Insects represent valuable food for many predators, and as such they have evolved a large panel of anti-predator adaptations. While deceptive adaptations such as camouflage and masquerade rest on ...avoiding detection by predators, aposematism relies on advertising chemical defenses with conspicuous warning signals, such as colorful patterns. Because the efficiency of a warning signal increases with its own local abundance, multiple aposematic prey exposed to the same predators benefit from converging on the same warning signal, a phenomenon originally observed by Henri Bates and Alfred Wallace and later understood and formalized by the German naturalist Fritz Müller 1 and called Müllerian mimicry. Convergence in warning signal is therefore due to positive frequency-dependent selection, leading to a ‘strength in numbers’ effect. Species sharing the same warning are said to be co-mimetic and interact mutualistically (i.e. individuals from either species benefit from the presence of individuals of co-mimetic species), and form mimicry rings.
Müllerian mimicry exists in a variety of organisms, including frogs, wasps, millipedes and beetles, but it has been best studied in butterflies (Fig. 1). Two neotropical butterfly clades have attracted considerable attention: the genus Heliconius (43 species) and the tribe Ithomiini (393 species).
Here, I review recent genetic and ecological results on Heliconius and Ithomiini butterflies that advance our knowledge on the proximal and ultimate drivers of mimicry, and on the evolutionary and ecological consequences of mimicry in terms of speciation, genetic architecture and ecological niche evolution. I also present recent results that help us understanding two apparent paradoxes: the embarrassing diversity of mimicry patterns despite strong selection for convergence, and the evolution of transparent wing patterns in aposematic butterflies, where conspicuous signals are supposed to be favored.
Selection on convergent wing colour pattern among mimetic butterflies is obviously strong, as illustrated by the striking similarity among distantly related species (Fig. 1A). Such convergent selection is expected to reduce warning signal diversity. Yet, diversity in warning signals is pervasive, at several geographical scales (Fig. 1B,C). Is this diversity transient, or is it stable? If so, what maintains it? Convergence in warning signal is driven by local predation pressure. Therefore, prey exposed to different communities of predators are not expected to converge on the same warning signal, as shown by theoretical models. In practice, geographical subspecies of mimetic butterflies, which occur in different regions, are exposed to different suites of predators and often harbour different colour patterns (Fig. 1B). At a much smaller scale, it has been shown that predators are segregated by microhabitat locally (for instance, some live in the canopy while other occupy the understorey), such that distinct mimicry rings can be maintained in different microhabitats (Fig. 1C). Therefore, mimicry diversity at various ecological scales can be maintained due to predator segregation 2.
Mimicry is also believed to be a driver of speciation. Indeed, in species harbouring multiple subspecies with distinct colour patterns (Fig. 1B), hybrids between subspecies typically have a recombinant, non-mimetic colour pattern, and suffer increased predation. Colour pattern is also often used as a mating cue such that mimetic butterflies mate assortatively, a likely consequence of selection against non-mimetic hybrids (reinforcement). Therefore, shifts in mimicry pattern causes both post- and pre-mating reproductive isolation, and, ultimately, speciation 2. Mimicry may therefore be one of the factors explaining the high diversity of Müllerian mimetic butterflies.
Mimicry raises the question of how convergent phenotypes are produced in different species. Are the same genes involved? Comparative analyses of genomic architectures controlling mimicry patterns in Heliconius reveal that homologous chromosomal regions, the “wing patterning toolkit” control much of mimicry variations in most species 2. Some of the genes involved have now been characterized, and include the transcription factor optix, the morphogen WntA, the cell-cycle regulator cortex and the transcription factor Aristaless1. Mimicry between Heliconius lineages has occurred through parallel evolution (independent recruitment of the same genes), except in a few cases where there is evidence for adaptive introgression of wing pattern genes 2. Mimicry can also incur strong selection on the genetic architecture of genes controlling colour pattern variation, as has been shown in the species H. numata. This species is unusual in that it is polymorphic within populations. Unlike other Heliconius species that embrace multiple species with distinct colour patterns, crosses between individuals harbouring different colour patterns that co-occur in H. numata never produce offspring with intermediate colour pattern. Instead, offspring look like either of their parents. Recent genetic and behavioural studies have shown that all variation is controlled at a single locus containing tightly linked genes (i.e. a supergene), and that different colour patterns correspond to different supergene haplotypes, which are characterized by different inversions of chromosome fragments within the supergene. Therefore, recombination between morphs is strongly reduced. Moreover, there is a strict series of dominance among morphs that co-occur. Both mechanisms prevent the formation of intermediate colour pattern, and have likely evolved as a response to selection against individuals with such intermediate, non-mimetic colour patterns 2.
