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Beldade, P.

Publications and source records attributed to Beldade, P..

11 recordsLinked to original sources

Dietary ethanol affects feeding behaviour, flight performance, and mating success in a fruit-feeding butterfly

O_LIThe evolution of fleshy fruits around 124 million years ago introduced a nutritious resource and drove shifts toward fruit-feeding across the animal kingdom, leading to a variety of adaptations for locating and exploiting this resource. Fruits are inherently dynamic, changing in physical, chemical, and biological properties as they progress from development through ripening to decay. C_LIO_LIFruit fermentation produces ethanol, a volatile compound that is simultaneously caloric, intoxicating, and potentially noxious. While the immediate and long-term effects of dietary ethanol are well documented in mammals, and to some extent in insects such as Drosophila, very little is known about its impact on frugivorous butterflies. C_LIO_LIAlthough ethanol can serve as a foraging cue for frugivorous butterflies, its ingestion may impair performance and reduce fitness. Here, we examine how dietary ethanol affects ecologically and reproductively relevant behaviours in the Afrotropical butterfly Bicyclus anynana, a species that feeds on fermenting fruits in the wild. C_LIO_LIWe found that butterflies exposed to ethanol-supplemented diets initiated feeding more rapidly, but also spent less time feeding, and they required more stimuli to sustain flight. Moreover, feeding behaviour differed between males and females and between mated and virgin individuals, while flight performance differed between sexes but was not affected by mating status. C_LIO_LIGiven the involvement of flight in male courtship, we also tested the hypothesis that negative effects of ethanol consumption on flight would impair courtship. We found that males fed on ethanol-supplemented diets--particularly young ones--had reduced mating success and took longer to secure a mating. C_LIO_LITogether, our findings demonstrate that ethanol consumption affects behaviours closely tied to survival and fitness in B. anynana, suggesting that exposure to fermenting resources may impose selective pressures on physiology, behaviour, and reproductive strategies in frugivorous insects. C_LI

animal behavior and cognition↗

Wound-induced eyespots on butterfly wings at the intersection of immune response and pigmentation development

Butterfly eyespots are striking examples of evolutionary novelty arising through the repurposing of ancestral genetic pathways, including pathways involved in wound healing. Given the activation of the immune system during wound healing, and the known links between immunity and pigmentation, we hypothesized that the immune response triggered by wounding contributes to the formation of wound-induced ectopic eyespots on butterfly wings. We tested this hypothesis by wounding the wings of Bicyclus anynana pupae and modulating immune challenge levels with application of varying quantities of heat-killed bacteria. These led to up-regulation of defense-related genes in the wounded wing as well as in the contralateral non-wounded wing. Immune activation did not affect the likelihood of ectopic eyespot formation, but it did significantly influence the extent of pigmentation changes around injury sites: stronger immune activation produced larger ectopic eyespots. This effect was localized to the treated wing and did not affect contralateral, control wound-induced eyespots. Additionally, stronger immune challenges led to smaller overall wing size and to relatively smaller native eyespots. Our findings reveal that immune activation contributes to the development of wound-induced eyespots and impacts both pigmentation pattern formation and wing size regulation. These results underscore the complex interplay between immune function and developmental processes, and provide new insights into the origins of lineage-specific morphological innovations.

evolutionary biology↗

Thermal plasticity in protective wing pigmentation is modulated by genotype and food availability in an insect model of seasonal polyphenism.

Developmental plasticity refers to the phenomenon whereby an organisms phenotype depends on the environmental conditions experienced during development. This plasticity can match phenotype to ecological conditions and help organisms to cope with environmental heterogeneity, including differences between alternating seasons. Experimental studies of developmental plasticity often focus on the impact of individual environmental cues and do not take explicit account of genetic variation. In contrast, natural environments are complex, comprising multiple variables with combined effects that are poorly understood and may vary among genotypes. We investigated the effects of multifactorial environments on the development of the seasonally plastic eyespots of Bicyclus anynana butterflies. Eyespot size is known to depend on developmental temperature and to be involved in alternative seasonal strategies for predator avoidance. In nature, both temperature and food availability undergo seasonal fluctuations. However, our understanding of whether thermal plasticity in eyespot size varies in relation to food availability and across genotypes remains limited. To address this, we investigated the combined effects of temperature (T; two levels: 20{degrees}C and 27{degrees}C) and food availability (N; two levels: control and limited) during development. We examined their impact on wing and eyespot size in adult males and females from multiple genotypes (G; 28 families). We found evidence of thermal and nutritional plasticity, and of temperature-by-nutrition interactions (significant TxN) on the size of eyespots in both sexes. Food limitation resulted in relatively smaller eyespots and tempered the effects of temperature. Additionally, we found differences among families for thermal plasticity (significant GxT effects), but not for nutritional plasticity (non-significant GxN effects) nor for the combined effects of temperature and food limitation (non-significant GxTxN effects). Our results reveal the context dependence of thermal plasticity, with the slope of thermal reaction norms varying across genotypes and across nutritional environments. We discuss these results in light of the ecological significance of pigmentation and the value of considering thermal plasticity in studies of the biological impact of climate change.

