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Debat, V.

Publications and source records attributed to Debat, V..

At least 19 recordsLinked to original sources

Catch me if you can: wild Morpho butterflies trade speed for erraticity in escape flight

Predator-prey interactions shape the evolution of escape behavior in prey, including different combinations of evasive movements, that may enhance unpredictability in fleeing directions and trajectories. So-called protean motion can enhance survival of flying prey in the wild, but quantifying such behaviors under natural conditions remains challenging. Here we used stereoscopic high-speed videography to record the escape flight behavior of wild males of the butterfly species Morpho menelaus in the Amazonian rainforest, and reconstructed 3D flight trajectories using artificial-neural-network-based tracking. During the experiments, we used a lure to attract freely patrolling male butterflies and elicited escape flights by intercepting their trajectory with a looming insect net swing. We then compared the escape flight kinematics to the pre-attack patrolling behavior. Attacks first induced a rapid upward maneuvering, directly followed by an unpredictable horizontal turn. The following escape flight trajectories showed increased horizontal erraticity and greater intra-individual heading variability, as compared to the pre-attack flight. Surprisingly, the mean speed decreased in the escape phase, notably in the horizontal plane. A significant negative association between horizontal trajectory complexity and flight speed was detected, indicating a speed-erraticity trade-off. These results show that wild Morpho butterflies respond to attacks by combining a climbing maneuver with an unpredictable heading change, followed by a protean escape flight; this increased escape erraticity comes at the expense of reduced escape flight speed. Because these large and relatively slow-flying butterflies display bright iridescent blue coloration on their dorsal wing side, erraticity during flight might enhance the dynamic flash coloration, likely limiting accurate targeting by predators.

animal behavior and cognition↗

Repeated evolution of convergent iridescence in closely-related species of Morpho butterflies living in sympatry

The evolution of visual traits in closely-related species living in sympatry is highly influenced by their ecological interactions: while sexual selection tends to promote the divergence of visual cues involved in mate choice, natural selection via predation may promote the convergence of dissuasive signals between prey species, especially in unpalatable or evasive prey. Here, we investigate the impact of sympatry on the evolution of the blue structural colouration in the wings of two closely-related Morpho butterfly species across several localities throughout Central and South America. Dorsal iridescence might affect mate choice and species recognition, which should promote its local divergence among species. However, the bright flashes and dynamic colour patterns produced by iridescence during flight might also increase survival by confusing predators and favouring escape. Such an effect might in turn lead to convergence in wing iridescence between evasive species occurring in sympatry, a phenomenon dubbed evasive mimicry. To test the effect of these putative antagonistic selective forces on visual cues evolution, we quantified the variation of the structural blue colour displayed at 13 different combinations of illumination/observation angles, on the wings of two closely-related Morpho species. We contrasted 10 sympatric and 11 allopatric locations and specifically compared the phenotypic distances between individuals from different species. Phenotypic distances between heterospecific pairs of individuals were significantly smaller in sympatry, consistent with the hypothesis of a local convergence of iridescence due to evasive mimicry. Interestingly, sexual dimorphism was found between males and females, suggesting that the trade-off between natural and sexual selection on the evolution of iridescence might differ between sexes. Our results suggest that local predation pressures may promote repeated evolutionary convergence of structural colouration between evasive prey species living in sympatry.

evolutionary biology↗

Genome-wide screen for deficiencies modifying Cyclin G-induced developmental instability in Drosophila melanogaster.

Despite long-lasting interest and research efforts, the genetic bases of developmental stability - the robustness to developmental noise - and its most commonly used estimator, fluctuating asymmetry (FA), remain poorly understood. The Drosophila melanogaster Cyclin G gene (CycG) encodes a transcriptional cyclin that regulates growth and the cell cycle. Over-expression of a potentially more stable isoform of the protein (deleted of a PEST-rich domain, hereafter called CycG{Delta}P) induces extreme wing size and shape FA (i.e. high developmental noise), indicating a major disruption of developmental stability. Previous attempts to identify the genetic bases of FA have been impeded by the constitutively low level of developmental noise, limiting the power to detect any effect. Here, we leverage the extreme developmental instability induced by overexpression of CycG{Delta}Pto explore the genetic bases of FA: we perform a genome-wide screen for deficiencies that enhance or reduce CycG{Delta}P-induced wing FA. 499 deficiencies uncovering 90% of the euchromatic genome were combined with a recombinant chromosome expressing CycG{Delta}P. We identified 13 and 16 deficiencies that respectively enhance and decrease FA. Analysis of mutants for some genes located in these deficiencies shows that Cyclin G ensures homogeneous growth of organs in synergy with the major morphogens of the wing, Dpp and Wg, as well as the Hippo and InR/TOR pathways. They also reveal that CycG{Delta}P-induced FA involves Larp, a potential direct interactor of Cyclin G, that regulates translation at the mitochondrial membrane. This opens up new research perspectives for understanding developmental stability, suggesting a significant role for mitochondrial activity.

