Forest disturbance increases functional diversity but decreases phylogenetic diversity of an arboreal tropical ant community.

Tropical rainforest trees host a diverse arthropod fauna that can be characterised by their functional diversity (FD) and phylogenetic diversity (PD). Human disturbance degrades tropical forests, often coinciding with species invasion and altered assembly that leads to a decrease in FD and PD. Tree canopies are thought to be particularly vulnerable, but rarely investigated. Here, we studied the effects of forest disturbance on an ecologically important invertebrate group, the ants, in a lowland rainforest in New Guinea. We compared an early successional disturbed plot (secondary forest) to an old-growth plot (primary forest) by exhaustively sampling their ant communities in a total of 852 trees. We expected that for each tree community (1) disturbance would decrease FD and PD in tree-dwelling ants, mediated through species invasion. (2) Disturbance would decrease ant trait variation due to a more homogeneous environment. (3) The main drivers behind these changes would be different contributions of true tree-nesting species and visiting species. We calculated FD and PD based on a species-level phylogeny and 10 ecomorphological traits. Furthermore, we assessed by data exclusion the influence of species, which were not nesting in individual trees (visitors) or only nesting species (nesters), and of non-native species on FD and PD. Primary forests had higher ant species richness and PD than secondary forest. However, we consistently found increased FD in secondary forest. This pattern was robust even if we decoupled functional and phylogenetic signals, or if non-native ant species were excluded from the data. Visitors did not contribute strongly to FD, but they increased PD and their community weighted trait means often varied from nesters. Moreover, all community-weighted trait means changed after forest disturbance. Our finding of contradictory FD and PD patterns highlights the importance of integrative measures of diversity. Our results indicate that the tree community trait diversity is not negatively affected, but possibly even enhanced by disturbance. Therefore, the functional diversity of arboreal ants is relatively robust when compared between old-growth and young trees. However, further study with higher plot-replication is necessary to solidify and generalise our findings.

Contrasting levels of ß-diversity and underlying phylogenetic trends indicate different paths to chemical diversity in highland and lowland willow species.

Diverse specialised metabolites contributed to the success of vascular plants in colonising most terrestrial habitats. Understanding how distinct aspects of chemical diversity arise through heterogeneous environmental pressures can help us understand the effects of abiotic and biotic stress on plant evolution and community assembly. We examined highland and lowland willow species within a phylogenetic framework to test for trends in their chemical α-diversity (richness) and ß-diversity (variation among species sympatric in elevation). We show that differences in chemistry among willows growing at different elevations occur mainly through shifts in chemical ß-diversity and due to convergence or divergence among species sharing their elevation level. We also detect contrasting phylogenetic trends in concentration and α-diversity of metabolites in highland and lowland willow species. The resulting elevational patterns contribute to the chemical diversity of willows and suggest that variable selective pressure across ecological gradients may, more generally, underpin complex changes in plant chemistry.

Body size, not species identity, drives body heating in alpine Erebia butterflies.

Efficient thermoregulation is crucial for animals living under fluctuating climatic and weather conditions. We studied the body heating of six butterfly species of the genus Erebia (Lepidoptera: Nymphalidae) that co-occur in the European Alps. We tested whether butterfly physical characteristics (body size, wing loading) are responsible for the inter-specific differences in body temperatures recorded previously under natural conditions. We used a thermal camera to measure body heating of wild butterfly individuals in a laboratory experiment with artificial light and heating sources. We revealed that physical characteristics had a small effect on explaining inter-specific differences in mean body temperatures recorded in the field. Our results show that larger butterflies, with higher weight and wing loading, heated up more slowly but reached the same asymptotic body temperature as smaller butterflies. Altogether, our results suggest that differences in body temperatures among Erebia species observed in the field might be caused mainly by species-specific microhabitat use and point towards an important role of active behavioural thermoregulation in adult butterflies. We speculate that microclimate heterogeneity in mountain habitats facilitates behavioural thermoregulation of adults. Similarly, microclimate structuring might also increase survival of less mobile butterfly life stages, i.e., eggs, larvae and pupae. Thus, landscape heterogeneity in management practices may facilitate long term survival of montane invertebrates under increased anthropogenic pressures.