Selection incurred by mimicry can also affect multiple ecological dimensions. Indeed, mimicry rings are segregated by microhabitat and habitat, and theoretical work and phylogenetic comparative analyses on Ithomiini butterflies have shown that the association between mimicry and (micro)habitat is adaptive, i.e. it is not due to shared ancestry, but most likely to selection for convergence on both colour pattern and ecological niche 2. Moreover, since larval hostplants are also likely segregated ecologically, co-mimetic species tend to use the same hostplant more often than expected at random. Therefore, mimicry, a kind of mutualistic interaction, drives convergence along multiple ecological dimensions, not only colour pattern.
Finally, although the efficiency and memorability of a warning signal increases with its conspicuousness, the vast majority of Ithomiini species are transparent to some degrees, although all of them have conspicuous pattern elements (Fig. 2). Why has transparency evolved in aposematic butterflies? Bird vision modelling and detectability and palatability tests with bird predators have shown that transparent species are less detectable than opaque species; yet, they are no less unpalatable, and in fact they may even be more unpalatable 3. Transparent species probably make the best of both worlds: they suffer less attacks from naïve predators because they are less often detected and, if they are detected by an ‘educated’ predator, they are not attacked because they are recognized as unpalatable. However, all else being equal, the predator learning process is expected to take longer with transparent than with opaque butterflies. Since increased unpalatability increases predator learning rate, we hypothesize that transparency can only evolve in highly unpalatable lineages, where it is less costly in terms of predator learning, which is consistent with the observation that all transparent species studied thus far are highly unpalatable.
In conclusion, Müllerian mimicry is a compelling example of the power of natural selection, where the evolution of defences against predators drives the evolution of conspicuous warning signals, which in turn drives convergence in those signals. Evolutionary implications of mimicry go well beyond warning signal convergence, since mimicry also affects the evolution of the ecological niche at various scales, and the genetic architecture of warning signals. The apparent paradox of the maintenance of mimicry diversity is now well understood, but the origin of diversity in the first place is still puzzling, since new warning signal are initially rare and should be selected against. However complex cognitive strategies of predators, such as the optimal sampling strategy, may protect rare warning signals, thereby enabling them to increase in frequency until they are common enough to be recognized and avoided by a large number of predators, and may be part of the explanation of the origin of diversity.
Finally, another apparent paradox, the evolution of transparent wing colour patterns in aposematic butterflies is also now understood. Yet, transparent wings, which entail a reduction in membrane coverage by scales and a reduction in wing pigmentation, may incur costs in terms of thermoregulation and hydrophobicity, which remain to be explored.
Evolutionary convergence of color pattern in mimetic species is tightly linked with the evolution of chemical defenses. Yet, the evolutionary forces involved in natural variations of chemical ...defenses in aposematic species are still understudied. Herein, we focus on the evolution of chemical defenses in the butterfly tribe Heliconiini. These neotropical butterflies contain large concentrations of cyanogenic glucosides, cyanide‐releasing compounds acting as predator deterrent. These compounds are either de novo synthesized or sequestered from their Passiflora host plant, so that their concentrations may depend on host plant specialization and host plant availability. We sampled 375 wild Heliconiini butterflies across Central and South America, covering 43% species of this clade, and quantify individual variations in the different CGs using liquid chromatography coupled with tandem mass spectrometry. We detected new compounds and important variations in chemical defenses both within and among species. Based on the most recent and well‐studied phylogeny of Heliconiini, we show that ecological factors such as mimetic interactions and host plant specialization have a significant association with chemical profiles, but these effects are largely explained by phylogenetic relationships. Our results therefore suggest that shared ancestries largely contribute to chemical defense variation, pointing out at the interaction between historical and ecological factors in the evolution of Müllerian mimicry.
Within Heliconiini butterflies, we show that ecological factors such as mimetic interactions and host plant specialization have a significant effect on chemical profiles, but these effects are largely explained by phylogenetic relationships. Our results suggest that shared ancestries largely contribute to chemical defence variation, pointing out at the interaction between historical and ecological factors in the evolution of Müllerian mimicry.
