Search bioRxiv⌕ Search

Biology subjects

Llaurens, V.

Publications and source records attributed to Llaurens, 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↗

Do tropical birds avoid evasive prey? An experimental study in Ecuadorian avian communities

The effect of predator behaviours on the evolution of colour pattern has been extensively studied in chemically defended prey but much less so in evasive prey, although similar selection regimes might be at play. Most previous work on the recognition and learning of colour patterns by predators has relied on experiments with few model predator species, preventing a proper assessment of how natural predator communities shape the evolution of prey signals. Here, we investigate predation on evasive iridescent blue Morpho helenor butterflies by wild avian communities in a tropical forest, using artificial butterflies exposed to natural bird assemblages attracted to insect-light traps in the field. We presented five prey types: evasive (local and exotic Morpho), cryptic, palatable-control and unpalatable-control. We recorded attacks from 43 different bird species, and compared attack latency, attack order and predation exerted by different birds on different prey types. Most birds avoided evasive and defended prey, but attack responses differed depending on their levels of specialization towards insect prey. Avoidance of conspicuous coloured prey was more prevalent in specialist flight-feeding, invertivorous birds, whereas more opportunistic treehunter and frugivorous guilds had weaker discrimination. Exotic and local evasive iridescent blue Morphos experienced similar predation rates, suggesting a generalization of iridescent blue signals associated with evasiveness by most birds. Finally, contrasting selection on ventral vs. dorsal patterns was detected in M. helenor, where cryptic ventral surfaces were exposed to attack by ground-foraging birds, whereas conspicuous iridescent blue coloration displayed during flight is associated with reduced attack rates. By revealing potential differences in the responses of specialist and generalist predators, this study highlights the importance of accounting for diversity of predator traits and behaviours when investigating the evolution of aposematism, mimicry, and other anti-predator adaptations.

evolutionary biology↗

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↗

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↗

Evolution of divergent daily temporal niches shaped by male-male competition can generate sympatric speciation

Specialisation into different ecological niches is assumed as an important driver of speciation in sympatry. Here we focused on male-male competition fuelling population divergence, without assuming any ecological specialisation. We investigated how antagonistic interactions between males can promote divergent evolution of timings of reproductive activities during the day, as observed in some closely-related insect species living in sympatry. We used a multi-locus, comprehensive stochastic model to investigate the evolution of (1) the timing of reproductive activity as a quantitative trait and (2) neutral loci that may generate genetic incompatibilities among divergent individuals. We specifically explore how male-male competition for female access can generate negative frequency-dependence on the timing of reproductive activities and fuel population divergence. Our simulations in finite populations highlight the strong effect of male-male competition and operational sex-ratio on the evolution of divergent temporal niches. They also show how genetic incompatibilities promote the differentiation among populations with divergent temporal niches, but may also impair their co-existence. Our model therefore highlights male-male competition as an important factor shaping the evolution of diel niches, that may fuel sympatric speciation.

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↗

Time-dependent effects of species interactions at macroevolutionary scale shape the diversity of mimetic butterflies.

Evidence that species interactions can affect macroevolutionary dynamics of trait and species diversification is scarce. Mutualistic Mullerian mimicry is a compelling example of example of ecological interactions that has been shown to drive evolutionary convergence, Here, we test how mutualistic Mullerian mimicry shapes macroevolutionary patterns of diversification in the Ithomiini butterflies. We show that the age of color patterns is the primary determinant of species richness within mimicry rings but not phylogenetic diversity. We find pervasive phylogenetic signal in mimicry rings and in color patterns associated within polymorphic species. Only a small set of mimicry rings show high phylogenetic diversity. We identify patterns of saturation in the accumulation of new mimicry rings and in the number of evolutionary convergences towards the most species-rich mimicry rings. Those saturation patterns are likely caused by niche filling along various ecological dimensions, within and among the mimetic communities living in sympatry. The time-dependent effects detected in our study illustrate how neutral processes and ecological interactions interact and shape species and phenotypic diversification.

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↗

Influence of sex-limited mimicry on extinction risk in Aculeata: a theoretical approach.

AO_SCPLOWBSTRACTC_SCPLOWPositive ecological interactions can play a role in community structure and species co-existence. A well-documented case of mutualistic interaction is Mullerian mimicry, the convergence of colour pattern in defended species living in sympatry. By reducing predation pressure, Mullerian mimicry may limit local extinction risks of defended species, but this positive effect can be weakened by undefended mimics (Batesian mimicry). While mimicry was well-studied in neotropical butterflies, it remains surprisingly poorly studied in wasps and bees (Hymenoptera: Aculeata). However, only females are defended in Aculeata and this female-limited defence may modulate the effect of Mullerian mimicry on extinction risks. Here, we focus on the effect of Mullerian mimicry on extinction risk in Aculeata, using a population dynamics model for two species. We show that Mullerian mimicry has a positive effect on species co-existence, but this effect depends on the sex-ratio. We found that the probability of extinction increases as the proportion of undefended males increases in the population, however co-existence still occurs if females are sufficiently abundant or noxious. Furthermore, we detected a destabilising effect of dual sex-limited mimicry (when each sex resembles a different model) on species co-existence. In a context of massive population decline caused by anthropic activities, our findings highlight the potential importance of Mullerian mimicry as an overlooked mechanism linked to extinction risk in wasp and bee species.

ecology↗

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↗

Origin and persistence of polymorphism in loci targeted by disassortative preference: a general model