Madagascar's extraordinary biodiversity: Evolution, distribution, and use.

Madagascar's biota is hyperdiverse and includes exceptional levels of endemicity. We review the current state of knowledge on Madagascar's past and current terrestrial and freshwater biodiversity by compiling and presenting comprehensive data on species diversity, endemism, and rates of species description and human uses, in addition to presenting an updated and simplified map of vegetation types. We report a substantial increase of records and species new to science in recent years; however, the diversity and evolution of many groups remain practically unknown (e.g., fungi and most invertebrates). Digitization efforts are increasing the resolution of species richness patterns and we highlight the crucial role of field- and collections-based research for advancing biodiversity knowledge and identifying gaps in our understanding, particularly as species richness corresponds closely to collection effort. Phylogenetic diversity patterns mirror that of species richness and endemism in most of the analyzed groups. We highlight humid forests as centers of diversity and endemism because of their role as refugia and centers of recent and rapid radiations. However, the distinct endemism of other areas, such as the grassland-woodland mosaic of the Central Highlands and the spiny forest of the southwest, is also biologically important despite lower species richness. The documented uses of Malagasy biodiversity are manifold, with much potential for the uncovering of new useful traits for food, medicine, and climate mitigation. The data presented here showcase Madagascar as a unique "living laboratory" for our understanding of evolution and the complex interactions between people and nature. The gathering and analysis of biodiversity data must continue and accelerate if we are to fully understand and safeguard this unique subset of Earth's biodiversity.

Madagascar's extraordinary biodiversity: Threats and opportunities.

Madagascar's unique biota is heavily affected by human activity and is under intense threat. Here, we review the current state of knowledge on the conservation status of Madagascar's terrestrial and freshwater biodiversity by presenting data and analyses on documented and predicted species-level conservation statuses, the most prevalent and relevant threats, ex situ collections and programs, and the coverage and comprehensiveness of protected areas. The existing terrestrial protected area network in Madagascar covers 10.4% of its land area and includes at least part of the range of the majority of described native species of vertebrates with known distributions (97.1% of freshwater fishes, amphibians, reptiles, birds, and mammals combined) and plants (67.7%). The overall figures are higher for threatened species (97.7% of threatened vertebrates and 79.6% of threatened plants occurring within at least one protected area). International Union for Conservation of Nature (IUCN) Red List assessments and Bayesian neural network analyses for plants identify overexploitation of biological resources and unsustainable agriculture as the most prominent threats to biodiversity. We highlight five opportunities for action at multiple levels to ensure that conservation and ecological restoration objectives, programs, and activities take account of complex underlying and interacting factors and produce tangible benefits for the biodiversity and people of Madagascar.

A bioinformatic platform to integrate target capture and whole genome sequences of various read depths for phylogenomics.

The increasing availability of short-read whole genome sequencing (WGS) provides unprecedented opportunities to study ecological and evolutionary processes. Although loci of interest can be extracted from WGS data and combined with target sequence data, this requires suitable bioinformatic workflows. Here, we test different assembly and locus extraction strategies and implement them into secapr, a pipeline that processes short-read data into multilocus alignments for phylogenetics and molecular ecology analyses. We integrate the processing of data from low-coverage WGS (<30×) and target sequence capture into a flexible framework, while optimizing de novo contig assembly and loci extraction. Specifically, we test different assembly strategies by contrasting their ability to recover loci from targeted butterfly protein-coding genes, using four data sets: a WGS data set across different average coverages (10×, 5× and 2×) and a data set for which these loci were enriched prior to sequencing via target sequence capture. Using the resulting de novo contigs, we account for potential errors within contigs and infer phylogenetic trees to evaluate the ability of each assembly strategy to recover species relationships. We demonstrate that choosing multiple sizes of kmer simultaneously for assembly results in the highest yield of extracted loci from de novo assembled contigs, while data sets derived from sequencing read depths as low as 5× recovers the expected species relationships in phylogenetic trees. By making the tested assembly approaches available in the secapr pipeline, we hope to inspire future studies to incorporate complementary data and make an informed choice on the optimal assembly strategy.

