Biology subjects

Joron, M.

Publications and source records attributed to Joron, M..

At least 19 recordsLinked to original sources

bioRxiv2026

Contrasting signatures of interspecific gene flow in the Atlantic Forest endemic butterfly Heliconius besckei

Gene flow between diverging species can reshuffle genomic variation and greatly influence the speciation process, sometimes reinforcing, sometimes eroding species boundaries. However, the effect of ecological and historical processes on the patterns of introgression remains poorly understood. Here, we focus on the evolutionary history of Heliconius besckei, a geographically restricted butterfly endemic to the Brazilian Atlantic Forest, together with the mimetic H. melpomene nanna, the sympatric non-mimetic H. ethilla narcaea, and its closely related H. numata robigus. Using whole-genome sequencing, genome-wide tests of introgression, demographic modelling and palaeoclimatic species distribution models, we tested the extent and timing of interspecific gene flow in relation to mimicry, ecological context, and changes in geographic overlap. Despite strong genomic differentiation among the four focal Heliconius species, we detected widespread signatures of interspecific gene flow, greatly influenced by geographical overlap. Demographic models including post-divergence gene flow were better supported than strict-isolation models. In addition, genome-wide introgression analyses showed more numerous and larger candidate introgressed regions between H. besckei and H. ethilla narcaea, consistent with recurrent opportunities for exchange between these currently sympatric species. Species distribution models further recovered repeated expansions of suitable habitat for H. besckei during cold periods, providing a potential geographic context for secondary contact within the Atlantic Forest. Together, our results reveal recurrent gene flow occurring under different temporal, geographic, and potentially selective contexts, and show that the evolutionary history of a geographically restricted lineage can be shaped by repeated genetic exchange while substantial species differentiation is maintained.

evolutionary biology↗

bioRxiv2025

Rapid adaptation of an invasive species to climate at a local and continental scale revealed by citizen science

Rapid evolution and evolutionary rescue are key mechanisms modulating the success of invasive species, allowing to rapidly adapt to new conditions and to recover from a bottleneck after the introduction. Despite being a well-known mechanism overall, examples of rapid evolution from invasive species and on broad geographic ranges are poorly documented. The box tree moth (Cydalima perspectalis) is a polymorphic invasive species that recently colonized Europe, but the ecological factors driving the morph frequencies in natural populations are still largely unknown. Here we took advantage of citizen science, that allows for an unprecedented amount of observations across a large spatial scale, and pheromone trapping, for a more targeted sampling, to detect differences in morph ratios for our model species across Europe and Asia. We then fitted linear regressions and generalized mixed models to detect what variables in the invasive environment drive their frequencies. We found that the melanic form of this moth is maintained at intermediate frequencies in the entire range, but that both at the continental scale and at the local scale, its frequency is higher in warmer and drier conditions. This finding supports the hypothesis of a rapid evolution of colour polymorphism in this invasive species, that established the observed cline in roughly 27 generations. Finally, we provide a physiological rationale of the observed cline, using an experimental approach, showing that melanic individuals have a better resistance to desiccation, compatible with their higher frequency in warmer and drier climates.

evolutionary biology↗

bioRxiv2025

Perceptual maps reveal rampant convergence in butterfly wing patterns across the Neotropics

In 1879, Fritz Muller formulated the first mathematical evolutionary model to explain mutualistic mimicry between coexisting defended prey. Yet, whether local mimicry drives the structure of aposematic prey signals across their entire geographic distribution remains untested because the perception of pattern similarity has never been assessed at large spatial scale. Here, we implement a citizen science survey to map, throughout the Neotropics, variation in the wing patterns of heliconiine butterflies (Nymphalidae) as perceived by vertebrate cognitive systems. We show that despite a continuum of perceived similarity in wing patterns at the continental scale, the convergence of sympatric species into discrete mimicry rings is ubiquitous among local communities. These results expand Mullers historical predictions by quantifying the rampant convergence of prey signals across an entire continent.