genetics↗

Association of iridescence and tails with flight proxies suggests that predation drives convergence in skipper butterflies

1. Phenotypic evolution is shaped by phylogenetic, ecological and biomechanical constraints. Butterfly wings offer an ideal system to explore these constraints as their evolution is strongly influenced by natural and sexual selection affecting colour patterns and wing shape in relation to visual signalling and flight performance. 2. We focus on Eudamina skippers, butterflies with large-scale phenotypic convergences involving wing shape and colour pattern. Using a comprehensive morphometric dataset encompassing 176 species, we assess their morphological evolution in a phylogenetic framework. 3. We show that hindwing tails and dorsal iridescence, proposed to signal high escape ability, have repeatedly evolved in tropical species. Hindwing tails are associated with intermediate body size, low wing loading and a forewing shape that facilitates manoeuvrability; iridescence is more common in large species with significantly high wing loading and aspect ratio, indicating high flight speed and manoeuvrability. 4. The evolution of all tested morphometric traits is best described by Ornstein-Uhlenbeck models, indicating stabilising selection around fitness optima in Eudamina. Models testing for random drift or early burst dynamics were rejected in all cases. 5. We reveal a clear co-evolution between the fore- and hindwing shapes, despite both wings having different functional constraints. Hindwing tails have a significant recurrent effect on forewing shape in lineages evolving them independently, suggesting the existence of evolutionary trade-offs between flight performance and antipredator defences. 6. Our study shows that the convergent morphologies across Eudamina have likely arisen not by neutral evolution but by ecological selection influenced by biomechanical constraints.

evolutionary biology↗

Evolution of opsin genes in closely-related species of butterflies specialized in different microhabitats.

How do adaptive processes acting on the coevolution of opsin genes shape the evolution of colour vision in animals? At large phylogenetic scales, natural selection due to the contrasted light environments has been found to impact the evolution of photoreceptor genes. However, in closely-related species, species interactions due to sexual selection or competition may also influence opsin evolution. Here, we investigate the diversification of opsin sequences and their expression in closely-related blue Morpho butterfly species, living in different vertical strata within tropical forests, to shed light on the biotic and abiotic selective pressures shaping the coordinated evolution of opsin genes. We combined comparative genomics, transcriptomics, and immunochemistry to characterize the expression and the spatial distribution of the opsin proteins found in the eyes of Morpho helenor. We detected a double duplication of the LW opsin and found unique ommatidial types compared to other butterfly species. We then investigated the evolution of opsin genes among 21 Morpho species, found signatures of positive selection on two opsin genes (LW3Rh and BRh), and identified key co-evolving amino-acids within and among these two opsin genes. We showed that such opsin evolution was correlated with both light environment and wing coloration, highlighting the joint effect of several selective pressures in the coordinated evolution of proteins.

evolutionary biology↗

Sending mixed signals: convergent iridescence and divergent chemical signals in sympatric sister-species of Amazonian butterflies

The evolution of traits in closely related species living in sympatry strongly depends on both shared selective pressures and reproductive interference. In closely-related Morpho butterfly species living in the understory of the neo-tropical rainforest, the blue iridescent coloration of the wings is likely involved in predation evasion, as well as in mate recognition and courtship. We used spectrophotometry, behavioral experiments, visual modeling and chemical analyses to characterize the evolution of visual and chemical traits in two closely-related species, Morpho helenor and Morpho achilles. We specifically compared trait variation between samples from allopatric and sympatric populations of M. helenor to test the effect of ecological interactions with M. achilles on trait evolution. We quantified the differences in wing iridescence and tested for variations in the sexual preference for this trait. We found a strong similarity in iridescence between M. helenor and M. achilles in sympatry while the iridescence of M. helenor diverged in allopatry, suggesting that predation favors local resemblance. Although intraspecific behavioral experiments showed that iridescent signals could be used as visual cues during intraspecific mate choice, the strong resemblance of the iridescent signals between species may impair these species visual recognition. In contrast, the divergent chemical bouquets detected between species suggest that the visual similarity of sympatric Morpho species may have favored the divergence of alternative traits involved in species recognition, such as chemical cues.