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.

Hard to catch: experimental evidence supports evasive mimicry.

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 Adelpha 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 Adelpha 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 Adelpha 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.

An "omics" approach to bridge community ecology and island biogeography.

Understanding the dynamics of communities in space and time requires reconciling ecological and evolutionary processes, including colonization, adaptation, speciation and extinction. In practice, this has been challenging because empirical data obtained by traditional methods and predictive models typically focus on particular processes driving local community assembly and biogeographical structure. In this issue of Molecular Ecology, by using phylogenomics, population genomics and phenomics approaches, Darwell et al. show that ant community assembly on islands is governed by predictable eco-evolutionary trends of geographical range expansion, adaptive radiation and local population decline. The authors provide one of the most robust lines of evidence that the evolutionary progression of island communities may often be directional and repeatable, as predicted by the concept of taxon cycles.

The Global Museum: natural history collections and the future of evolutionary science and public education.

Natural history museums are unique spaces for interdisciplinary research and educational innovation. Through extensive exhibits and public programming and by hosting rich communities of amateurs, students, and researchers at all stages of their careers, they can provide a place-based window to focus on integration of science and discovery, as well as a locus for community engagement. At the same time, like a synthesis radio telescope, when joined together through emerging digital resources, the global community of museums (the 'Global Museum') is more than the sum of its parts, allowing insights and answers to diverse biological, environmental, and societal questions at the global scale, across eons of time, and spanning vast diversity across the Tree of Life. We argue that, whereas natural history collections and museums began with a focus on describing the diversity and peculiarities of species on Earth, they are now increasingly leveraged in new ways that significantly expand their impact and relevance. These new directions include the possibility to ask new, often interdisciplinary questions in basic and applied science, such as in biomimetic design, and by contributing to solutions to climate change, global health and food security challenges. As institutions, they have long been incubators for cutting-edge research in biology while simultaneously providing core infrastructure for research on present and future societal needs. Here we explore how the intersection between pressing issues in environmental and human health and rapid technological innovation have reinforced the relevance of museum collections. We do this by providing examples as food for thought for both the broader academic community and museum scientists on the evolving role of museums. We also identify challenges to the realization of the full potential of natural history collections and the Global Museum to science and society and discuss the critical need to grow these collections. We then focus on mapping and modelling of museum data (including place-based approaches and discovery), and explore the main projects, platforms and databases enabling this growth. Finally, we aim to improve relevant protocols for the long-term storage of specimens and tissues, ensuring proper connection with tomorrow's technologies and hence further increasing the relevance of natural history museums.

Biodiversity seen through the perspective of insects: 10 simple rules on methodological choices and experimental design for genomic studies.

Massively parallel DNA sequencing opens up opportunities for bridging multiple temporal and spatial dimensions in biodiversity research, thanks to its efficiency to recover millions of nucleotide polymorphisms. Here, we identify the current status, discuss the main challenges, and look into future perspectives on biodiversity genomics focusing on insects, which arguably constitute the most diverse and ecologically important group among all animals. We suggest 10 simple rules that provide a succinct step-by-step guide and best-practices to anyone interested in biodiversity research through the study of insect genomics. To this end, we review relevant literature on biodiversity and evolutionary research in the field of entomology. Our compilation is targeted at researchers and students who may not yet be specialists in entomology or molecular biology. We foresee that the genomic revolution and its application to the study of non-model insect lineages will represent a major leap to our understanding of insect diversity.