evolutionary biology↗

bioRxiv2024

Draft genome and transcriptomic sequence data of three invasive insect species

Cydalima perspectalis (the box tree moth), Leptoglossus occidentalis (the western conifer seed bug), and Tecia solanivora (the Guatemalan tuber moth) are three economically harmful invasive insect species. This study presents their genomic and transcriptomic sequences, generated through whole- genome sequencing, RNA-seq transcriptomic data, and Hi-C sequencing. The resulting genome assemblies exhibit good quality, providing valuable insights into these species. The genome sizes are 500.4 Mb for C. perspectalis, 1.74 Gb for L. occidentalis, and 623.3 Mb for T. solanivora. These datasets are available in the NCBI Sequence Read Archive (BioProject PRJNA1140410) and serve as essential resources for population genomics studies and the development of effective pest management strategies, addressing significant gaps in the understanding of invasive insect species.

genomics↗

bioRxiv2024

Untangling the contribution of adaptive versus non-adaptive processes in the evolution of reproductive isolation between Coenonympha butterflies.

Speciation is a key evolutionary process which has been studied in numerous organisms and at multiple scales, from lineage radiation to gene expression. However, the factors explaining the rise of new species are not yet fully understood, and the relative contribution of neutral versus selective evolutionary processes in triggering and maintaining reproductive isolation between lineages is still debated. To explore this question, we study the divergence of two butterfly species, Coenonympha arcania and C. gardetta (Nymphalidae), which diverged relatively recently but show strong ecological differences. Whole genome sequence data reveal high overall differentiation between the two lineages, best explained by a long period of isolation at the early stage of their divergence. Demographically explicit approaches identify that 6.6% of the genome (32.7 Mbp) is impermeable to gene flow between the two species. Lots of these barrier loci are located on the Z chromosome, potentially spanning 75% of its length which would indicate that a large Z effect is at play in this speciation. Moreover, only a small proportion of barriers showed signatures of selection, suggesting that non-adaptive processes largely contributed to the build-up of reproductive isolation. Therefore, although genes involved in stress response and response to hypoxia are interesting candidates under selection, the adaptation of C. gardetta to alpine conditions may not to be the main driver of speciation. Our study brings an original example of intertwined adaptive and non-adaptive processes leading to reproductive isolation in a speciation with secondary contact and improves our understanding of the genomic underpinnings of species divergence.

evolutionary biology↗

bioRxiv2023

Positive and negative frequency-dependent selection acting on polymorphism in a palatable moth

