Rapid radiation of ant parasitic butterflies during the Miocene aridification of Africa.

Africa has undergone a progressive aridification during the last 20 My that presumably impacted organisms and fostered the evolution of life history adaptations. We test the hypothesis that shift to living in ant nests and feeding on ant brood by larvae of phyto-predaceous Lepidochrysops butterflies was an adaptive response to the aridification of Africa that facilitated the subsequent radiation of butterflies in this genus. Using anchored hybrid enrichment we constructed a time-calibrated phylogeny for Lepidochrysops and its closest, non-parasitic relatives in the Euchrysops section (Poloyommatini). We estimated ancestral areas across the phylogeny with process-based biogeographical models and diversification rates relying on time-variable and clade-heterogeneous birth-death models. The Euchrysops section originated with the emerging Miombo woodlands about 22 million years ago (Mya) and spread to drier biomes as they became available in the late Miocene. The diversification of the non-parasitic lineages decreased as aridification intensified around 10 Mya, culminating in diversity decline. In contrast, the diversification of the phyto-predaceous Lepidochrysops lineage proceeded rapidly from about 6.5 Mya when this unusual life history likely first evolved. The Miombo woodlands were the cradle for diversification of the Euchrysops section, and our findings are consistent with the hypothesis that aridification during the Miocene selected for a phyto-predaceous life history in species of Lepidochrysops, with ant nests likely providing caterpillars a safe refuge from fire and a source of food when vegetation was scarce.

Mutualistic interactions shape global spatial congruence and climatic niche evolution in Neotropical mimetic butterflies.

Understanding the mechanisms underlying species distributions and coexistence is both a priority and a challenge for biodiversity hotspots such as the Neotropics. Here, we highlight that Müllerian mimicry, where defended prey species display similar warning signals, is key to the maintenance of biodiversity in the c. 400 species of the Neotropical butterfly tribe Ithomiini (Nymphalidae: Danainae). We show that mimicry drives large-scale spatial association among phenotypically similar species, providing new empirical evidence for the validity of Müller's model at a macroecological scale. Additionally, we show that mimetic interactions drive the evolutionary convergence of species climatic niche, thereby strengthening the co-occurrence of co-mimetic species. This study provides new insights into the importance of mutualistic interactions in shaping both niche evolution and species assemblages at large spatial scales. Critically, in the context of climate change, our results highlight the vulnerability to extinction cascades of such adaptively assembled communities tied by positive interactions.

The origin of modern patterns of continental diversity in Mauritiinae palms: the Neotropical museum and the Afrotropical graveyard.

While the latitudinal diversity gradient has received much attention, biodiversity and species richness also vary between continents across similar latitudes. Fossil information can be used to understand the evolutionary mechanisms that generated such variation between continents of similar latitudes. We integrated fossil data into a phylogenetic analysis of the Mauritiinae palms, whose extant diversity is restricted to the Neotropics, but extended across Africa and India during most of the Cenozoic. Mauritiinae diverged from its sister lineage Raphiinae ca 106 Ma. Using ancestral state estimation and a lineage through time analysis, we found that diversity arose globally during the late Cretaceous and Palaeocene across South America, Africa and India. The Palaeocene-Eocene transition (ca 56 Ma) marked the end of global Mauritiinae expansion, and the beginning of their decline in both Africa and India. Mauritiinae disappeared from the Indian subcontinent and Africa at the end of the Eocene and the Miocene, respectively. By contrast, Neotropical diversity steadily increased over the last 80 Myr. Taken together, our results suggest that the Neotropics functioned as a continental-scale refuge for Mauritiinae palms, where lineages survived and diversified while global climatic changes that drastically reduced rainforests led to their demise on other continents.

Conserved ancestral tropical niche but different continental histories explain the latitudinal diversity gradient in brush-footed butterflies.