A Guide to Carrying Out a Phylogenomic Target Sequence Capture Project.

High-throughput DNA sequencing techniques enable time- and cost-effective sequencing of large portions of the genome. Instead of sequencing and annotating whole genomes, many phylogenetic studies focus sequencing effort on large sets of pre-selected loci, which further reduces costs and bioinformatic challenges while increasing coverage. One common approach that enriches loci before sequencing is often referred to as target sequence capture. This technique has been shown to be applicable to phylogenetic studies of greatly varying evolutionary depth. Moreover, it has proven to produce powerful, large multi-locus DNA sequence datasets suitable for phylogenetic analyses. However, target capture requires careful considerations, which may greatly affect the success of experiments. Here we provide a simple flowchart for designing phylogenomic target capture experiments. We discuss necessary decisions from the identification of target loci to the final bioinformatic processing of sequence data. We outline challenges and solutions related to the taxonomic scope, sample quality, and available genomic resources of target capture projects. We hope this review will serve as a useful roadmap for designing and carrying out successful phylogenetic target capture studies.

Conceptual and empirical advances in Neotropical biodiversity research.

The unparalleled biodiversity found in the American tropics (the Neotropics) has attracted the attention of naturalists for centuries. Despite major advances in recent years in our understanding of the origin and diversification of many Neotropical taxa and biotic regions, many questions remain to be answered. Additional biological and geological data are still needed, as well as methodological advances that are capable of bridging these research fields. In this review, aimed primarily at advanced students and early-career scientists, we introduce the concept of "trans-disciplinary biogeography," which refers to the integration of data from multiple areas of research in biology (e.g., community ecology, phylogeography, systematics, historical biogeography) and Earth and the physical sciences (e.g., geology, climatology, palaeontology), as a means to reconstruct the giant puzzle of Neotropical biodiversity and evolution in space and time. We caution against extrapolating results derived from the study of one or a few taxa to convey general scenarios of Neotropical evolution and landscape formation. We urge more coordination and integration of data and ideas among disciplines, transcending their traditional boundaries, as a basis for advancing tomorrow's ground-breaking research. Our review highlights the great opportunities for studying the Neotropical biota to understand the evolution of life.

Taxon cycle predictions supported by model-based inference in Indo-Pacific trap-jaw ants (Hymenoptera: Formicidae: Odontomachus).

Nonequilibrium dynamics and non-neutral processes, such as trait-dependent dispersal, are often missing from quantitative island biogeography models despite their potential explanatory value. One of the most influential nonequilibrium models is the taxon cycle, but it has been difficult to test its validity as a general biogeographical framework. Here, we test predictions of the taxon cycle model using six expected phylogenetic patterns and a time-calibrated phylogeny of Indo-Pacific Odontomachus (Hymenoptera: Formicidae: Ponerinae), one of the ant genera that E.O. Wilson used when first proposing the hypothesis. We used model-based inference and a newly developed trait-dependent dispersal model to jointly estimate ancestral biogeography, ecology (habitat preferences for forest interiors, vs. "marginal" habitats, such as savannahs, shorelines, disturbed areas) and the linkage between ecology and dispersal rates. We found strong evidence that habitat shifts from forest interior to open and disturbed habitats increased macroevolutionary dispersal rate. In addition, lineages occupying open and disturbed habitats can give rise to both island endemics re-occupying only forest interiors and taxa that re-expand geographical ranges. The phylogenetic predictions outlined in this study can be used in future work to evaluate the relative weights of neutral (e.g., geographical distance and area) and non-neutral (e.g., trait-dependent dispersal) processes in historical biogeography and community ecology.

An ant genus-group (Prenolepis) illuminates the biogeography and drivers of insect diversification in the Indo-Pacific.