Camouflage and warning signals are contrasted prey strategies reducing predator attack, which offer an excellent opportunity to study the evolutionary forces acting on prey appearance. Edible prey are often inconspicuous and escape predation by remaining undetected. Predators learn to find the most common ones, leading to apostatic selection (advantage to rare morphs) enhancing variation in cryptic prey. By contrast, defended prey are often conspicuous and escape predation by using warning colorations identifying them as unprofitable. Predators avoid the ones they are most familiar with, leading to positive frequency-dependence and warning signal uniformity. It is less clear, however, what happens when two morphs of the same species vary strongly in conspicuousness, and how to explain the maintenance of cryptic and conspicuous morphs within populations, in the case of profitable prey. Using the white and melanic morphs of the invasive Box Tree Moth (Cydalima perspectalis) presented at three different frequencies, we investigate whether a) caterpillars and adult moths are palatable for birds, b) the less conspicuous, melanic morph experiences lower predation rates and b) whether frequency-dependence balances morph frequencies. Our results suggest that the melanic morph enjoys a survival advantage owing to a lower visibility. However, our experiments show that, unexpectedly, the two color morphs experience opposite patterns of frequency-dependent predation, despite being both fully palatable to birds. The melanic morph is under apostatic selection, whereas the conspicuous, white morph is subject to positive frequency-dependence (safety in numbers). Our experiments also show some level of unpalatability in the caterpillars. These results offer novel insight into how predation triggers contrasting evolutionary patterns in a palatable, polymorphic species within two morphs that differ markedly in conspicuousness and within two different life stages. Lay summaryUnderstanding the factors influencing character variation in natural populations is a key question in evolutionary ecology. Predation is one of the main drivers of color evolution in prey communities and prey usually mitigate predation using camouflage or warning colors. Camouflage evolves because it lowers the probability of being detected by predators. Since predators are more efficient at finding prey which they are familiar with, prey which display a rare phenotype are favoured (negative frequency-dependent selection). By contrast, aposematism is defined by conspicuous appearance in toxic or otherwise unprofitable prey, and evolves because birds identify defended prey by learning to use their appearance as a warning signal. The most common signals are usually best identified and avoided (positive-frequency dependent selection). It is not clear, however, how these two forces combine when predators are facing cryptic and conspicuous morphs of the same species, and how to explain their coexistence. Here we investigate this question in a laboratory experiment, by presenting wild birds with a melanic and a white morph of the same moth. Unexpectedly, our results show that despite being both fully palatable to birds, the two color morphs are subject to very different types of selection depending on their frequencies. The melanic morph is favored when it is rare, the conspicuous white morph as it gets common. The simultaneous action of these forces may contribute to maintain color polymorphism in natural populations. We also show that caterpillars of this species are unpalatable and chemically defended, whereas adults are not, showing opposite strategies of predator defense in different life stages of the same species.

evolutionary biology↗

bioRxiv2022

Subtle introgression footprints at the end of the speciation continuum in a clade of Heliconius butterflies

Quantifying gene flow between lineages at different stages of the speciation continuum is central to understanding speciation. Heliconius butterflies have undergone an adaptive radiation in wing colour patterns driven partly by natural selection for local mimicry. Colour patterns are also known to be used as assortative mating cues. Therefore, wing pattern divergence is considered to play a role in speciation. A corollary is that mimicry between closely-related species may be associated with hybridization and interfere with reproductive isolation. Here, we take a multifaceted approach to explore speciation history, species boundaries, and traits involved in species differentiation between the two closely-related species H. hecale and H. ismenius. We focus on geographic regions where the two species mimic each other, and contrast this with geographic regions where they do not mimic each other. To examine population history and patterns of gene flow, we tested and compared a four-population model accounting for linked selection. This model suggests that the two species have remained isolated for a large part of their history, yet with a small amount of gene exchange. Accordingly, signatures of genomic introgression were small except at a major wing pattern allele and chemosensing genes, and stronger in the mimetic populations compared to non-mimetic populations. Behavioural assays confirm that visual confusion exists but that short-range cues determine strong sexual isolation. Tests for chemical differentiation between species identified major differences in putative pheromones which likely mediate mate choice and the maintenance of species differences.

evolutionary biology↗

bioRxiv2021

Dissecting supergene: evidence for recombination suppression among multiple functional loci within inversions.

Supergenes are genetic architectures associated with discrete and concerted variation in multiple traits. It has long been suggested that supergenes control these complex polymorphisms by suppressing recombination between set of coadapted genes. However, because recombination suppression hinders the dissociation of the individual effects of genes within supergenes, there is still little evidence that supergenes evolve by tightening linkage between coadapted genes. Here, combining an landmark-free phenotyping algorithm with multivariate genome wide association studies, we dissected the genetic basis of wing pattern variation in the butterfly Heliconius numata. We showed that the supergene controlling the striking wing-pattern polymorphism displayed by this species contains many independent loci associated with different features of wing patterns. The three chromosomal inversions of this supergene suppress recombination between these loci, supporting the hypothesis that they may have evolved because they captured beneficial combinations of alleles. Some of these loci are associated with colour variations only in morphs controlled by inversions, indicating that they were recruited after the formation of these inversions. Our study shows that supergenes and clusters of adaptive loci in general may form via the evolution of chromosomal rearrangements suppressing recombination between co-adapted loci but also via the subsequent recruitment of linked adaptive mutations.

