Mimicry is one of the best-studied examples of adaptation, and recent studies have provided new insights into the role of mimicry in speciation and diversification. Classical Müllerian mimicry theory ...predicts convergence in warning signal among protected species, yet tropical butterflies are exuberantly diverse in warning colour patterns, even within communities. We tested the hypothesis that microhabitat partitioning in aposematic butterflies and insectivorous birds can lead to selection for different colour patterns in different microhabitats and thus help maintain mimicry diversity. We measured distribution across flight height and topography for 64 species of clearwing butterflies (Ithomiini) and their co-mimics, and 127 species of insectivorous birds, in an Amazon rainforest community. For the majority of bird species, estimated encounter rates were non-random for the two most abundant mimicry rings. Furthermore, most butterfly species in these two mimicry rings displayed the warning colour pattern predicted to be optimal for anti-predator defence in their preferred microhabitats. These conclusions were supported by a field trial using butterfly specimens, which showed significantly different predation rates on colour patterns in two microhabitats. We therefore provide the first direct evidence to support the hypothesis that different mimicry patterns can represent stable, community-level adaptations to differing biotic environments.
Butterflies (Papilionoidea), with over 18,000 described species 1, have captivated naturalists and scientists for centuries. They play a central role in the study of speciation, community ecology, ...biogeography, climate change, and plant-insect interactions and include many model organisms and pest species 2, 3. However, a robust higher-level phylogenetic framework is lacking. To fill this gap, we inferred a dated phylogeny by analyzing the first phylogenomic dataset, including 352 loci (> 150,000 bp) from 207 species representing 98% of tribes, a 35-fold increase in gene sampling and 3-fold increase in taxon sampling over previous studies 4. Most data were generated with a new anchored hybrid enrichment (AHE) 5 gene kit (BUTTERFLY1.0) that includes both new and frequently used (e.g., 6) informative loci, enabling direct comparison and future dataset merging with previous studies. Butterflies originated around 119 million years ago (mya) in the late Cretaceous, but most extant lineages diverged after the Cretaceous-Paleogene (K-Pg) mass-extinction 65 mya. Our analyses support swallowtails (Papilionidae) as sister to all other butterflies, followed by skippers (Hesperiidae) + the nocturnal butterflies (Hedylidae) as sister to the remainder, indicating a secondary reversal from diurnality to nocturnality. The whites (Pieridae) were strongly supported as sister to brush-footed butterflies (Nymphalidae) and blues + metalmarks (Lycaenidae and Riodinidae). Ant association independently evolved once in Lycaenidae and twice in Riodinidae. This study overturns prior notions of the taxon’s evolutionary history, as many long-recognized subfamilies and tribes are para- or polyphyletic. It also provides a much-needed backbone for a revised classification of butterflies and for future comparative studies including genome evolution and ecology.
•Phylogenomic data provide a novel view of broad butterfly evolutionary relationships•Most current diversity originated after the K-Pg mass extinction•Many accepted higher taxa are para- or polyphyletic•Ant association originated three times independently in blues and metalmarks
Espeland et al. inferred a dated, molecular phylogeny of butterflies based on the largest and most taxonomically extensive phylogenomic dataset ever assembled for the group: 352 loci from 207 species representing all butterfly families and subfamilies and 98% of the tribes. This tree will provide a robust framework for future comparative analyses.
Most research on aposematism has focused on chemically defended prey, but the signalling difficulty of capture remains poorly explored. Similar to classical Batesian and Müllerian mimicry related to ...distastefulness, such 'evasive aposematism' may also lead to convergence in warning colours, known as evasive mimicry. A prime candidate group for evasive mimicry are
butterflies, which are agile insects and show remarkable colour pattern convergence. We tested the ability of naive blue tits to learn to avoid and generalize
wing patterns associated with the difficulty of capture and compared their response to that of birds that learned to associate the same wing patterns with distastefulness. Birds learned to avoid all wing patterns tested and generalized their aversion to other prey to some extent, but learning was faster with evasive prey compared to distasteful prey. Our results on generalization agree with longstanding observations of striking convergence in wing colour patterns among
species, since, in our experiments, perfect mimics of evasive and distasteful models were always protected during generalization and suffered the lowest attack rate. Moreover, generalization on evasive prey was broader compared to that on distasteful prey. Our results suggest that being hard to catch may deter predators at least as effectively as distastefulness. This study provides empirical evidence for evasive mimicry, a potentially widespread but poorly understood form of morphological convergence driven by predator selection.
