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.
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•This molecular study is aimed at understanding the diversity of of Boarmiini moths.•We inferred the evolution of Boarmiini with 346 taxa, up to eight gene regions.•The monophyly of ...Boarmiini and major genera is supported after taxonomic adjustments.•Most of the species have diversified relatively constant through time, but Cleora.•Biogeography suggests Holarctic origin. Dispersals to Africa and Australia through Asia.
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.
Multiple studies have demonstrated that partitioning of molecular datasets is important in model-based phylogenetic analyses. Commonly, partitioning is done
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.
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
-means. Different partitioning strategies were evaluated using BIC scores as calculated by PartitionFinder.
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.
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.
Eyespots are wing color pattern elements repeatedly observed in many butterflies,whose developmental genetics has been extensively documented. Nevertheless, theevolutionary forces shaping their ...diversification across species still remain largelyunknown. Here we investigate the evolution of eyespots in the 30 species of theneotropical genus Morpho. Morpho butterflies display a series of eyespots locatedon the ventral side of their wings, highly variable among species, ranging from large,conspicuous structures to vestigial spots. Applying geometric morphometrics to a largesample (N = 910) spanning all Morpho species and both sexes, we assess eyespotnumber, position, size, and shape. We detect a divergence in eyespot position betweenunderstory and canopy species, with an L-shaped configuration in canopy species anda line pattern in understory species, where the eyespots tend to fuse and form a stripein white and pale species. This effect is stronger than expected based on a Brownianmotion model of phylogenetic divergence, suggesting an adaptation to the microhabitatand an influence of the wing color on the evolution of pattern elements. Remarkably,this shift in color pattern is strongly correlated with a shift in wing shape. However,using a thin-plate spline interpolation, we show that the shape change is insufficientto explain the evolution of eyespot position as a developmental side effect of wingshape evolution, also pointing at an adaptive effect. Finally, we find a significant negativecorrelation between eyespot relative size and the within-species variation in eyespotnumber, position, size, and shape, suggesting a relaxed or apostatic selection on smalleyespots (rare phenotypes being favored as they are less likely to be remembered andthus detected by predators). We hypothesize that contrasted ecology may explain theobserved differences between species: large and phenotypically stable eyespots mightact as attack deflectors, small, variable faded eyespots might rather enhance crypsis,and pale species stripe pattern might disrupt the outline of the wing.
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.
Combining ecology, biogeography, phenotypes and phylogeny of the Neotropical Morpho butterflies, we show that microhabitat conditions explain correlated changes in host‐plants, rates of wing evolution and species diversification.
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. Butterflies; Early Cretaceous; fossils; host plants; marginal prior; Papilionoidea; time-calibration.
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.
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.
Mutualistic interactions shape global spatial patterns and climatic niche evolution in Neotropical mimetic butterflies: mimicry turnover at the continental scale demonstrates large‐scale spatial congruence of phenotypically similar ithomiine butterflies (Nymphalidae: Danainae) associated with the climatic niche convergence of mimetic species.
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.
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