evolutionary biology↗

bioRxiv2021

Supergene formation is associated with a major shift in genome-wide patterns of diversity in a butterfly

Selection shapes genetic diversity around target mutations, yet little is known about how selection on specific loci affects the genetic trajectories of populations, including their genome-wide patterns of diversity and demographic responses. Here we study the patterns of genetic variation and geographic structure in a neotropical butterfly, Heliconius numata, and its closely related allies in the so-called melpomene-silvaniform clade. H. numata is known to have evolved an inversion supergene which controls variation in wing patterns involved in mimicry associations with distinct groups of co-mimics whereas it is associated to disassortative mate preferences and heterozygote advantage at this locus. We contrasted patterns of genetic diversity and structure 1) among extant polymorphic and monomorphic populations of H. numata, 2) between H. numata and its close relatives, and 3) between ancestral lineages. We show that H. numata populations which carry the inversions as a balanced polymorphism show markedly distinct patterns of diversity compared to all other taxa. They show the highest genetic diversity and effective population size estimates in the entire clade, as well as a low level of geographic structure and isolation by distance across the entire Amazon basin. By contrast, monomorphic populations of H. numata as well as its sister species and their ancestral lineages all show lower effective population sizes and genetic diversity, and higher levels of geographical structure across the continent. One hypothesis is that the large effective population size of polymorphic populations could be caused by the shift to a regime of balancing selection due to the genetic load and disassortative preferences associated with inversions. Testing this hypothesis with forward simulations supported the observation of increased diversity in populations with the supergene. Our results are consistent with the hypothesis that the formation of the supergene triggered a change in gene flow, causing a general increase in genetic diversity and the homogenisation of genomes at the continental scale.

evolutionary biology↗

bioRxiv2020

Admixture can readily lead to the formation of supergenes

Supergenes are genetic architectures allowing the segregation of alternative combinations of alleles underlying complex phenotypes. The co-segregation of sets of alleles at linked loci is determined by polymorphic chromosomal rearrangements suppressing recombination locally. Supergenes are involved in many complex polymorphisms, including sexual, color or behavioral polymorphisms in numerous plants, fungi, mammals, fish, and insects. Despite a long history of empirical and theoretical research, the genetic origin of supergenes remains poorly understood. Here, using a population genetic two-island model, we explore how the evolution of overdominant chromosomal inversions may lead to the formation of supergenes. We show that the evolution of inversions in differentiated populations connected by gene flow leads to an increase in frequency of poorly adapted, immigrant haplotypes. When inversions are associated with recessive fitness cost hampering their fixation (such as a mutational load), this results in the formation of supergenes. These results provide a realistic scenario for the evolution of supergenes and inversion polymorphisms in general, and bring new light into the importance of admixture in the formation of new genetic architectures.

evolutionary biology↗

bioRxiv2020

Costly mate preferences can promote reproductive isolation along ecological gradients

Species often replace each other spatially along contact zones, giving scope for parapatric speciation. In models of parapatric speciation driven by assortative mating, costs of female choosiness have so far be ignored. Yet, if females encounter only a limited number of males, those that are too choosy may remain unmated, and this should create direct sexual selection against choosiness. In our individual-based model of parapatric ecological speciation, disruptive viability selection leads to divergence of an ecological trait. Additionally, female choosiness (following a matching mating rule based on the same ecological trait) can evolve at the risk of remaining unmated, and can limit gene flow between diverging populations. In line with previous litterature, out of the contact zone, the evolution of cost-free choosiness stops at intermediate values due to indirect selection against strong choosiness. Here we show that a weak cost of choosiness, by modifying genotypic frequencies on which viability selection acts, reduces this selection pressure, thus permitting the evolution of stronger choosiness than in the absence of costs. In strong contrast to sympatric models, costs of choosiness can therefore promote reproductive isolation in parapatry.