The Malay Archipelago and the tropical South Pacific (hereafter the Indo-Pacific region) are considered biodiversity hotspots, yet a general understanding of the origins and diversification of species-rich groups in the region remains elusive. We aimed to test hypotheses for the evolutionary processes driving insect species diversity in the Indo-Pacific using a higher-level and comprehensive phylogenetic hypothesis for an ant clade consisting of seven genera. We estimated divergence times and reconstructed the biogeographical history of ant species in the Prenolepis genus-group (Formicidae: Formicinae: Lasiini). We used a fossil-calibrated phylogeny to infer ancestral geographical ranges utilizing a biogeographic model that includes founder-event speciation. Ancestral state reconstructions of the ants' ecological preferences, and diversification rates were estimated for selected Indo-Pacific clades. Overall, we report that faunal interchange between Asia and Australia has occurred since at least 20-25 Ma, and early dispersal to the Fijian Basin happened during the early and mid-Miocene (ca. 10-20 Ma). Differences in diversification rates across Indo-Pacific clades may be related to ecological preference breadth, which in turn may have facilitated geographical range expansions. Ancient dispersal routes suggested by our results agree with the palaeogeography of the region. For this particular group of ants, the rapid orogenesis in New Guinea and possibly subsequent ecological shifts may have promoted their rapid diversification and widespread distribution across the Indo-Pacific.

Molecular phylogenetics and diversification of trap-jaw ants in the genera Anochetus and Odontomachus (Hymenoptera: Formicidae).

Ants in the genera Anochetus and Odontomachus belong to one of the largest clades in the subfamily Ponerinae, and are one of four lineages of ants possessing spring-loaded "trap-jaws." Here we present results from the first global species-level molecular phylogenetic analysis of these trap-jaw ants, reconstructed from one mitochondrial, one ribosomal RNA, and three nuclear protein-coding genes. Bayesian and likelihood analyses strongly support reciprocal monophyly for the genera Anochetus and Odontomachus. Additionally, we found strong support for seven trap-jaw ant clades (four in Anochetus and three in Odontomachus) mostly concordant with geographic distribution. Ambiguity remains concerning the closest living non-trap-jaw ant relative of the Anochetus+Odontomachus clade, but Bayes factor hypothesis testing strongly suggests that trap-jaw ants evolved from a short mandible ancestor. Ponerine trap-jaw ants originated in the early Eocene (52.5Mya) in either South America or Southeast Asia, where they have radiated rapidly in the last 30million years, and subsequently dispersed multiple times to Africa and Australia. These results will guide future taxonomic work on the group and act as a phylogenetic framework to study the macroevolution of extreme ant mouthpart specialization.

Investigating the timing of origin and evolutionary processes shaping regional species diversity: Insights from simulated data and neotropical butterfly diversification rates.

Different diversification scenarios have been proposed to explain the origin of extant biodiversity. However, most existing meta-analyses of time-calibrated phylogenies rely on approaches that do not quantitatively test alternative diversification processes. Here, I highlight the shortcomings of using species divergence ranks, which is a method widely used in meta-analyses. Divergence ranks consist of categorizing cladogenetic events to certain periods of time, typically to either Pleistocene or to pre-Pleistocene ages. This approach has been claimed to shed light on the origin of most extant species and the timing and dynamics of diversification in any biogeographical region. However, interpretations drawn from such method often confound two fundamental questions in macroevolutionary studies, tempo (timing of evolutionary rate shifts) and mode ("how" and "why" of speciation). By using simulated phylogenies under four diversification scenarios, constant-rate, diversity-dependence, high extinction, and high speciation rates in the Pleistocene, I showed that interpretations based on species divergence ranks might have been seriously misleading. Future meta-analyses of dated phylogenies need to be aware of the impacts of incomplete taxonomic sampling, tree topology, and divergence time uncertainties, as well as they might be benefited by including quantitative tests of alternative diversification models that acknowledge extinction and diversity dependence.

Causes of endemic radiation in the Caribbean: evidence from the historical biogeography and diversification of the butterfly genus Calisto (Nymphalidae: Satyrinae: Satyrini).