Abstract
DNA ‘barcoding’ has contributed greatly to resolving species limits in rapidly diverging tropical insect groups. Here, we explored species diversity in the widespread, cryptic Neotropical ...butterfly genus Hermeuptychia by generating 601 new sequences of the cytochrome c oxidase I (COI) barcode, tripling available information. Our dataset focused in particular on Ecuador, a biogeographically pivotal country, with additional sequences from Brazil, Costa Rica, French Guiana, Guatemala, Mexico, Panama and Peru. We examined the performance of two phylogeny-based approaches for objectively delineating species, Generalized Mixed Yule Coalescent (GMYC) and Poisson Tree Processes (PTP), as well as a clustering-based approach, Automatic Barcode Gap Discovery (ABGD), on the combined dataset, including our data and 302 published sequences. In general, GMYC and PTP tended to cluster or split likely species as assessed from morphology, depending on model settings, whereas ABGD was less sensitive and produced a more plausible classification. Numerous sequences formed well-supported clades, putative species, that were unrepresented in previously published datasets. The average diversity across all methods was 45 species, in contrast to the 11 species recognized in the current taxonomy. The resulting COI dataset, in combination with ongoing genomic and morphological research, should significantly clarify our understanding of Hermeuptychia species diversity.
Environmental heterogeneity is considered an important factor supporting the evolution and maintenance of biodiversity. At small scales, such heterogeneity is thought to promote species co-existence ...through an increase in niche opportunities. Amazonia, the largest and most biodiverse rainforest in the world, presents a large number of vegetation types within its territory. Here, we tested the hypothesis that butterfly assemblages differ among five vegetation types at a small scale (less than 1 km2) in a region of Southern Amazonia. The vegetation types studied were forest gap, terra firme, igapó, semi-deciduous forest, and bamboo forest. The richest and most abundant community was in forest gap; igapó was the least rich, but held the second most abundant community and the only one with nine indicator species instead of two or three. Assemblage composition differed among all vegetation types, with the exception of forest gap and bamboo forest. Different light levels, temperatures, humidity, and host plant availability among vegetation types are likely relevant factors influencing these butterfly assemblages. The results suggest that the presence of various vegetation types in the region promotes the coexistence of butterfly species, and that specific threats to each vegetation type should be addressed to conserve the region’s biodiversity.
The Neotropics harbour the most diverse flora and fauna on Earth. The Andes are a major centre of diversification and source of diversity for adjacent areas in plants and vertebrates, but studies on ...insects remain scarce, even though they constitute the largest fraction of terrestrial biodiversity. Here, we combine molecular and morphological characters to generate a dated phylogeny of the butterfly genus Pteronymia (Nymphalidae: Danainae), which we use to infer spatial, elevational and temporal diversification patterns. We first propose six taxonomic changes that raise the generic species total to 53, making Pteronymia the most diverse genus of the tribe Ithomiini. Our biogeographic reconstruction shows that Pteronymia originated in the Northern Andes, where it diversified extensively. Some lineages colonized lowlands and adjacent montane areas, but diversification in those areas remained scarce. The recent colonization of lowland areas was reflected by an increase in the rate of evolution of species' elevational ranges towards present. By contrast, speciation rate decelerated with time, with no extinction. The geological history of the Andes and adjacent regions have likely contributed to Pteronymia diversification by providing compartmentalized habitats and an array of biotic and abiotic conditions, and by limiting dispersal between some areas while promoting interchange across others.
The Heliconiini genera Agraulis and Dryas are widely distributed throughout the Neotropics and into adjacent temperate regions, and although they are currently treated as monotypic, both show ...significant geographic phenotypic variation. In this work, we employ six genetic markers (4199 bp), two mitochondrial and four nuclear, to perform coalescent species delimitation analyses in Bayesian Phylogenetics and Phylogeography (BPP) and in integrated BPP (iBPP), the latter also includes linear measurements and wings landmarks. We also analyze cytochrome c oxidase I (COI) barcode sequences for each genus using genetic distances, haplotype networks and a character‐based approach. Based on the model testing results, complemented with data from previous studies, we performed morphometric analyses to compare fore and hindwing size, aspect ratio and shape among the new species. In addition, we compared the forewing spot pattern of hypothesizes species using the r package patternize and, for Dryas, compared the colour patterns of mature larvae. Model testing of the molecular species delimitation outputs favoured a seven species hypothesis for Agraulis and a four species hypothesis for Dryas. Average distances among COI barcode sequences of these groups were from 1.09 to 5.81% in Agraulis and from 1.09 to 3.44% in Dryas. Within‐group distances ranged from 0 to 1.11% and between 0 and 2.43%, respectively. NeighborNet haplotype networks showed that all but one of the species are monophyletic, and the character‐based approach found exclusive diagnostic positions for most species, while the rest can be recognized by unique combinations of the 44 informative nucleotide positions analysed. Morphometric analysis supported all species of Agraulis and Dryas based on wing shape, and also in several cases on wing sizes and aspect ratio (hindwing length–forewing length), including A. v. galapagensis, which was absent from the molecular study. The analysis of the forewing spot pattern also revealed differences among most species hypothesis. The colour pattern of the last instar larva is also diagnostic for each Dryas species hypothesis. Locality data for species in both genera show that most of them are allopatric albeit a few have contact zones being parapatric at some locations. Based on the observed genetic differences, which covary with morphology and geographical distribution, we recommend the recognition of eight species of Agraulis: A. incarnata, A. vanillae, A. forbesi new status, A. insularis reinstated status, A. maculosa new status, A. lucina reinstated status, A. galapagensis new status and one undescribed species, and four species of Dryas: D. iulia, D. dominicana revised status, D. lucia revised status and D. alcionea reinstated status. Further work is needed to investigate, which selective forces have led to the current configurations of venation and wing shape, the probable gene flow among species with a focus on Agraulis and gather more data on species ecology.