evolutionary biology↗

bioRxiv2020

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↗

bioRxiv2019

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↗

bioRxiv2019

Classic and introgressed selective sweeps shape mimicry loci across a butterfly adaptive radiation

Natural selection leaves distinct signatures in the genome that can reveal the targets and history of adaptive evolution. By analysing high-coverage genome sequence data from four major colour pattern loci sampled from nearly 600 individuals in 53 populations, we show pervasive selection on wing patterns across the Heliconius adaptive radiation. The strongest signatures correspond to loci with the greatest phenotypic effects, consistent with visual selection by predators, and are found in colour patterns with geographically restricted distributions. These recent sweeps are similar between co-mimics and indicate colour pattern turn-over events despite strong stabilizing selection. Using simulations we compare sweep signatures expected under classic hard sweeps with those resulting from adaptive introgression, an important aspect of mimicry evolution in Heliconius. Simulated recipient populations show a distinct volcano pattern with peaks of increased genetic diversity around the selected target, consistent with patterns found in some populations. Our genomic data provide unprecedented insights into the recent history of selection across the Heliconius adaptive radiation.

evolutionary biology↗

bioRxiv2019

How heterozygote advantage can promote the evolution of disassortative mating and shape the underlying geneticarchitecture?

The evolution of mate preferences may depend on natural selection acting on the mating cues and on the underlying genetic architecture. While the evolution of assortative mating with respect to locally adapted traits has been well-characterized, the evolution of disassortative mating is poorly characterized. Here we aim at understanding the evolution of disassortative mating for traits under strong balancing selection, by focusing on polymorphic mimicry as an illustrative example. Positive frequency-dependent selection exerted by predators generates local selection on wing patterns acting against rare variants and promoting local monomorphism. This acts across species boundaries, favouring Mullerian mimicry among defended species. In this well-characterized adaptive landscape, polymorphic mimicry is rare but is observed in a butterfly species, associated with polymorphic chromosomal inversions. Because inversions are often associated with recessive deleterious mutations, we hypothesize they may induce heterozygote advantage at the color pattern locus, putatively favoring the evolution of disassortative mating. To explore the conditions underlying the emergence of disassortative mating, we modeled both a trait locus (colour pattern for instance), subject to mutational load, and a preference locus. We confirm that heterozygote advantage favors the evolution of disassortative mating and show that disassortative mating is more likely to emerge if at least one allele at the trait locus is free from any recessive deleterious mutations. We modelled different possible genetic architectures underlying mate choice behaviour, such as self referencing alleles, or specific preference or rejection alleles. Our results showed that self referencing or rejection alleles linked to the color pattern locus can be under positive selection and enable the emergence of disassortative mating. However rejection alleles allow the emergence of disassortative mating only when the color pattern and preference loci are tightly linked. Our results therefore provide relevant predictions on both the selection regimes and the genetic architecture favoring the emergence of disassortative mating and a theoretical framework in which to interprete empirical data on mate preferences in wild populations.

evolutionary biology↗

bioRxiv2018

Genomic architecture and introgression shape a butterfly radiation

We here pioneer a low-cost assembly strategy for 20 Heliconiini genomes to characterize the evolutionary history of the rapidly radiating genus Heliconius. A bifurcating tree provides a poor fit to the data, and we therefore explore a reticulate phylogeny for Heliconius. We probe the genomic architecture of gene flow, and develop a new method to distinguish incomplete lineage sorting from introgression. We find that most loci with non-canonical histories arose through introgression, and are strongly underrepresented in regions of low recombination and high gene density. This is expected if introgressed alleles are more likely to be purged in such regions due to tighter linkage with incompatibility loci. Finally, we identify a hitherto unrecognized inversion, and show it is a convergent structural rearrangement that captures a known color pattern switch locus within the genus. Our multi-genome assembly approach enables an improved understanding of adaptive radiation.