evolutionary biology↗

Increased evolutionary rate in the Z-chromosome of Morpho butterflies and implications for speciation.

The evolution of reproductive isolation between populations shapes divergence in genome structure and content: comparing the genomes of closely-related species can thus enlighten the speciation process. Comparisons of genomes of allopatric vs. sympatric species sharing similar vs. dissimilar ecological niches allows to specifically investigate the effect of reinforcement and ecological specialization on genome evolution. In the butterfly genus Morpho, several species can be found in sympatry presenting specialisation in different microhabitats and temporal niches. Here, we sequenced, assembled and annotated the genomes of 8 Morpho species and used previously published genomes of three other Morpho species to study genomic rearrangements and signatures of positive selection. We found extensive chromosomal rearrangements in the Z chromosome compared to the autosomes, particularly among closely related sympatric species occupying similar niches, pointing at the putative role of inversions in preventing gene flow at a postzygotic level. We also detected a higher proportion of genes under positive selection on the Z-chromosome compared to the autosomes, suggesting a potential role of the Z-chromosome in driving adaptive evolution in Morpho. Finally, because of the divergence in daily activities between species, we studied the evolution of eight genes involved in the circadian clock and detected a signature of positive selection on the gene Period, located in the Z chromosome. By studying the evolution of genome structure and coding sequences, our study indicates fast evolution of the Z-chromosome, partly driven by selection, throughout this genus, highlighting the putative implication of this sexual chromosome on pre and post-zygotic isolation.

evolutionary biology↗

Evolution of genetic (co)variances during the worldwide invasion of Drosophila suzukii

The extent to which phenotypic evolution can be constrained by genetic correlations is an important question in evolutionary biology. To address this question, biological invasions are opportune models where derived, invasive populations can be compared to their extant ancestors, allowing to track the evolution of genetic correlations from the ancestor, throughout the invasion process. In this paper, we focused on the worldwide invasion of Drosophila suzukii (Matsumara, 1931), and investigated the evolution of the genetic covariance matrix G of wing shape between ancestral native, and derived invasive populations. Leveraging demographic history resolved by population genetics approaches, we tested whether G remained stable during the invasion. Using a multivariate QST-FST approach, we further tested whether or not the observed phenotypic divergence in wing shape aligned with a neutral scenario of evolution. Our results show moderate yet significant quantitative genetic differentiation of wing shape among D. suzukii populations and a relative stability in the structure of G, presenting a roughly spherical shape but slightly different volumes. These characteristics likely reflect the demographic history of populations and suggest a low level of genetic constraint on wing shape evolution. The divergence between populations was greater than expected under a purely neutral model of evolution, compatible with an effect of divergent selection among them. Overall, our study suggests that selection and drift, but not ancestral genetic constraints, affected the early stages of wing shape evolution during D. suzukii invasion.

evolutionary biology↗

Genome assembly of three Amazonian Morpho butterflyspecies reveals Z-chromosome rearrangements betweenclosely-related species living in sympatry

The genomic processes enabling speciation and the coexistence of species in sympatry are still largely unknown. Here we describe the whole genome sequencing and assembly of three closely-related species from the butterfly genus Morpho: Morpho achilles (Linnaeus, 1758), M. helenor (Cramer, 1776) and M. deidamia (Hubner, 1819). These large blue butterflies are emblematic species of the Amazonian rainforest. They live in sympatry in a wide range of their geographical distribution and display parallel diversification of dorsal wing colour pattern, suggesting local mimicry. By sequencing, assembling and annotating their genomes, we aim at uncovering pre-zygotic barriers preventing gene flow between these sympatric species. We found a genome size of 480 Mb for the three species and a chromosomal number ranging from 2n = 54 for M. deidamia to 2n = 56 for M. achilles and M. helenor. We also detected inversions on the sex chromosome Z that were differentially fixed between species, suggesting that chromosomal rearrangements may contribute to their reproductive isolation. The annotation of their genomes allowed us to recover in each species at least 12,000 protein-coding genes and to discover duplications of genes potentially involved in pre-zygotic isolation like genes controlling colour discrimination (L-opsin). Altogether, the assembly and the annotation of these three new reference genomes open new research avenues into the genomic architecture of speciation and reinforcement in sympatry, establishing Morpho butterflies as a new eco-evolutionary model.