Prey populations have evolved multiple strategies to escape predation. Camouflage is a strategy resting on avoiding detection by potential predators, whereas aposematism relies on advertising ...chemical defences with conspicuous warning signals. While camouflaged phenotypes are subject to negative frequency-dependent selection, aposematic preys are under positive frequency-dependence, where the efficiency of a signal increases with its own local abundance. Because of his “strength-in-number” effect, multiple chemically-defended species exposed to the same suite of predators gain a selective advantage from converging on the same warning signals. Convergence in warning signals is called Müllerian mimicry. Here, we review the results of recent genetic and ecological research on two well-studied groups of neotropical Müllerian mimetic butterflies, the genus Heliconius and the tribe Ithomiini, which advertise their unpalatability through conspicuous wing colour patterns. Mimicry represents a major adaptation in these groups, where the effects of selection extend well beyond mere phenotypic resemblance. Selection acts on other traits used as mating cues, on the genetic architecture of colour pattern and even on the ecological niche of species. The origin of mimicry itself and the coexistence of multiple mimicry patterns are well understood, but the ultimate drivers of mimicry diversity remain unclear.
The mechanic properties of cell membranes control many biological processes. The complexity of natural membranes is often dealt with by building synthetic vesicles (Giant Unilamellar Vesicles, GUVs), ...which can be thought as micron-sized minimal cells. Micropipette aspiration technique is the gold standard to characterize membrane mechanics, but it involves manual, long and tedious experiments. Microfluidics is perfectly suited to handle GUVs and permits in particular to conceive on-chip micropipettes for automated, systematic studies of membrane mechanical moduli. We developed a microfabrication process that enables obtaining the required 3-level channels including a micropipette in the intermediate level, with micrometric alignment, sufficiently low adhesion and roughness. We extended the theoretical analysis of micropipette, valid for cylindrical geometries that microfabrication does not allow, to the on-chip geometry, by considering the deformation of a vesicle in a square cross-section trap. We confirmed the validity of our approach thanks to systematic experiments performed on GUVs with well-characterized compositions: the obtained values of the membrane stretching modulus are in quantitative agreement with the literature. As a case study, we used our device to show that GUVs challenged with copolymer micelles, typically used for drug delivery, displayed a significantly decrease of the membrane stretching modulus, which could mediate internalization of these nanovectors. This study opens the path to systematic studies of the influence of physico-chemical environment on the mechanics of cell membranes.
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•An on-chip micropipette is developed to probe the mechanics of biomembranes•The fabrication process involves 3-level glass‑silicon channels including an intermediate pipette in the middle level•The micropipette theoretical analysis has been extended to the geometry of the chip•Stretching modulus of standard lipid membrane is recovered. Self-assembled nanoparticles lower membrane’s stretching modulus
Caterpillar mimicry is surprisingly scarce, despite many examples of apparently defended, aposematic species. Here, we describe two possible examples of caterpillar mimicry in two tribes of the ...Neotropical Danainae: Danaini and Ithomiini. The first example, from the Caribbean island of Hispaniola, includes two subtribes of Danaini: Danaus plexippus (L.), Danaus gilippus (Cramer), Danaus cleophile (Godart) (Danaina), Anetia briarea (Godart), and Anetia jaegeri (Ménétriés) (Itunina). The first two widespread Danaus species have unusually dark phenotypes on Hispaniola, which we suggest are the result of mimicry with endemic Caribbean danaines. The second example, from the upper Amazon of eastern Ecuador, involves four subtribes of Ithomiini: Forbestra olivencia (Bates) (Mechanitina), Hypothyris fluonia (Hewitson), Hypothyris semifulva (Salvin) (Napeogenina), Ithomia amarilla Haensch (Ithomiina), Hyposcada anchiala (Hewitson), Oleria sexmaculata (Haensch) (Oleriina), and Pseudoscada florula (Hewitson) (Godyridina). Hyposcada illinissa (Hewitson) (Oleriina) is a possible additional member. This mimicry ring shows a color pattern known only from the upper Amazon, with the caterpillar having a yellow body and bright blue anterior and posterior segments, and this pattern has clearly evolved at least four times in the Ithomiini. We suggest that precise mimicry among caterpillars may be rarer than among adult butterflies because of a lack of sexual selection to drive the initial evolution of bright colors in larvae. We also suggest that the evolution of warning colors in protected caterpillars is more difficult than in butterflies, because a novel, conspicuous caterpillar is less able to avoid capture than the more agile adult.
