Which cues are sexy? The evolution of mate preference in sympatric species reveals the contrasted effect of adaptation and reproductive interference.

Mate preferences may target traits (a) enhancing offspring adaptation and (b) reducing heterospecific matings. Because similar selective pressures are acting on traits shared by different sympatric species, preference-enhancing offspring adaptation may increase heterospecific mating, in sharp contrast with the classical case of so-called "magic traits." Using a mathematical model, we study which and how many traits will be used during mate choice, when preferences for locally adapted traits increase heterospecific mating. In particular, we study the evolution of preference toward an adaptive versus a neutral trait in sympatric species. We take into account sensory trade-offs, which may limit the emergence of preference for several traits. Our model highlights that the evolution of preference toward adaptive versus neutral traits depends on the selective regimes acting on traits but also on heterospecific interactions. When the costs of heterospecific interactions are high, mate preference is likely to target neutral traits that become a reliable cue limiting heterospecific matings. We show that the evolution of preference toward a neutral trait benefits from a positive feedback loop: The more preference targets the neutral trait, the more it becomes a reliable cue for species recognition. We then reveal the key role of sensory trade-offs and the cost of choosiness favoring the evolution of preferences targeting adaptive traits, rather than traits reducing heterospecific mating. When sensory trade-offs and the cost of choosiness are low, we also show that preferences targeting multiple traits evolve, improving offspring fitness by both transmitting adapted alleles and reducing heterospecific mating. Altogether, our model aims at reconciling "good gene" and reinforcement models to provide general predictions on the evolution of mate preferences within natural communities.

A colourful duplication.

A genetic duplication event during evolution allowed male wood tiger moths to have either yellow or white patterns on their wings.

Convergence in sympatric swallowtail butterflies reveals ecological interactions as a key driver of worldwide trait diversification.

Ecological interactions can promote phenotypic diversification in sympatric species. While competition can enhance trait divergence, other ecological interactions may promote convergence in sympatric species. Within butterflies, evolutionary convergences in wing color patterns have been reported between distantly related species, especially in females of palatable species, where mimetic color patterns are promoted by predator communities shared with defended species living in sympatry. Wing color patterns are also often involved in species recognition in butterflies, and divergence in this trait has been reported in closely related species living in sympatry as a result of reproductive character displacement. Here, we investigate the effect of sympatry between species on the convergence vs. divergence of their wing color patterns in relation to phylogenetic distance, focusing on the iconic swallowtail butterflies (family Papilionidae). We developed an unsupervised machine learning-based method to estimate phenotypic distances among wing color patterns of 337 species, enabling us to finely quantify morphological diversity at the global scale among species and allowing us to compute pairwise phenotypic distances between sympatric and allopatric species pairs. We found phenotypic convergence in sympatry, stronger among distantly related species, while divergence was weaker and restricted to closely related males. The convergence was stronger among females than males, suggesting that differential selective pressures acting on the two sexes drove sexual dimorphism. Our results highlight the significant effect of ecological interactions driven by predation pressures on trait diversification in Papilionidae and provide evidence for the interaction between phylogenetic proximity and ecological interactions in sympatry, acting on macroevolutionary patterns of phenotypic diversification.

The Limits of Evolutionary Convergence in Sympatry: Reproductive Interference and Historical Constraints Leading to Local Diversity in Warning Traits.

AbstractMutualistic 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 toward the exact same signal. Moreover, warning traits are also involved in mate recognition, so trait convergence might result in heterospecific courtship and mating. Here, we develop a mathematical model to investigate the strength and direction of the evolution of warning traits 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 the 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 because of historical constraints and highlights the importance of female and predator discrimination 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.

Patterns of morphological variation highlight the effect of natural selection on eyespots modularity in the butterfly Morpho telemachus.

Morphological correlations can not only stem from developmental constraints but also from selective pressures. Butterfly eyespots are repeated wing color pattern elements, widespread across species. As developmental serial homologs, they are controlled by similar developmental pathways imposing correlations among eyespots: selection on a single eyespot may induce correlated responses in all eyespots. We study the variations in the ventral eyespots of Morpho telemachus, where two different selective regimes are likely to act: while most eyespots are always-visible, two eyespots are conditionally displayed: hidden at rest, they can be exposed when the butterflies are threatened, or during sexual interactions. We investigate how such contrasted selection across eyespots can alter the covariations imposed by their shared developmental origin. We quantified eyespots covariations within a large population of M. telemachus and compared the observed patterns to those found in M. helenor, where all eyespots are always-visible and thus probably affected by a similar selection regime. We found that M. telemachus conditionally displayed eyespots are less variable than always-visible eyespots and that these two eyespots form a separate variational module in this species, in contrast to M. helenor. Our results suggest that eyespots covariations were shaped by selection, highlighting how natural selection may promote the evolution of modularity.