genomics↗

Automatically producing large morphometric datasets from natural history collection images: a case study of Lepidoptera wing shape

Publicly available image data (2D and 3D) from biological specimens is becoming extremely widespread, notably following digitization efforts from natural history institutions worldwide. To deal with this huge amount of data, high-throughput phenotyping methods are being developed by researchers, to extract biologically meaningful data, in correlation with the burgeoning of the field of phenomics. Here we explore the potential of a combination of simple image treatment algorithms, with a geometric morphometrics contour analysis, applicable to strongly standardized images such as collections of Lepidotera. Using a previously manually landmarked dataset of Morpho butterflies, we show that our automated approach can produce a morphospace similar to that produced by a manual approach. Although the former is more noisy than the latter, it appears to pick up phylogenetic and to some extent ecological signal. Applying then the same approach to a large dataset of images from two different museums, we produce a morphospace containing >5000 specimens, representing 851 species in 24 families of butterflies and moths. The most notable feature of this space is that Sphingidae morphology is clearly separate from the rest, and appears much more constrained. We also show some indirect evidence that at this large interspecific level, potential museum related bias (e.g. inter-user bias in specimen preparation and photography) can be negligible. Altogether, our results suggest that this approach has the potential to produce large-scale analysis of morphology, and could be refined to include more specimens.

evolutionary biology↗

Evidence of attack deflection suggests adaptive evolution of wing tails in butterflies

Predation is a powerful selective force shaping many behavioural and morphological traits in prey species. The deflection of predator attacks from vital parts of the prey usually involves the coordinated evolution of prey body shape and colour. Here, we test the deflection effect of hindwing tails in the swallowtail butterfly Iphiclides podalirius. In this species, hindwings display long tails associated with a conspicuous colour pattern. By surveying the wings within a wild population of I. podalirius, we observed that wing damage was much more frequent on the tails. We then used a standardised behavioural assay employing dummy butterflies with real I. podalirius wings to study the location of attacks by great tits Parus major. Wing tails and conspicuous coloration of the hindwings were struck more often than the rest of the body by birds. Finally, we characterised the mechanical properties of fresh wings and found that the tail vein was more fragile than the others, suggesting facilitated escape ability of butterflies attacked at this location. Our results clearly support the deflective effect of hindwing tails and suggest that predation is an important selective driver of the evolution of wing tails and colour pattern in butterflies.

evolutionary biology↗

Long-term evolution of quantitative traits in the Drosophila melanogaster species subgroup

Quantitative genetics aims at untangling the genetic and environmental effects on phenotypic variation. Trait heritability, which summarizes the relative importance of genetic effects, is estimated at the intraspecific level, but theory predicts that heritability could influence long-term evolution of quantitative traits. The phylogenetic signal concept bears resemblance to heritability and it has often been called species-level heritability. Under certain conditions, such as trait neutrality or contribution to phylogenesis, within-species heritability and between-species phylogenetic signal should be correlated. Here, we investigate the potential relationship between these two concepts by examining the evolution of multiple morphological traits for which heritability has been estimated in Drosophila melanogaster. Specifically, we analysed 42 morphological traits in both sexes on a phylogeny inferred from 22 nuclear genes for nine species of the melanogaster subgroup. We used Pagels {lambda} as a measurement of phylogenetic signal because it is the least influenced by the number of analysed taxa. Pigmentation traits showed the strongest concordance with the phylogeny, but no correlation was found between phylogenetic signal and heritability estimates mined from the literature. We obtained data for multiple climatic variables inferred from the geographical distribution of each species. Phylogenetic regression of quantitative traits on climatic variables showed a significantly positive correlation with heritability. Convergent selection, the response to which depends on the trait heritability, may have led to the null association between phylogenetic signal and heritability for morphological traits in Drosophila. We discuss the possible causes of discrepancy between both statistics and caution against their confusion in evolutionary biology.

evolutionary biology↗

Punctual ecological changes rather than global factors drive species diversification and the evolution of wing phenotypes in Morpho butterflies.