Understanding the processes underlying diversification is a central question in evolutionary biology. For butterflies, access to new host plants provides opportunities for adaptive speciation. On the ...one hand, locally abundant host species can generate ecologically significant selection pressure. But a diversity of host plant species within the geographic range of each population and/or species might also eliminate any advantage conferred by specialization. This paper focuses on four Melinaea species, which are oligophagous on the family Solanaceae: M. menophilus, M. satevis, M. marsaeus, and finally, M. mothone. We examined both female preference and larval performance on two host plant species that commonly occur in this butterfly's native range, Juanulloa parasitica and Trianaea speciosa, to determine whether the different Melinaea species show evidence of local adaptation.
In choice experiments, M. mothone females used both host plants for oviposition, whereas all other species used J. parasitica almost exclusively. In no choice experiment, M. mothone was the only species that readily accepted T. speciosa as a larval host plant. Larval survival was highest on J. parasitica (82.0 % vs. 60.9 %) and development took longer on T. speciosa (14.12 days vs. 13.35 days), except for M. mothone, which did equally well on both host plants. For all species, average pupal weight was highest on J. parasitica (450.66 mg vs. 420.01 mg), although this difference was least apparent in M. mothone.
We did not find that coexisting species of Melinaea partition host plant resources as expected if speciation is primarily driven by host plant divergence. Although M. mothone shows evidence of local adaptation to a novel host plant, T. speciosa, which co-occurs, it does not preferentially lay more eggs on or perform better on this host plant than on host plants used by other Melinaea species and not present in its distributional range. It is likely that diversification in this genus is driven by co-occurring Müllerian mimics and the resulting predation pressure, although this is also likely made possible by greater niche diversity as a consequence of plasticity for potential hosts.
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 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.
Abstract
Butterflies of the genus Melinaea have conspicuous warning colours and are thought to be the prime distasteful models in many cases of mimicry in the Neotropics. Colour pattern variability ...has made systematics challenging and previous studies have found little to no genetic differentiation. This paper provides detailed descriptions of the immature stages of seven Melinaea taxa from north-eastern Peru, including distribution and host plant use, in addition to measures of genetic differentiation using microsatellite markers and mitochondrial sequences. Development time and immature stages were similar, making it difficult to elucidate taxonomy based on larval morphological characters. All taxa used Juanulloa as a host plant (Solanaceae), except Melinaea ‘marsaeus’ mothone, which occurs at higher elevations and used Trianaea (Solanaceae). The seven taxa show virtually no mitochondrial divergence, suggesting a recent radiation. Microsatellite markers, however, revealed distinct genetic clusters and evidence of admixture, demonstrating a complex diversification history. Ecological and genetic differentiation observed for Mel. ‘marsaeus’ mothone prompts for a taxonomic status revision to Melinaea mothone mothone and the taxonomic status of Melinaea ‘satevis’ tarapotensis remains unclear. Clearly, further work is needed to clarify the systematics and to shed light on the processes driving speciation in this genus.
Ant colonies may have a single or several reproductive queens (monogyny and polygyny, respectively). In polygynous colonies, colony reproduction may occur by budding, forming multinest, polydomous ...colonies. In most cases, budding leads to strong genetic structuring within populations, and positive relatedness among nestmates. However, in a few cases, polydomous populations may be unicolonial, with no structuring and intra-nest relatedness approaching zero. We investigated the spatial organisation and genetic structure of a polygynous, polydomous population of Formica truncorum in Finland. F. truncorum shifts nest sites between hibernation and the reproductive season, which raises the following question: are colonies maintained as genetic entities throughout the seasons, or is the population unicolonial throughout the season? Using nest-specific marking and five microsatellite loci, we found a high degree of mixing between individuals of the population, and no evidence for a biologically significant genetic structuring. The nestmate relatedness was also indistinguishable from zero. Taken together, the results show that the population is unicolonial. In addition, we found that the population has undergone a recent bottleneck, suggesting that the entire population may have been founded by a very limited number of females. The precise causes for unicoloniality in this species remain open, but we discuss the potential influence of intra-specific competition, disintegration of recognition cues and the particular hibernation habits of this species.
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