Host-pathogen interactions under pressure: A review and meta-analysis of stress-mediated effects on disease dynamics.

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 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 891 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 limitations or environmental stress gradients. Our results carry implications for conservation and disease emergence and reveal areas for future work.

To colour a bird: The evolution of carotenoid-based colouration in passerines is shaped by sexual selection, ecology and life history.

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.

How signals interact in multimodal displays: Insights from a robotic frog.

IN FOCUS: Caldart, M. V., M. B. dos Santos & G. 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.

A molecularphylogeny offorktail damselflies(genus Ischnura)revealsa dynamic macroevolutionary history of female colour polymorphisms.

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.

Temperature drives pre-reproductive selection and shapes the biogeography of a female polymorphism.

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.

Macroevolutionary Origin and Adaptive Function of a Polymorphic Female Signal Involved in Sexual Conflict.

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.

Toxicity and Alkaloid Profiling of the Skin of the Golfo Dulcean Poison Frog Phyllobates vittatus (Dendrobatidae).

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.

Intra- and intersexual differences in parasite resistance and female fitness tolerance in a polymorphic insect.

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.

The genomics and evolution of inter-sexual mimicry and female-limited polymorphisms in damselflies.

Sex-limited morphs can provide profound insights into the evolution and genomic architecture of complex phenotypes. Inter-sexual mimicry is one particular type of sex-limited polymorphism in which a novel morph resembles the opposite sex. While inter-sexual mimics are known in both sexes and a diverse range of animals, their evolutionary origin is poorly understood. Here, we investigated the genomic basis of female-limited morphs and male mimicry in the common bluetail damselfly. Differential gene expression between morphs has been documented in damselflies, but no causal locus has been previously identified. We found that male mimicry originated in an ancestrally sexually dimorphic lineage in association with multiple structural changes, probably driven by transposable element activity. These changes resulted in ~900 kb of novel genomic content that is partly shared by male mimics in a close relative, indicating that male mimicry is a trans-species polymorphism. More recently, a third morph originated following the translocation of part of the male-mimicry sequence into a genomic position ~3.5 mb apart. We provide evidence of balancing selection maintaining male mimicry, in line with previous field population studies. Our results underscore how structural variants affecting a handful of potentially regulatory genes and morph-specific genes can give rise to novel and complex phenotypic polymorphisms.

Changes in gene expression during female reproductive development in a color polymorphic insect.

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.

The odonate phenotypic database, a new open data resource for comparative studies of an old insect order.

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.

Individualistic population responses of five frog species in two changing tropical environments over time.

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.

Not everything is black and white: color and behavioral variation reveal a continuum between cryptic and aposematic strategies in a polymorphic poison frog.

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.