The global increase in species richness toward the tropics across continents and taxonomic groups, referred to as the latitudinal diversity gradient, stimulated the formulation of many hypotheses to explain the underlying mechanisms of this pattern. We evaluate several of these hypotheses to explain spatial diversity patterns in a butterfly family, the Nymphalidae, by assessing the contributions of speciation, extinction, and dispersal, and also the extent to which these processes differ among regions at the same latitude. We generate a time-calibrated phylogeny containing 2,866 nymphalid species (~45% of extant diversity). Neither speciation nor extinction rate variations consistently explain the latitudinal diversity gradient among regions because temporal diversification dynamics differ greatly across longitude. The Neotropical diversity results from low extinction rates, not high speciation rates, and biotic interchanges with other regions are rare. Southeast Asia is also characterized by a low speciation rate but, unlike the Neotropics, is the main source of dispersal events through time. Our results suggest that global climate change throughout the Cenozoic, combined with tropical niche conservatism, played a major role in generating the modern latitudinal diversity gradient of nymphalid butterflies.

Punctuational ecological changes rather than global factors drive species diversification and the evolution of wing phenotypes in Morpho butterflies.

Assessing the relative importance of geographical and ecological drivers of evolution is paramount to understand the diversification of species and traits at the macroevolutionary scale. Here, we use an integrative approach, combining phylogenetics, biogeography, ecology and quantified phenotypes to investigate the drivers of both species and phenotypic diversification of the iconic Neotropical butterfly genus Morpho. We generated a time-calibrated phylogeny for all known species and inferred historical biogeography. We fitted models of time-dependent (accounting for rate heterogeneity across the phylogeny) and paleoenvironment-dependent diversification (accounting for global effect on the phylogeny). We used geometric morphometrics to assess variation of wing size and shape across the tree and investigated their dynamics of evolution. We found that the diversification of Morpho is best explained when considering variable diversification rates across the tree, possibly associated with lineages occupying different microhabitat conditions. First, a shift from understory to canopy was characterized by an increased speciation rate partially coupled with an increasing rate of wing shape evolution. Second, the occupation of dense bamboo thickets accompanying a major host-plant shift from dicotyledons towards monocotyledons was associated with a simultaneous diversification rate shift and an evolutionary 'jump' of wing size. Our study points to a diversification pattern driven by punctuational ecological changes instead of a global driver or biogeographic history.

Molecular phylogeny, classification, biogeography and diversification patterns of a diverse group of moths (Geometridae: Boarmiini).

Understanding how and why some groups have become more species-rich than others, and how past biogeography may have shaped their current distribution, are questions that evolutionary biologists have long attempted to answer. We investigated diversification patterns and historical biogeography of a hyperdiverse lineage of Lepidoptera, the geometrid moths, by studying its most species-rich tribe Boarmiini, which comprises ca. 200 genera and ca. known 3000 species. We inferred the evolutionary relationships of Boarmiini based on a dataset of 346 taxa, with up to eight genetic markers under a maximum likelihood approach. The monophyly of Boarmiini is strongly supported. However, the phylogenetic position of many taxa does not agree with current taxonomy, although the monophyly of most major genera within the tribe is supported after minor adjustments. Three genera are synonymized, one new combination is proposed, and four species are placed in incertae sedis within Boarmiini. Our results support the idea of a rapid initial diversification of Boarmiini, which also implies that no major taxonomic subdivisions of the group can currently be proposed. A time-calibrated tree and biogeographical analyses suggest that boarmiines appeared in Laurasia ca. 52 Mya, followed by dispersal events throughout the Australasian, African and Neotropical regions. Most of the transcontinental dispersal events occurred in the Eocene, a period of intense geological activity and rapid climate change. Diversification analyses showed a relatively constant diversification rate for all Boarmiini, except in one clade containing the species-rich genus Cleora. The present work represents a substantial contribution towards understanding the evolutionary origin of Boarmiini moths. Our results, inevitably biased by taxon sampling, highlight the difficulties with working on species-rich groups that have not received much attention outside of Europe. Specifically, poor knowledge of the natural history of geometrids (particularly in tropical clades) limits our ability to identify key innovations underlying the diversification of boarmiines.