evolutionary biology↗

Genetic basis of variation in thermal developmental plasticity for Drosophila melanogaster body pigmentation

Seasonal differences in insect pigmentation are attributed to the influence of ambient temperature on pigmentation development. This thermal plasticity is adaptive and heritable, thereby capable of evolving. However, the specific genes contributing to the variation in plasticity that can drive its evolution remain largely unknown. To address this, we analyzed pigmentation and pigmentation plasticity in Drosophila melanogaster. We measured two components of pigmentation in the thorax and abdomen: overall darkness and the proportion of length covered by darker pattern elements (a trident in the thorax and bands in the abdomen) in females from two developmental temperatures (17{degrees}C or 28{degrees}C) and 191 genotypes. Using a GWAS approach to identify the genetic basis of variation in pigmentation and its response to temperature, we identified numerous dispersed QTLs, including some mapping to melanogenesis genes (yellow, ebony, and tan). Remarkably, we observed limited overlap between QTLs for variation within specific temperatures and those influencing thermal plasticity, as well as minimal overlap between plasticity QTLs across pigmentation components and across body parts. For most traits, consistent with selection favoring the retention of plasticity, we found that lower plasticity alleles were often at lower frequencies. The functional analysis of selected candidate QTLs and pigmentation genes largely confirmed their contributions to variation in pigmentation and/or pigmentation plasticity. Overall, our study reveals the existence and underlying basis of extensive and trait-specific genetic variation for pigmentation and pigmentation plasticity, offering a rich reservoir of raw material for natural selection to shape the independent evolution of these traits.

evolutionary biology↗

Effects of Wolbachia on transposable element activity largely depend on Drosophila melanogaster host genotype

Transposable elements (TEs) are repetitive DNA sequences capable of changing position in host genomes, thereby causing mutations. TE insertions typically have deleterious effects but they can also be beneficial. Increasing evidence of the contribution of TEs to adaptive evolution further raises interest in understanding what factors impact TE activity. Based on previous studies associating the bacterial endosymbiont Wolbachia to changes in the abundance of piRNAs, a mechanism for TE repression, and to transposition of specific TEs, we hypothesized that Wolbachia infection would interfere with TE activity. We tested this hypothesis by studying expression of 14 TEs in a panel of 25 Drosophila melanogaster host genotypes, naturally infected with Wolbachia and annotated for TE insertions. The host genotypes differed significantly in Wolbachia titers inside individual flies, with broad-sense heritability around 20%, and in the number of TE insertions, which depended greatly on TE identity. By removing Wolbachia from the target host genotypes, we generated a panel of 25 pairs of Wolbachia-positive and Wolbachia-negative lines in which we quantified transcription levels our target TEs. We found variation in TE expression that was dependent on Wolbachia status, TE identity, and host genotype. Comparing between pairs of Wolbachia-positive and Wolbachia-negative flies, we found that Wolbachia removal affected TE expression in 23.7% of the TE-genotype combinations tested, with up to 4.6 times differences in median level of transcript. Our data shows that Wolbachia can impact TE activity in host genomes, underscoring the importance this endosymbiont can have in the generation of genetic novelty in hosts.

evolutionary biology↗

Mosaic evolution of molecular pathways for sex pheromone communication in a butterfly

Unraveling the origin of molecular pathways underlying the evolution of adaptive traits is essential for understanding how new lineages emerge, including the relative contribution of conserved, ancestral traits, and newly evolved, derived traits. Here, we investigated the evolutionary divergence of sex pheromone communication from moths (mostly nocturnal) to butterflies (mostly diurnal) that occurred ~98 million years ago. In moths, females typically emit pheromones to attract male mates, but in butterflies pheromones and used by females for mate choice. The molecular bases of sex pheromone communication are well understood in moths, but have remained virtually unexplored in butterflies. We used a combination of transcriptomics, real time qPCR, and phylogenetics, to identify genes involved in different steps of sex pheromone communication in the butterfly Bicyclus anynana. Our results show that the biosynthesis and reception of sex pheromones relies both on moth-specific gene families (reductases) and on more ancestral insect gene families (desaturases, olfactory receptors, odorant binding proteins). Interestingly, B. anynana further appears to use what was believed to be the moth-specific neuropeptide Pheromone Biosynthesis Activating Neuropeptide (PBAN) for regulation of sex pheromone production. Altogether, our results suggest that a mosaic pattern best explains how sex pheromone communication evolved in butterflies, with some molecular components derived from moths, and others conserved from more ancient insect ancestors. This is the first large-scale analysis of the genetic pathways underlying sex pheromone communication in a butterfly.