Dominance mechanisms in supergene alleles controlling butterfly wing pattern variation: insights from gene expression in Heliconius numata.

Loci under balancing selection, where multiple alleles are maintained, offer a relevant opportunity to investigate the role of natural selection in shaping genetic dominance: the high frequency of heterozygotes at these loci has been shown to enable the evolution of dominance among alleles. In the butterfly Heliconius numata, mimetic wing color variations are controlled by an inversion polymorphism of a circa 2 Mb genomic region (supergene P), with strong dominance between sympatric alleles. To test how differences in dominance observed on wing patterns correlate with variations in expression levels throughout the supergene region, we sequenced the complete transcriptome of heterozygotes at the prepupal stage and compared it to corresponding homozygotes. By defining dominance based on non-overlapping ranges of transcript expression between genotypes, we found contrasting patterns of dominance between the supergene and the rest of the genome; the patterns of transcript expression in the heterozygotes were more similar to the expression observed in the dominant homozygotes in the supergene region. Dominance also differed among the three subinversions of the supergene, suggesting possible epistatic interactions among their gene contents underlying dominance evolution. We found the expression pattern of the melanization gene cortex located in the P-region to predict wing pattern phenotype in the heterozygote. We also identify new candidate genes that are potentially involved in mimetic color pattern variations highlighting the relevance of transcriptomic analyses in heterozygotes to pinpoint candidate genes in non-recombining regions.

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 regimes of natural or sexual selection. Here, we develop a unified theoretical framework to explore how polymorphism at targeted loci can be generated and maintained by either disassortative mating choice or balancing selection due to, for example, heterozygote advantage. 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 the population. Our results highlight the significance of the shape of this function for both the number of alleles maintained and their level of genetic divergence. Large number of alleles are maintained with substantial replacement of alleles, when disassortative advantage slowly increases with allelic differentiation . 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 explain how disassortative mate choice may lead to various levels of allelic differentiation and polymorphism, and shed light on the effect of mate preferences on the persistence of balanced and unbalanced polymorphism in natural population.

Evolutionary origins of sexual dimorphism: Lessons from female-limited mimicry in butterflies.

The striking female-limited mimicry observed in some butterfly species is a text-book example of sexually dimorphic trait submitted to intense natural selection. Two main evolutionary hypotheses, based on natural and sexual selection respectively, have been proposed. Predation pressure favoring mimicry toward defended species could be higher in females because of their slower flight, and thus overcome developmental constraints favoring the ancestral trait that limits the evolution of mimicry in males but not in females. Alternatively, the evolution of mimicry in males could be limited by female preference for non-mimetic males. However, the evolutionary origin of female preference for non-mimetic males remains unclear. Here, we hypothesize that costly sexual interactions between individuals from distinct sympatric species might intensify because of mimicry, therefore promoting female preference for non-mimetic trait. Using a mathematical model, we compare the evolution of female-limited mimicry when assuming either alternative selective hypotheses. We show that the patterns of divergence of male and female trait from the ancestral traits can differ between these selection regimes. We specifically highlight that divergence in female trait is not a signature of the effect of natural selection. Our results also evidence why female-limited mimicry is more frequently observed in Batesian mimics.

Divergence of climbing escape flight performance in Morpho butterflies living in different microhabitats.

Habitat specialization can influence the evolution of animal movement in promoting divergent locomotor abilities adapted to contrasting environmental conditions, differences in vegetation clutter or predatory communities. While the effect of habitat on the evolution of locomotion and particularly escape performance has been well investigated in terrestrial animals, it remains understudied in flying animals. Here, we investigated whether specialization of Morpho butterfly species into different vertical strata of the Amazonian forest affects the performance of upward escape flight manoeuvres. Using stereoscopic high-speed videography, we compared the climbing flight kinematics of seven Morpho species living either in the forest canopy or in the understory. We show that butterflies from canopy species display strikingly higher climbing speed and steeper ascent angle compared with understory species. Although climbing speed increased with wing speed and angle of attack, the higher climb angle observed in canopy species was best explained by their higher body pitch angle, resulting in more upward-directed aerodynamic thrust forces. Climb angle also scales positively with weight-normalized wing area, and this weight-normalized wing area was higher in canopy species. This shows that a combined divergence in flight behaviour and morphology contributes to the evolution of increased climbing flight abilities in canopy species.