Butterfly dichromatism primarily evolved via Darwin's, not Wallace's, model.

Sexual dimorphism is typically thought to result from sexual selection for elaborated male traits, as proposed by Darwin. However, natural selection could reduce expression of elaborated traits in females, as proposed by Wallace. Darwin and Wallace debated the origins of dichromatism in birds and butterflies, and although evidence in birds is roughly equal, if not in favor of Wallace's model, butterflies lack a similar scale of study. Here, we present a large-scale comparative phylogenetic analysis of the evolution of butterfly coloration, using all European non-hesperiid butterfly species (n = 369). We modeled evolutionary changes in coloration for each species and sex along their phylogeny, thereby estimating the rate and direction of evolution in three-dimensional color space using a novel implementation of phylogenetic ridge regression. We show that male coloration evolved faster than female coloration, especially in strongly dichromatic clades, with male contribution to changes in dichromatism roughly twice that of females. These patterns are consistent with a classic Darwinian model of dichromatism via sexual selection on male coloration, suggesting this model was the dominant driver of dichromatism in European butterflies.

A complete time-calibrated multi-gene phylogeny of the European butterflies.

With the aim of supporting ecological analyses in butterflies, the third most species-rich superfamily of Lepidoptera, this paper presents the first time-calibrated phylogeny of all 496 extant butterfly species in Europe, including 18 very localised endemics for which no public DNA sequences had been available previously. It is based on a concatenated alignment of the mitochondrial gene COI and up to eleven nuclear gene fragments, using Bayesian inferences of phylogeny. To avoid analytical biases that could result from our region-focussed sampling, our European tree was grafted upon a global genus-level backbone butterfly phylogeny for analyses. In addition to a consensus tree, the posterior distribution of trees and the fully concatenated alignment are provided for future analyses. Altogether a complete phylogenetic framework of European butterflies for use by the ecological and evolutionary communities is presented.

Priors and Posteriors in Bayesian Timing of Divergence Analyses: The Age of Butterflies Revisited.

The need for robust estimates of times of divergence is essential for downstream analyses, yet assessing this robustness is still rare. We generated a time-calibrated genus-level phylogeny of butterflies (Papilionoidea), including 994 taxa, up to 10 gene fragments and an unprecedented set of 12 fossils and 10 host-plant node calibration points. We compared marginal priors and posterior distributions to assess the relative importance of the former on the latter. This approach revealed a strong influence of the set of priors on the root age but for most calibrated nodes posterior distributions shifted from the marginal prior, indicating significant information in the molecular data set. Using a very conservative approach we estimated an origin of butterflies at 107.6 Ma, approximately equivalent to the latest Early Cretaceous, with a credibility interval ranging from 89.5 Ma (mid Late Cretaceous) to 129.5 Ma (mid Early Cretaceous). In addition, we tested the effects of changing fossil calibration priors, tree prior, different sets of calibrations and different sampling fractions but our estimate remained robust to these alternative assumptions. With 994 genera, this tree provides a comprehensive source of secondary calibrations for studies on butterflies.

A simple method for data partitioning based on relative evolutionary rates.