LSIDurn: lsid:
zoobank.org: pub: 9E8C9F6E‐91C3‐4FB2‐804D‐1A9C4BD2EABB.
Molecular, morphometric and forewing pattern analyses support several species in the hitherto monotypic passion‐vine butterfly genera Agraulis and Dryas.
All data analysed co‐vary geographically with colour pattern of Dryas mature larvae also varying accordingly. While Dryas species are fully allopatric, most adjacent Agraulis species have contact zones.
Agraulis and Dryas populations face a broad array of ecological conditions across their distributions from the arid Pacific coast to the Amazon basin and the West Indies, which likely have influenced speciation processes.
Despite more than a century of biological research on the evolution and maintenance of mimetic signals, the relative frequencies of models and mimics necessary to establish and maintain Batesian ...mimicry in natural populations remain understudied. Here we investigate the frequency-dependent dynamics of imperfect Batesian mimicry, using predation experiments involving artificial butterfly models. We use two geographically distinct populations of Adelpha butterflies that vary in their relative frequencies of a putatively defended model (Adelpha iphiclus) and Batesian mimic (Adelpha serpa). We found that in Costa Rica, where both species share similar abundances, Batesian mimicry breaks down, and predators more readily attack artificial butterfly models of the presumed mimic, A. serpa. By contrast, in Ecuador, where A. iphiclus (model) is significantly more abundant than A. serpa (mimic), both species are equally protected from predation. Our results provide compelling experimental evidence that imperfect Batesian mimicry is frequency-dependent on the relative abundance of models and mimics in natural populations, and contribute to the growing body of evidence that complex dynamics, such as seasonality or the availability of alternative prey, influence the evolution of mimetic traits.
Patterns of larval food plant use and immature stage morphology help clarify Neotropical butterfly species diversity, and, in many cases, lineages identified with molecular data are corroborated by ...morphology and ecology of immature stages. Here, we investigate cryptic species in Adelpha butterflies (Nymphalidae), a group known for challenging adult wing similarity coupled with mimicry, and for its remarkably wide larval food plant breadth. We focus on the Adelpha serpa‐group and in particular Adelpha serpa celerio, whose immatures have been documented feeding on 11 plant families. Our analyses of A. serpa, and among serpa‐group species across the Neotropics, revealed evidence of cryptic species, but the pattern within A. serpa celerio showed relatively weak mtDNA and morphological differences, and no differentiation in food plant use. We conclude that A. serpa should be revised and recognize A. serpa to include the nominate subspecies and recognize A. celerio (revised status) as a geographically widespread species and a larval food plant generalist that contains A. c. celerio (revised status), A. c. duiliae (revised status) and A. c. diadochus (revised status). Four additional species within the serpa‐group show strong evidence of harbouring allopatric cryptic species, and further research should be done to clarify their species limits.
DNA 'barcoding' relies on a short fragment of mitochondrial DNA to infer identification of specimens. The method depends on genetic diversity being markedly lower within than between species. Closely ...related species are most likely to share genetic variation in communities where speciation rates are rapid and effective population sizes are large, such that coalescence times are long. We assessed the applicability of DNA barcoding (here the 5′ half of the cytochrome c oxidase I) to a diverse community of butterflies from the upper Amazon, using a group with a well-established morphological taxonomy to serve as a reference. Only 77% of species could be accurately identified using the barcode data, a figure that dropped to 68% in species represented in the analyses by more than one geographical race and at least one congener. The use of additional mitochondrial sequence data hardly improved species identification, while a fragment of a nuclear gene resolved issues in some of the problematic species. We acknowledge the utility of barcodes when morphological characters are ambiguous or unknown, but we also recommend the addition of nuclear sequence data, and caution that species-level identification rates might be lower in the most diverse habitats of our planet.
PDF