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 (HW) tails in the swallowtail butterfly Iphiclides podalirius. In this species, HWs 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 standardized 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 HWs were struck more often than the rest of the body by birds. Finally, we characterized 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 HW tails and suggest that predation is an important selective driver of the evolution of wing tails and colour pattern in butterflies.

Genome assembly of 3 Amazonian Morpho butterfly species reveals Z-chromosome rearrangements between closely related species living in sympatry.

The genomic processes enabling speciation and species coexistence in sympatry are still largely unknown. Here we describe the whole-genome sequencing and assembly of 3 closely related species from the butterfly genus Morpho: Morpho achilles (Linnaeus, 1758), Morpho helenor (Cramer, 1776), and Morpho deidamia (Höbner, 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 color pattern, suggesting local mimicry. By sequencing, assembling, and annotating their genomes, we aim at uncovering prezygotic barriers preventing gene flow between these sympatric species. We found a genome size of  480 Mb for the 3 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 prezygotic isolation like genes controlling color discrimination (L-opsin). Altogether, the assembly and the annotation of these 3 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.

Convergent morphology and divergent phenology promote the coexistence of Morpho butterfly species.

The coexistence of closely-related species in sympatry is puzzling because ecological niche proximity imposes strong competition and reproductive interference. A striking example is the widespread wing pattern convergence of several blue-banded Morpho butterfly species with overlapping ranges of distribution. Here we perform a series of field experiments using flying Morpho dummies placed in a natural habitat. We show that similarity in wing colour pattern indeed leads to interspecific territoriality and courtship among sympatric species. In spite of such behavioural interference, demographic inference from genomic data shows that sympatric closely-related Morpho species are genetically isolated. Mark-recapture experiments in the two most closely-related species unravel a strong temporal segregation in patrolling activity of males. Such divergence in phenology reduces the costs of reproductive interference while simultaneously preserving the benefits of convergence in non-reproductive traits in response to common ecological pressures. Henceforth, the evolution of multiple traits may favour species diversification in sympatry by partitioning niche in different dimensions.

Adaptive evolution of flight in Morpho butterflies.

The diversity of flying animals suggests that countless combinations of flight morphologies and behaviors have evolved with specific lifestyles, thereby exploiting diverse aerodynamic mechanisms. How morphology, flight behavior, and aerodynamic properties together diversify with contrasting ecology remains to be elucidated. We studied the adaptive codivergence 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 modeling. 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 distinct combinations of flight behavior, wing shape, and aerodynamic mechanisms, highlighting the multiple pathways of adaptive evolution.

When Do Opposites Attract? A Model Uncovering the Evolution of Disassortative Mating.

AbstractDisassortative mating is a rare form of mate preference that promotes the persistence of polymorphism. While the evolution of assortative mating and its consequences for 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 evolution of disassortative preferences. We predict conditions of evolution of disassortative mating coherent with selection regimes acting on traits observed in the wild. We also show that disassortative mating generates sexual selection, which disadvantages heterozygotes at the cue locus, limiting the evolution of disassortative preferences. Altogether, our results partially explain why this behavior is rare in natural populations.

Foraging efficiency in temporally predictable environments: is a long-term temporal memory really advantageous?

Cognitive abilities enabling animals that feed on ephemeral but yearly renewable resources to infer when resources are available may have been favoured by natural selection, but the magnitude of the benefits brought by these abilities remains poorly known. Using computer simulations, we compared the efficiencies of three main types of foragers with different abilities to process temporal information, in spatially and/or temporally homogeneous or heterogeneous environments. One was endowed with a sampling memory, which stores recent experience about the availability of the different food types. The other two were endowed with a chronological or associative memory, which stores long-term temporal information about absolute times of these availabilities or delays between them, respectively. To determine the range of possible efficiencies, we also simulated a forager without temporal cognition but which simply targeted the closest and possibly empty food sources, and a perfectly prescient forager, able to know at any time which food source was effectively providing food. The sampling, associative and chronological foragers were far more efficient than the forager without temporal cognition in temporally predictable environments, and interestingly, their efficiencies increased with the level of temporal heterogeneity. The use of a long-term temporal memory results in a foraging efficiency up to 1.16 times better (chronological memory) or 1.14 times worse (associative memory) than the use of a simple sampling memory. Our results thus show that, for everyday foraging, a long-term temporal memory did not provide a clear benefit over a simple short-term memory that keeps track of the current resource availability. Long-term temporal memories may therefore have emerged in contexts where short-term temporal cognition is useless, i.e. when the anticipation of future environmental changes is strongly needed.