The emergence and persistence of polymorphism within populations generally requires specific selective regimes. Here, we develop an unifying theoretical framework to explore how disassortative mating can generate and maintain polymorphism at the targeted loci. To this aim, we model the dynamics of alleles at a single locus A in a population of haploid individuals, where reproductive success depends on the combination of alleles carried by the parents at locus A. Our theoretical study of the model confirms that the conditions for the persistence of a given level of allelic polymorphism depend on the relative reproductive advantages among pairs of individuals. Interestingly, equilibria with unbalanced allelic frequencies were shown to emerge from successive introduction of mutants.We then investigate the role of the function linking allelic divergence to reproductive advantage on the evolutionary fate of alleles within population. Our results highlight the significance of the shape of this function on both the number of alleles maintained and their level of genetic divergence. Large number of alleles are maintained with substantial turn-over among alleles when disassortative advantage slowly increases when allelic differentiation becomes large. In contrast, few highly differentiated alleles are predicted to be maintained when genetic differentiation has a strong effect on disassortative advantage. These opposite effects predicted by our model shed light on the levels of allelic differentiation and polymorphism empirically observed in loci targeted by disassortative mate choice.

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↗

The limits of evolutionary convergence in sympatry: reproductive interference and developmental constraints leading to local diversity in aposematic signals

Mutualistic interactions between defended species represent a striking case of evolutionary convergence in sympatry, driven by the increased protection against predators brought by mimicry in warning traits. However, such convergence is often limited: sympatric defended species frequently display different or imperfectly similar warning traits. The phylogenetic distance between sympatric species may indeed prevent evolution towards the exact same signal. Moreover, warning traits are also involved in mate recognition, so that trait convergence might result in heterospecific courtship and mating. Here, we develop a mathematical model to investigate the strength and direction of evolution of warning trait in defended species with different ancestral traits. Specifically, we determine the effect of phenotypic distances between ancestral trait states of sympatric defended species and of costs of heterospecific sexual interactions on imperfect mimicry and trait divergence. Our analytical results confirm that reproductive interference and historical constraints limit the convergence of warning traits, leading to either complete divergence, or imperfect mimicry. Our model reveals that imperfect mimicry evolves only when ancestral trait values differ between species due to historical constraints and highlights the importance of female and predator discriminations in the evolution of such imperfect mimicry. Our study thus provides new predictions on how reproductive interference interacts with historical constraints and may promote the emergence of novel warning traits, enhancing mimetic diversity.

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↗

When do opposites attract? A model uncovering the evolution of disassortative mating

Disassortative mating is a rare form of mate preference that promotes the persistence of polymorphism. While the evolution of assortative mating, and its consequences on trait variation and speciation have been extensively studied, the conditions enabling the evolution of disassortative mating are still poorly understood. Mate preferences increase the risk of missing mating opportunities, a cost that can be compensated by a greater fitness of offspring. Heterozygote advantage should therefore promote the evolution of disassortative mating, which maximizes the number of heterozygous offspring. From the analysis of a two-locus diploid model, with one locus controlling the mating cue under viability selection and the other locus coding for the level of disassortative preference, we show that heterozygote advantage and negative frequency-dependent viability selection acting at the cue locus promote the fixation of disassortative preferences. The conditions predicted to enable the evolution of disassortative mating in our model match the selection regimes acting on traits subject to disassortative mating behavior in the wild. In sharp contrast with the evolution of assortative preferences, we also show that disassortative mating generates a negative frequency-dependent sexual selection, which in turn disadvantages heterozygotes at the cue locus, limiting the evolution of disassortative preferences. This negative feedback loop could explain why this behavior is rare in natural populations.

evolutionary biology↗

Mutation accumulation in chromosomal inversions maintains wing pattern polymorphism in a butterfly

While natural selection favours the fittest genotype, polymorphisms are maintained over evolutionary timescales in numerous species. Why these long-lived polymorphisms are often associated with chromosomal rearrangements remains obscure. Combining genome assemblies, population genomic analyses, and fitness assays, we studied the factors maintaining multiple mimetic morphs in the butterfly Heliconius numata. We show that the polymorphism is maintained because three chromosomal inversions controlling wing patterns express a recessive mutational load, which prevents their fixation despite their ecological advantage. Since inversions suppress recombination and hamper genetic purging, their formation fostered the capture and accumulation of deleterious variants. This suggests that many complex polymorphisms, instead of representing adaptations to the existence of alternative ecological optima, could be maintained primarily because chromosomal rearrangements are prone to carrying recessive harmful mutations.

evolutionary biology↗

Artificial selection on male size depletes genetic variance but not covariance of life history traits in the yellow dung fly

The evolutionary potential of organisms depends on the presence of sufficient genetic variation for traits subject to selection, as well as on the genetic covariances among them. While genetic variation ultimately derives from mutation, theory predicts the depletion of genetic (co)variation under consistent directional or stabilizing selection in natural populations. We estimated and compared additive genetic (co)variances for several standard life history traits, including some for which this has never been assessed, before and after 24 generations of artificial selection on male size in the yellow dung fly Scathophaga stercoraria (Diptera: Scathophagidae) using a series of standard half-sib breeding experiments. As predicted, genetic variances (VA), heritabilities (h2) and evolvabilities (IA) of body size, development time, first clutch size, and female age at first clutch were lower after selection. As independent selection lines were crossed prior to testing, we can rule out that this reduction is due to genetic drift. In contrast to the variances, and against expectation, the additive genetic correlations between the sexes for development time and body size remained strong and positive (rA = 0.8-0.9), while the genetic correlation between these traits within the sexes tended to strengthen (but not significantly so). Our study documents that the effect of selection on genetic variance is predictable, whereas that on genetic correlations is not.

evolutionary biology↗