BACKGROUND: Multiple studies have demonstrated that partitioning of molecular datasets is important in model-based phylogenetic analyses. Commonly, partitioning is done a priori based on some known properties of sequence evolution, e.g. differences in rate of evolution among codon positions of a protein-coding gene. Here we propose a new method for data partitioning based on relative evolutionary rates of the sites in the alignment of the dataset being analysed. The rates are inferred using the previously published Tree Independent Generation of Evolutionary Rates (TIGER), and the partitioning is conducted using our novel python script RatePartitions. We conducted simulations to assess the performance of our new method, and we applied it to eight published multi-locus phylogenetic datasets, representing different taxonomic ranks within the insect order Lepidoptera (butterflies and moths) and one phylogenomic dataset, which included ultra-conserved elements as well as introns. METHODS: We used TIGER-rates to generate relative evolutionary rates for all sites in the alignments. Then, using RatePartitions, we partitioned the data into partitions based on their relative evolutionary rate. RatePartitions applies a simple formula that ensures a distribution of sites into partitions following the distribution of rates of the characters from the full dataset. This ensures that the invariable sites are placed in a partition with slowly evolving sites, avoiding the pitfalls of previously used methods, such as k-means. Different partitioning strategies were evaluated using BIC scores as calculated by PartitionFinder. RESULTS: Simulations did not highlight any misbehaviour of our partitioning approach, even under difficult parameter conditions or missing data. In all eight phylogenetic datasets, partitioning using TIGER-rates and RatePartitions was significantly better as measured by the BIC scores than other partitioning strategies, such as the commonly used partitioning by gene and codon position. We compared the resulting topologies and node support for these eight datasets as well as for the phylogenomic dataset. DISCUSSION: We developed a new method of partitioning phylogenetic datasets without using any prior knowledge (e.g. DNA sequence evolution). This method is entirely based on the properties of the data being analysed and can be applied to DNA sequences (protein-coding, introns, ultra-conserved elements), protein sequences, as well as morphological characters. A likely explanation for why our method performs better than other tested partitioning strategies is that it accounts for the heterogeneity in the data to a much greater extent than when data are simply subdivided based on prior knowledge.

Contrasting patterns of Andean diversification among three diverse clades of Neotropical clearwing butterflies.

The Neotropical region is the most biodiverse on Earth, in a large part due to the highly diverse tropical Andean biota. The Andes are a potentially important driver of diversification within the mountains and for neighboring regions. We compared the role of the Andes in diversification among three subtribes of Ithomiini butterflies endemic to the Neotropics, Dircennina, Oleriina, and Godyridina. The diversification patterns of Godyridina have been studied previously. Here, we generate the first time-calibrated phylogeny for the largest ithomiine subtribe, Dircennina, and we reanalyze a published phylogeny of Oleriina to test different biogeographic scenarios involving the Andes within an identical framework. We found common diversification patterns across the three subtribes, as well as major differences. In Dircennina and Oleriina, our results reveal a congruent pattern of diversification related to the Andes with an Andean origin, which contrasts with the Amazonian origin and multiple Andean colonizations of Godyridina. In each of the three subtribes, a clade diversified in the Northern Andes at a faster rate. Diversification within Amazonia occurred in Oleriina and Godyridina, while virtually no speciation occurred in Dircennina in this region. Dircennina was therefore characterized by higher diversification rates within the Andes compared to non-Andean regions, while in Oleriina and Godyridina, we found no difference between these regions. Our results and discussion highlight the importance of comparative approaches in biogeographic studies.

North Andean origin and diversification of the largest ithomiine butterfly genus.

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.

Mutualistic mimicry enhances species diversification through spatial segregation and extension of the ecological niche space.

Species richness varies among clades, yet the drivers of diversification creating this variation remain poorly understood. While abiotic factors likely drive some of the variation in species richness, ecological interactions may also contribute. Here, we examine one class of potential contributors to species richness variation that is particularly poorly understood: mutualistic interactions. We aim to elucidate large-scale patterns of diversification mediated by mutualistic interactions using a spatially explicit population-based model. We focus on mutualistic Müllerian mimicry between conspicuous toxic prey species, where convergence in color patterns emerges from predators' learning process. To investigate the effects of Müllerian mimicry on species diversification, we assume that some speciation events stem from shifts in ecological niches, and can also be associated with shift in mimetic color pattern. Through the emergence of spatial mosaics of mimetic color patterns, Müllerian mimicry constrains the geographical distribution of species and allows different species occupying similar ecological niches to exist simultaneously in different regions. Müllerian mimicry and the resulting spatial segregation of mimetic color patterns thus generate more balanced phylogenetic trees and increase overall species diversity. Our study sheds light on complex effects of Müllerian mimicry on ecological, spatial, and phylogenetic diversification.