evolutionary biology↗

Many ways to make darker flies: Intra- and inter-specific variation in Drosophila body pigmentation components

Body pigmentation is an evolutionarily diversified and ecologically relevant trait that shows variation within and between species, and important roles in animal survival and reproduction. Insect pigmentation, in particular, provides some of the most compelling examples of adaptive evolution and its ecological and genetic bases. Yet, while pigmentation includes multiple aspects of color and color pattern that may vary more or less independently, its study frequently focuses on one single aspect. Here, we develop a method to quantify color and color pattern in Drosophila body pigmentation, decomposing thorax and abdominal pigmentation into distinct measurable traits, and we quantify different sources of variation in those traits. For each body part, we measured overall darkness, as well as four other pigmentation properties distinguishing between background color and color of the darker pattern elements that decorate the two body parts. By focusing on two standard D. melanogaster laboratory populations, we show that pigmentation components vary and co-vary in different manners depending on sex, genetic background, and developmental temperature. By studying three natural populations of D. melanogaster along a latitudinal cline and five other Drosophila species, we then show that evolution of lighter or darker bodies can be achieved by changing distinct component traits. Our study underscores the value of detailed phenotyping for a better understanding of phenotypic variation and diversification, and the ecological pressures and genetic mechanisms underlying them.

evolutionary biology↗

Predicting and Analyzing the Response to Selection on Correlated Characters

The breeders equation generally provides robust predictions for the short-term evolution of single characters. When selection targets two or more characters simultaneously, there are often large discrepancies between predicted and observed responses. We assessed how well this standard model predicts responses to bivariate selection on wing color pattern characteristics in the tropical butterfly Bicyclus anynana. In separate laboratory selection experiments, two sets of serially repeated eyespots were subjected to ten generations of concerted and antagonistic selection for either size or color composition. We compared predicted and actual selection responses over successive generations, using the phenotypic data, selection differentials, and estimates of the genetic variance-covariance matrix G. We found differences in the precision of predictions between directions of selection but did not find any evidence of systematic biases in our predictions depending on the direction of selection. Our investigation revealed significant environmental effects on trait evolution across generations. When these were accounted for, predictions using the standard model improved considerably. In the experiment on eyespot size, secondary splitting of selection lines allowed the estimation of changes in G after nine generations of selection. Changes were not in general agreement with expectations from the breeders equation. A contour plot of prediction errors across trait space suggests that directional epistasis in the eyespot genotype-phenotype map might occur but estimates of changes in G are too model-dependent to verify whether they agree with that hypothesis. Altogether, our results underscore the need for quantitative genetics to investigate and estimate potential effects of multivariate non-linear genotype-phenotype maps and of environmental effects on G.

evolutionary biology↗

Genetic basis of thermal plasticity variation in Drosophila melanogaster body size

Body size is a quantitative trait that is closely associated to fitness and under the control of both genetic and environmental factors. While developmental plasticity for this and other traits is heritable and under selection, little is known about the genetic basis for variation in plasticity that can provide the raw material for its evolution. We quantified genetic variation for body size plasticity in Drosophila melanogaster by measuring thorax and abdomen length of females reared at two temperatures from a panel representing naturally segregating alleles, the Drosophila Genetic Reference Panel (DGRP). We found variation between genotypes for the levels and direction of thermal plasticity in size of both body parts. We then used a Genome-Wide Association Study (GWAS) approach to unravel the genetic basis of inter-genotype variation in body size plasticity, and used different approaches to validate selected QTLs and to explore potential pleiotropic effects. We found mostly \"private QTLs\", with little overlap between the candidate loci underlying variation in plasticity for thorax versus abdomen size, for different properties of the plastic response, and for size versus size plasticity. We also found that the putative functions of plasticity QTLs were diverse and that alleles for higher plasticity were found at lower frequencies in the target population. Importantly, a number of our plasticity QTLs have been targets of selection in other populations. Our data sheds light onto the genetic basis of inter-genotype variation in size plasticity that is necessary for its evolution.\n\nSignificance StatementThe environmental conditions under which development takes place can affect developmental outcomes and lead to the production of phenotypes adjusted to the environment adults will live in. This developmental plasticity, which can help organisms cope with environmental heterogeneity, is heritable and under selection. Plasticity can itself evolve, a process that will be partly dependent on the available genetic variation for this trait. Using a wild-derived D. melanogaster panel, we identified DNA sequence variants associated to variation in thermal plasticity for body size. We found that these variants correspond to a diverse set of gene functions. Furthermore, their effects differ between body parts and properties of the thermal response, which can, therefore, evolve independently. Our results shed new light onto a number of key questions about the long discussed genes for plasticity.