The integrative biology of genetic dominance.

Dominance is a basic property of inheritance systems describing the link between a diploid genotype at a single locus and the resulting phenotype. Models for the evolution of dominance have long been framed as an opposition between the irreconcilable views of Fisher in 1928 supporting the role of largely elusive dominance modifiers and Wright in 1929, who viewed dominance as an emerging property of the structure of enzymatic pathways. Recent theoretical and empirical advances however suggest that these opposing views can be reconciled, notably using models investigating the regulation of gene expression and developmental processes. In this more comprehensive framework, phenotypic dominance emerges from departures from linearity between any levels of integration in the genotype-to-phenotype map. Here, we review how these different models illuminate the emergence and evolution of dominance. We then detail recent empirical studies shedding new light on the diversity of molecular and physiological mechanisms underlying dominance and its evolution. By reconciling population genetics and functional biology, we hope our review will facilitate cross-talk among research fields in the integrative study of dominance evolution.

Assessing the Role of Developmental and Environmental Factors in Chemical Defence Variation in Heliconiini Butterflies.

Chemical defences in animals are both incredibly widespread and highly diverse. Yet despite the important role they play in mediating interactions between predators and prey, extensive differences in the amounts and types of chemical compounds can exist between individuals, even within species and populations. Here we investigate the potential role of environment and development on the chemical defences of warningly coloured butterfly species from the tribe Heliconiini, which can both synthesize and sequester cyanogenic glycosides (CGs). We reared 5 Heliconiini species in captivity, each on a single species-specific host plant as larvae, and compared them to individuals collected in the wild to ascertain whether the variation in CG content observed in the field might be the result of differences in host plant availability. Three of these species were reared as larvae on the same host plant, Passiflora riparia, to further test how species, sex, and age affected the type and amount of different defensive CGs, and how they affected the ratio of synthesized to sequestered compounds. Then, focusing on the generalist species Heliconius numata, we specifically explored variation in chemical profiles as a result of the host plant consumed by caterpillars and their brood line, using rearing experiments carried out on two naturally co-occurring host plants with differing CG profiles. Our results show significant differences in both the amount of synthesized and sequestered compounds between butterflies reared in captivity and those collected in the field. We also found a significant effect of species and an effect of sex in some, but not all, species. We show that chemical defences in H. numata continue to increase throughout their life, likely because of continued biosynthesis, and we suggest that variation in the amount of synthesized CGs in this species does not appear to stem from larval host plants, although this warrants further study. Interestingly, we detected a significant effect of brood lines, consistent with heritability influencing CG concentrations in H. numata. Altogether, our results point to multiple factors resulting in chemical defence variation in Heliconiini butterflies and highlight the overlooked effect of synthesis capabilities, which may be genetically determined to some extent.

Mutation load at a mimicry supergene sheds new light on the evolution of inversion polymorphisms.

Chromosomal inversions are ubiquitous in genomes and often coordinate complex phenotypes, such as the covariation of behavior and morphology in many birds, fishes, insects or mammals1-11. However, why and how inversions become associated with polymorphic traits remains obscure. Here we show that despite a strong selective advantage when they form, inversions accumulate recessive deleterious mutations that generate frequency-dependent selection and promote their maintenance at intermediate frequency. Combining genomics and in vivo fitness analyses in a model butterfly for wing-pattern polymorphism, Heliconius numata, we reveal that three ecologically advantageous inversions have built up a heavy mutational load from the sequential accumulation of deleterious mutations and transposable elements. Inversions associate with sharply reduced viability when homozygous, which prevents them from replacing ancestral chromosome arrangements. Our results suggest that other complex polymorphisms, rather than representing adaptations to competing ecological optima, could evolve because chromosomal rearrangements are intrinsically prone to carrying recessive harmful mutations.

Evolution and genetic architecture of disassortative mating at a locus under heterozygote advantage.

The evolution of mate choice is a major topic in evolutionary biology because it is thought to be a key factor in trait and species diversification. Here, we aim at uncovering the ecological conditions and genetic architecture enabling the puzzling evolution of disassortative mating based on adaptive traits. This rare form of mate choice is observed for some polymorphic traits but theoretical predictions on the emergence and persistence of this behavior are largely lacking. Thus, we developed a mathematical model to specifically understand the evolution of disassortative mating based on mimetic color pattern in the polymorphic butterfly Heliconius numata. 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 modeled different possible genetic architectures underlying mate choice behavior, 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 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.