BACKGROUND: Calisto is the largest butterfly genus in the West Indies but its systematics, historical biogeography and the causes of its diversification have not been previously rigorously evaluated. Several studies attempting to explain the wide-ranging diversity of Calisto gave different weights to vicariance, dispersal and adaptive radiation. We utilized molecular phylogenetic approaches and secondary calibrations points to estimate lineage ages. In addition, we used the dispersal-extinction-cladogenesis model and Caribbean paleogeographical information to reconstruct ancestral geographical distributions. We also evaluated different models of diversification to estimate the dynamics of lineage radiation within Calisto. By understanding the evolution of Calisto butterflies, we attempt to identify the main processes acting on insular insect diversity and the causes of its origin and its maintenance. RESULTS: The crown age of Calisto was estimated to the early Oligocene (31 ± 5 Ma), and a single shift in diversification rate following a diversity-dependent speciation process was the best explanation for the present-day diversity found within the genus. A major increase in diversification rate was recovered at 14 Ma, following geological arrangements that favoured the availability of empty niches. Inferred ancestral distributional ranges suggested that the origin of extant Calisto is in agreement with a vicariant model and the origin of the Cuban lineage was likely the result of vicariance caused by the Cuba-Hispaniola split. A long-distance dispersal was the best explanation for the colonization of Jamaica and the Bahamas. CONCLUSIONS: The ancestral geographical distribution of Calisto is in line with the paleogeographical model of Caribbean colonization, which favours island-to-island vicariance. Because the sister lineage of Calisto remains ambiguous, its arrival to the West Indies remains to be explained, although, given its age and historical biogeography, the hypothesized GAARlandia land bridge might have been a plausible introduction route from continental America. Intra-island radiation caused by ecological innovation and the abiotic creation of niche spaces was found to be the main force shaping Calisto diversity and island endemism in Hispaniola and Cuba.

Permanent genetic resources added to Molecular Ecology Resources Database 1 February 2013-31 March 2013.

This article documents the addition of 142 microsatellite marker loci to the Molecular Ecology Resources database. Loci were developed for the following species: Agriophyllum squarrosum, Amazilia cyanocephala, Batillaria attramentaria, Fungal strain CTeY1 (Ascomycota), Gadopsis marmoratus, Juniperus phoenicea subsp. turbinata, Liriomyza sativae, Lupinus polyphyllus, Metschnikowia reukaufii, Puccinia striiformis and Xylocopa grisescens. These loci were cross-tested on the following species: Amazilia beryllina, Amazilia candida, Amazilia rutila, Amazilia tzacatl, Amazilia violiceps, Amazilia yucatanensis, Campylopterus curvipennis, Cynanthus sordidus, Hylocharis leucotis, Juniperus brevifolia, Juniperus cedrus, Juniperus osteosperma, Juniperus oxycedrus, Juniperus thurifera, Liriomyza bryoniae, Liriomyza chinensis, Liriomyza huidobrensis and Liriomyza trifolii.

New Calisto species from Cuba, with insights on the relationships of Cuban and Bahamian taxa (Lepidoptera, Nymphalidae, Satyrinae).

Three new species and a new subspecies of Calisto Hübner are described from Cuba, Calisto torrei sp. n. Núñez, Calisto dissimulatum sp. n. Núñez, Calisto aquilum sp. n. Núñez, and Calisto aquilum occidentalis ssp. n. Núñez. The immature stages of C. torrei and C. dissimulatum are also described. Notes on the distribution and biology of the species are given. All Cuban and Bahamian taxa form a monophyletic group which seems to have originated in northeastern Cuba spreading later to the west. DNA sequence data also allowed to recognize both Bahamian taxa, Calisto sibylla and Calisto apollinis stat. n., as distinct species, and to synonymize Calisto herophile parsonsi syn. n. under Calisto herophile.