Assessing the relative importance of geographical and ecological drivers of evolution is paramount to understand the diversification of species and traits at the macroevolutionary scale. Here, we use an integrative approach, combining phylogenetics, biogeography, ecology, and quantified phenotypes to investigate the drivers of both species and phenotypic diversification of the iconic Neotropical butterfly genus Morpho. We generated a time-calibrated phylogeny for all known species and inferred historical biogeography. We fitted models of time-dependent (accounting for rate heterogeneity across the phylogeny) and paleoenvironment-dependent diversification (accounting for global effect on the phylogeny). We used geometric morphometrics to assess variation of wing size and shape across the tree, and investigated their dynamics of evolution. We found that the diversification of Morpho is best explained when considering multiple independent diversification dynamics across the tree, possibly associated with lineages occupying different microhabitat conditions. First, a shift from understory to canopy was characterized by an increased speciation rate partially coupled with an increasing rate of wing shape evolution. Second, the occupation of dense bamboo thickets accompanying a major host-plant shift from dicotyledons towards monocotyledons was associated with a simultaneous diversification rate shift and an evolutionary "jump" of wing size. Our study points to a diversification pattern driven by punctual ecological changes instead of a global driver or biogeographic history.

evolutionary biology↗

Gliding in the Amazonian canopy: adaptive evolution of flight in Morpho butterflies

The diversity of flying animals suggests that countless combinations of morphologies and behaviors have evolved with specific lifestyles, thereby exploiting diverse aerodynamic mechanisms. Elucidating how morphology, flight behavior and aerodynamic properties together diversify with contrasted ecologies remains however seldom accomplished. Here, we studied the adaptive co-divergence in wing shape, flight behavior and aerodynamic efficiency among Morpho butterflies living in different forest strata, by combining high-speed videography in the field with morphometric analyses and aerodynamic modelling. By comparing canopy and understory species, we show that adaptation to an open canopy environment resulted in increased glide efficiency. Moreover, this enhanced glide efficiency was achieved by different canopy species through strikingly distinct combinations of flight behavior, wing shape and aerodynamic mechanisms, highlighting the multiple pathways of adaptive evolution. One Sentence SummaryBy combining high-speed videography, geometric morphometrics and computational aerodynamic modelling, our study of wild Amazonian Morpho butterflies reveals a strong contrast between the efficient gliding flight of canopy species and the powerful flapping flight of understory species, pointing at a combined adaptive divergence of wing shape and flight behavior among sympatric species flying in different forest strata.

evolutionary biology↗

Convergent morphology and divergent phenology: unravelling the coexistence of mimetic Morpho butterfly species

The emergence and persistence of closely-related species in sympatry is puzzling because the potential gene flow and the common local selective pressures may lead to either merging or competitive exclusion. Some species of Morpho butterflies occurring in sympatry display highly similar wing colour patterns. Associated with erratic flight abilities, their bright colouration may limit predator success and discourage future attacks. The evolution of similar colouration in sympatric species is thus likely under local selection by predators (i.e. escape mimicry). Such phenotypic similarity may promote interspecific territoriality and/or reproductive interference, questioning how closely-related co-mimetic species become sexually isolated and coexist in sympatry. We performed a series of field experiments using flying Morpho dummies placed in a natural habitat where wild males commonly patrol. Analysing the interactions of wild Morpho with different dummies, we show that similarity in wing colour pattern leads to interspecific territoriality and courtship among sympatric species. Using genomic data, we then showed that sympatric Morpho species are surprisingly strictly isolated despite their close relatedness and the observed heterospecific interactions. Finally, using a mark-recapture experiment, we discovered a strong temporal segregation in patrolling activity of males from two co-mimetic sister species. Such divergence in phenology may favour sympatry between closely-related species, despite behavioural interferences induced by the local convergence in colour pattern. Altogether, our findings show that temporal segregation may facilitate the co-existence of closely-related species sharing the same ecological niche, suggesting that phenological shifts may represent an overlooked factor of sympatric speciation. Our study therefore highlights how the evolution of multiple traits may favour species diversification in sympatry by partitioning niche in different dimensions.