Into the Andes: multiple independent colonizations drive montane diversity in the Neotropical clearwing butterflies Godyridina.

Understanding why species richness peaks along the Andes is a fundamental question in the study of Neotropical biodiversity. Several biogeographic and diversification scenarios have been proposed in the literature, but there is confusion about the processes underlying each scenario, and assessing their relative contribution is not straightforward. Here, we propose to refine these scenarios into a framework which evaluates four evolutionary mechanisms: higher speciation rate in the Andes, lower extinction rates in the Andes, older colonization times and higher colonization rates of the Andes from adjacent areas. We apply this framework to a species-rich subtribe of Neotropical butterflies whose diversity peaks in the Andes, the Godyridina (Nymphalidae: Ithomiini). We generated a time-calibrated phylogeny of the Godyridina and fitted time-dependent diversification models. Using trait-dependent diversification models and ancestral state reconstruction methods we then compared different biogeographic scenarios. We found strong evidence that the rates of colonization into the Andes were higher than the other way round. Those colonizations and the subsequent local diversification at equal rates in the Andes and in non-Andean regions mechanically increased the species richness of Andean regions compared to that of non-Andean regions ('species-attractor' hypothesis). We also found support for increasing speciation rates associated with Andean lineages. Our work highlights the importance of the Andean slopes in repeatedly attracting non-Andean lineages, most likely as a result of the diversity of habitats and/or host plants. Applying this analytical framework to other clades will bring important insights into the evolutionary mechanisms underlying the most species-rich biodiversity hotspot on the planet.

Morpho morphometrics: Shared ancestry and selection drive the evolution of wing size and shape in Morpho butterflies.

Butterfly wings harbor highly diverse phenotypes and are involved in many functions. Wing size and shape result from interactions between adaptive processes, phylogenetic history, and developmental constraints, which are complex to disentangle. Here, we focus on the genus Morpho (Nymphalidae: Satyrinae, 30 species), which presents a high diversity of sizes, shapes, and color patterns. First, we generate a comprehensive molecular phylogeny of these 30 species. Next, using 911 collection specimens, we quantify the variation of wing size and shape across species, to assess the importance of shared ancestry, microhabitat use, and sexual selection in the evolution of the wings. While accounting for phylogenetic and allometric effects, we detect a significant difference in wing shape but not size among microhabitats. Fore and hindwings covary at the individual and species levels, and the covariation differs among microhabitats. However, the microhabitat structure in covariation disappears when phylogenetic relationships are taken into account. Our results demonstrate that microhabitat has driven wing shape evolution, although it has not strongly affected forewing and hindwing integration. We also found that sexual dimorphism of forewing shape and color pattern are coupled, suggesting a common selective force.

Mutualistic mimicry and filtering by altitude shape the structure of Andean butterfly communities.

Both the abiotic environment and abiotic interactions among species contribute to shaping species assemblages. While the roles of habitat filtering and competitive interactions are clearly established, less is known about how positive interactions, whereby species benefit from the presence of one another, affect community structure. Here we assess the importance of positive interactions by studying Andean communities of butterflies that interact mutualistically via Müllerian mimicry. We show that communities at similar altitudes have a similar phylogenetic composition, confirming that filtering by altitude is an important process. We also provide evidence that species that interact mutualistically (i.e., species that share the same mimicry wing pattern) coexist at large scales more often than expected by chance. Furthermore, we detect an association between mimicry structure and altitude that is stronger than expected even when phylogeny is corrected for, indicating adaptive convergence for wing pattern and/or altitudinal range driven by mutualistic interactions. Positive interactions extend far beyond Müllerian mimicry, with many examples in plants and animals, and their role in the evolution and assembly of communities may be more pervasive than is currently appreciated. Our findings have strong implications for the evolution and resilience of community structure in a changing world.