being less visible under some measures, green frogs may appear as bright as red frogs for conspecifics but not birds, when viewed on dark backgrounds. Additionally, green males called more intermittently than red males when advertising to distant females, but they exhibited a dramatic increase in calling activity in proximity of a female and were as active as red males in this context. Together, our results suggest that green frogs retain context-dependent conspicuousness to conspecifics despite the evolution of relative crypsis to potential predators.

In animals with complex life cycles, fitness trade-offs across life stages determine the optimal time for transitions between stages. If these trade-offs vary predictably, adaptive plasticity in the timing of life history transitions may evolve. For instance, embryos of many species are capable of accelerating hatching to escape from egg predation and other hazards, but for plasticity in hatching timing to be selectively maintained, early hatching must also entail costs, probably in subsequent life stages. However the post-hatching environment, which influences this cost, is variable in nature. We assessed how two elements of the post-hatching environment, predator species and age structure created by hatching age plasticity, affect costs of hatching early in red-eyed treefrogs, Agalychnis callidryas. Red-eyed treefrog embryos were induced to hatch at the onset of hatching competence or near the peak of spontaneous hatching and exposed to one of three insect predators in single or mixed hatching-age treatments. Age structure created by hatching-age plasticity did not affect tadpole survivorship or growth; however, the consequences of hatching timing depended on predator species and foraging mode. Tadpoles that were induced to hatch early experienced initially higher mortality rates only with the more actively foraging predator. Nonetheless, mortality costs of accelerated hatching were apparent with all predators once we factored in the longer duration of exposure that early hatchlings experience in nature. This study suggests that extended exposure of young larvae to predators may be a general cost of early hatching, explaining why spontaneous hatching occurs later in life across variable environmental contexts.

We used a simple engineering principle, which suggests that the width of a road needed for a smooth traffic flow is proportional to the peak traffic volume (“engineering hypothesis”), to analyze the adaptive significance of trail width at branching points in the leaf-cutting ant Atta cephalotes. Since the flow of outgoing ants splits at trail bifurcations and merges when ants return to the nest through the same paths, the sum of branch widths should equal the width of the trail section upstream of the bifurcation. We measured the width of branches and their preceding trail section and also performed field measurements and manipulations to analyze ant flow, number of collisions, and ant speed in different trail sectors. Contrary to the prediction of the “engineering hypothesis”, the sum of branch widths was larger than the width of the trail immediately before the bifurcation. Our data contradict the “trail addition hypothesis” and support the “border effect hypothesis” to explain this pattern. First, the width of the widest branch was smaller than the width of the trail upstream of the bifurcation, an unexpected result if one branch is merely the continuation of the basal trail. Second, ants collided with obstacles more often in the margin than in the central portion of the trail, relocated ants from central to margin trail sectors reduced their speed, and ant flow was higher in the central sections of the trail. Since the delaying effect of trail margins increases as the trail width decreases, ants may build branches wider than expected to reduce the border effect. The delaying effect of trail margins should be included in the analysis of costs and benefits to fully understand the adaptive value of the design of ant trail networks.

Roughly 40% of amphibian species are in decline with habitat loss, disease, and climate change being the most cited threats. Heterogeneity of extrinsic (e.g. climate) and intrinsic (e.g. local adaptations) factors across a species' range should influence population response to climate change and other threats. Here we examine relative detectability changes for five direct-developing leaf litter frogs between 42-year sampling periods at one Lowland Tropical Forest site (51 m.a.s.l.) and one Premontane Wet Forest site (1100 m.a.s.l.) in southwest Costa Rica. We identify individualistic changes in relative detectability among populations between sampling periods at different elevations. Both common and rare species showed site-specific declines, and no species exhibited significant declines at both sites. Detection changes are correlated with changes in temperature, dry season rainfall, and leaf litter depth since 1969. Our study species share Least Concern conservation status, life history traits, and close phylogenetic relationship, yet their populations changed individualistically both within and among species. These results counter current views of the uniformity or predictability of amphibian decline response and suggest additional complexity for conservation decisions.

Aposematism and crypsis are often viewed as two extremes of a continuum of visual conspicuousness to predators. Theory predicts that behavioral and coloration conspicuousness should vary in tandem along the conspicuousness spectrum for antipredator strategies to be effective. Here we used visual modeling of contrast and behavioral observations to examine the conspicuousness of four populations of the granular poison frog, Oophaga granulifera, which exhibits almost continuous variation in dorsal color. The patterns of geographic variation in color, visual contrast, and behavior support a gradient of overall conspicuousness along the distribution of O. granulifera. Red and green populations, at the extremes of the color distribution, differ in all elements of color, contrast, and behavior, strongly reflecting aposematic and cryptic strategies. However, there is no smooth cline in any elements of behavior or coloration between the two extremes. Instead populations of intermediate colors attain intermediate conspicuousness by displaying different combinations of aposematic and cryptic traits. We argue that coloration divergence among populations may be linked to the evolution of a gradient of strategies to balance the costs of detection by predators and the benefits of learned aversion.

To understand host–parasite interactions, it is necessary to quantify variation and covariation in defence traits. We quantified parasite resistance and fitness tolerance of a polymorphic damselfly ( Ischnura elegans ), an insect with three discrete female colour morphs but with monomorphic males. We quantified sex and morph differences in parasite resistance (prevalence and intensity of water mite infections) and morph-specific fitness tolerance in the females in natural populations for over a decade. There was no evidence for higher parasite susceptibility in males as a cost of sexual selection, whereas differences in defence mechanisms between female morphs are consistent with correlational selection operating on combinations of parasite resistance and tolerance. We suggest that tolerance differences between female morphs interact with frequency-dependent sexual conflict, which maintains the polymorphism locally. Host–parasite interactions can therefore shape intra- and intersexual phenotypic divergence and interfere with sexual selection and sexual conflict.

Aposematism and crypsis are often viewed as two extremes of a continuum of visual conspicuousness to predators. Theory predicts that behavioral and coloration conspicuousness should vary in tandem along the conspicuousness spectrum for antipredator strategies to be effective. Here we used visual modeling of contrast and behavioral observations to examine the conspicuousness of four populations of the granular poison frog, Oophaga granulifera, which exhibits almost continuous variation in dorsal color. The patterns of geographic variation in color, visual contrast, and behavior support a gradient of overall conspicuousness along the distribution of O. granulifera. Red and green populations, at the extremes of the color distribution, differ in all elements of color, contrast, and behavior, strongly reflecting aposematic and cryptic strategies. However, there is no smooth cline in any elements of behavior or coloration between the two extremes. Instead populations of intermediate colors attain intermediate conspicuousness by displaying different combinations of aposematic and cryptic traits. We argue that coloration divergence among populations may be linked to the evolution of a gradient of strategies to balance the costs of detection by predators and the benefits of learned aversion.