evolutionary biology↗

Seasonal plasticity for anti-predatory strategies: matching colour and colour preference for effective crypsis

Effective anti-predatory strategies typically require matching appearance and behavior in prey, and there are many compelling examples of behavioral repertoires that enhance the effectiveness of morphological defenses. When protective adult morphology is induced by developmental environmental conditions predictive of future predation risk, adult behavior should be adjusted accordingly to maximize predator avoidance. While behavior is typically strongly affected by the adult environment, developmental plasticity in adult behavior -- mediated by the same pre-adult environmental cues that affect morphology -- could ensure an effective match between anti-predatory morphology and behavior. The coordination of environmentally-induced responses may be especially important in populations exposed to predictable environmental fluctuations (e.g. seasonality). Here, we studied early and late life environmental effects on a suite of traits expected to work together for effective crypsis. We focused on wing color and background color preference in Bicyclus anynana, a model of developmental plasticity that relies on crypsis as a seasonal strategy for predator avoidance. Using a full-factorial design, we disentangled effects of developmental and adult ambient temperature on both appearance and behavior. We showed that developmental conditions affect both adult color and color preference, with temperatures that simulate natural dry season conditions leading to browner butterflies with a perching preference for brown backgrounds. This effect was stronger in females, especially when butterflies were tested at lower ambient temperatures. In contrast to the expectation that motionlessness enhances crypsis, we found no support for our hypothesis that the browner dry-season butterflies would be less active. We argue that the integration of developmental plasticity for morphological and behavioral traits might improve the effectiveness of seasonal anti-predatory strategies. IMPACT SUMMARY To avoid predation, prey rely on strategies that typically include a variety of morphological and behavioral characteristics working together to deceive or scare predators. While some protective traits are a constitutive property of the prey species (e.g. hedgehog spines), others are produced only when the risk of encountering predators is high. For example, Daphnia crustaceans develop protective helmets and spines when exposed to cues that signal predator presence. When anti-predator morphologies are environmentally-induced, or plastic, the responses of associated behavioral traits should also be environmentally-dependent to ensure that animals exhibit behavioral repertoires that match their appearance. We used the tropical butterfly Bicyclus anynana, the squinting bush brown, to study these coordinated responses. In its natural habitat, with alternating dry and wet seasons, this thermally plastic butterfly alternates between seasonal forms with distinct wing color patterns related to distinct strategies to avoid predation. Dry season individuals, which develop under cooler temperatures, have small pattern elements on their wings and are cryptic against the brown background of dry foliage. In contrast, wet season individuals have large ornamental pattern elements that deflect attacks from predators towards the wing margin and away from their vulnerable bodies. We tested whether the cooler temperatures of the dry season also influenced other traits that can presumably improve the effectiveness of camouflage. In particular, we found that both the ornamental colors (appearance) and the choice of resting background colors (behavior) were affected by the temperature experienced during development. We found that dry season temperatures lead to browner butterflies with a stronger preference to rest on brown backgrounds. While behavior is typically very flexible in relation to changes in the adult environment, a developmental imprint on adult behavior can help ensure an effective match between the cryptic appearance and background choice behavior.

evolutionary biology↗

Complex effects of day and night temperature fluctuations on thermally plastic traits in an experimental model of adaptive seasonal plasticity.

BackgroundChanges in development in response to seasonally variable environments can produce phenotypes adjusted to fluctuating seasonal conditions and help organisms cope with temporal heterogeneity. In contrast to what happens in natural situations, experimental studies of developmental plasticity typically use environmental factors held constant during development, precluding assessment of potential environment-by-environment interaction effects.\n\nResultsWe tested effects of circadian fluctuations in temperature on a series of thermally plastic traits in a model of adaptive seasonal plasticity, the butterfly Bicyclus anynana. Comparing phenotypes from individuals reared under two types of fluctuations (warmer days with cooler nights, and cooler days with warmer nights) and those reared under a constant temperature of the same daily average allowed us to identify complex patterns of response to day and night temperatures. We found evidence of additive-like effects (for body size), but also different types of \"dominance\"-type effects where one particular period of the light cycle (for development time) or one particular extreme temperature (for eyespot size) had a relatively larger contribution to phenotype expression. We also gathered evidence against the hypothesis that thermal plasticity in development time drives thermal plasticity in other traits.\n\nConclusionsCombined effects of fluctuating day and night temperatures include additive-like effects as well as different types of environmental-dominance interaction effects. Differences between plastic traits reveal independent responses to temperature, and possible independent assessment of temperature conditions. Our study underscores the importance of understanding how organisms integrate complex environmental information towards a complete understanding of natural phenotypic variation and of the potential impact of environmental change thereon.

evolutionary biology↗