evolutionary biology↗

Convergence in sympatry: evolution of blue-banded wing pattern in Morpho butterflies

Species interactions such as mimicry can promote trait convergence but disentangling this effect from those of shared ecology, evolutionary history and niche conservatism is often challenging. Here by focusing on wing color pattern variation within and between three butterfly species living in sympatry in a large proportion of their range, we tested the effect of species interactions on trait diversification. These butterflies display a conspicuous iridescent blue coloration on the dorsal side of their wings and a cryptic brownish colour on the ventral side. Combined with an erratic and fast flight, these color patterns increase the difficulty of capture by predators and contribute to the high escape abilities of these butterflies. We hypothesize that, beyond their direct contribution to predator escape, these wing patterns can be used as signals of escape abilities by predators, resulting in positive frequency-dependent selection favouring convergence in wing pattern in sympatry. To test this hypothesis, we quantified dorsal wing pattern variations of 723 butterflies from the three species sampled throughout their distribution, including sympatric and allopatric situations and compared the phenotypic distances between species, sex and localities. We detected a significant effect of localities on colour pattern, and higher inter-specific resemblance in sympatry as compared to allopatry, consistent with the hypothesis of local convergence of wing patterns. Our results provide some support to the existence of escape mimicry in the wild and stress the importance of estimating trait variation within species to understand trait variation between species, and to a larger extent, trait diversification at the macro-evolutionary scale.

evolutionary biology↗

Limited plasticity of Drosophila suzukii wing spot size in response to developmental temperature

Phenotypic plasticity is an important mechanism allowing adaptation to new environments and as such it has been suggested to facilitate biological invasions. Under this assumption, invasive populations are predicted to exhibit stronger plastic responses than native populations. Drosophila suzukii is an invasive species whose males harbor a spot on the wing tip. In this study, by manipulating developmental temperature, we compare the phenotypic plasticity of wing spot size of two invasive populations with that of a native population. We then compare the results with data obtained from wild-caught flies from different natural populations. While both wing size and spot size are plastic to temperature, no difference in plasticity was detected between native and invasive populations, rejecting the hypothesis of a role of the wing-spot plasticity in the invasion success. In contrast we observed a remarkable stability in the spot-to-wing ratio across temperatures, as well as among geographic populations. This stability suggests either that the spot relative size is under stabilizing selection, or that its variation might be constrained by a tight developmental correlation between spot size and wing size. Our data show that this correlation was lost at high temperature, leading to an increased variation in the relative spot size, particularly marked in the two invasive populations. This suggests (i) that D. suzukiis development is impaired by hot temperatures, in agreement with the cold-adapted status of this species; (ii) that the spot size can be decoupled from wing size, rejecting the hypothesis of an absolute constraint and suggesting that the wing color pattern might be under stabilizing (sexual) selection; (iii) that such sexual selection might be relaxed in the invasive populations. Finally, a subtle but consistent directional asymmetry in spot size was detected in favor of the right side in all populations and temperatures, possibly indicative of a lateralized sexual behavior.

ecology↗

Limited thermal plasticity and geographic divergence in the ovipositor of Drosophila suzukii

Phenotypic plasticity has been repeatedly suggested to facilitate adaptation to new environmental conditions, as in invasions. Here we investigate this possibility by focusing on the worldwide invasion of Drosophila suzukii: an invasive species that has rapidly colonized all continents over the last decade. This species is characterized by a highly developed ovipositor, allowing females to lay eggs through the skin of ripe fruits. Using a novel approach based on the combined use of SEM and photogrammetry, we quantified the ovipositor size and 3D shape, contrasting invasive and native populations raised at three different developmental temperatures. We found a small but significant effect of temperature and geographic origin on the ovipositor shape, showing the occurrence of both geographic differentiation and plasticity to temperature. The shape reaction norms are in turn strikingly similar among populations, suggesting very little difference in shape plasticity among invasive and native populations, and therefore rejecting the hypothesis of a particular role for plasticity of the ovipositor in the invasion success. Overall, the ovipositor shape seems to be a fairly robust trait, indicative of stabilizing selection. The large performance spectrum rather than the flexibility of the ovipositor would thus contribute to the success of D. suzukii worldwide invasion.

developmental biology↗