evolutionary biology↗

bioRxiv2018

Genome-wide admixture is common across the Heliconius radiation

How frequent is gene flow between species? The pattern of evolution is typically portrayed as a phylogenetic tree, implying that speciation is a series of splits between lineages. Yet gene flow between good species is increasingly recognized as an important mechanism in the diversification of radiations, often spreading adaptive traits and leading to a complex pattern of phylogenetic incongruence. This process has thus far been studied in cases involving few species, or geographically restricted to spaces like islands, but not on the scale of a continental radiation. Previous studies have documented gene flow, adaptive introgression and hybrid speciation in a small subsection of the charismatic Neotropical butterflies Heliconius. Using genome-wide resequencing of 40 out of 45 species in the genus we demonstrate for the first time that admixture has played a role throughout the evolution of Heliconius and the sister genus Eueides. Modelling of phylogenetic networks based on 6848 orthologous autosomal genes (Maximum Pseudo-Likelihood Networks) or 5,483,419 high quality SNPs (Ancestral Recombination Graph) uncovers nine new cases of interspecific gene flow at up to half of the genome. However, f4 statistics of admixture show that the extent of the process has varied between subgenera. Evidence for introgression is found at all five loci controlling the colour and shape of the mimetic wing patterns, including in the putative hybrid species H. hecalesia, characterised by an unusual hindwing. Due to hybridization and incomplete coalescence during rapid speciation, individual gene trees show rampant discordance. Although reduced gene flow and faster coalescence are expected at the Z chromosome, we discover high levels of conflict between the 416 sex-linked loci. Despite this discordant pattern, both concatenation and multispecies coalescent approaches yield surprisingly consistent and fully supported genome-wide phylogenies. We conclude that the imposition of the bifurcating tree model without testing for interspecific gene flow may distort our perception of adaptive radiations and thus the ability to study trait evolution in a comparative framework.

evolutionary biology↗

bioRxiv2018

Generalisation behaviour of predators toward warning signals displayed by harmful prey: answers from a video-game played by humans.

The persistence of several warning signals in sympatry is a puzzling evolutionary question because selection favours convergence of colour patterns among toxic species. Such convergence is shaped by predators reaction to similar but not identical stimulus, i.e. generalisation behaviour. However, studying generalisation behaviour in complex natural communities of predators is challenging, and is thus generally limited to simple variations of prey colour patterns. Here, we used humans as surrogate predators to investigate generalisation behaviours on two prey communities with different level of warning signals complexity. Humans generalisation capacities were estimated using a computer game simulating a simple (4 morphs) and a complex (10 morphs) community of defended (associated with a penalty) and palatable butterflies. Colour patterns used in the game are actually observed in natural populations of the defended butterflies H. numata, and generalisation behaviour of natural predators communities on these colour patterns have previously been investigated in the wild, allowing direct comparison with human behaviour. We investigated human predation behaviour by recording attack rates on the different defended and palatable colour patterns, as well as player survival time (i.e. score). Phenotypic similarity among the different colour patterns was precisely quantified using a custom algorithm accounting for both colour and pattern variations (CPM method). By analysing attack behaviours of 491 game players, we found that learning was more efficient in the simple prey community. Additionally, profitable prey gained protection from sharing key visual features with unprofitable prey in both communities while learning, in accordance with natural predator behaviours. Moreover, other behaviours observed in natural predators, such as colour neophobia, were detected in humans and shaped morph vulnerability during the game. Similarities between our results in humans and the reaction of natural predator communities to the same colour patterns validate our video-game as a useful proxy to study predator behaviour. This experimental set-up can thus be compared to natural systems, enabling further investigations of generalisation on mimicry evolution.

evolutionary biology↗