Fossil and phylogenetic analyses reveal recurrent periods of diversification and extinction in dictyopteran insects.

Variations of speciation and extinction rates determine the fate of clades through time. Periods of high diversification and extinction (possibly mass-extinction events) can punctuate the evolutionary history of various clades, but they remain loosely defined for many biological groups, especially nonmarine invertebrates like insects. Here, we examine whether the cockroaches, mantises and termites (altogether included in Dictyoptera) have experienced episodic pulses of speciation or extinction and how these pulses may be associated with environmental fluctuations or mass extinctions. We relied on molecular phylogeny and fossil data to shed light on the times and rates at which dictyopterans diversified. The diversification of Dictyoptera has alternated between (i) periods of high diversification in the late Carboniferous, Early-Middle Triassic, Early Cretaceous and middle Palaeogene, and (ii) periods of high extinction rates particularly at the Permian-Triassic boundary, but not necessarily correlated with the major global biodiversity crises as in the mid-Cretaceous. This study advocates the importance of analyzing, when possible, both molecular phylogeny and fossil data to unveil diversification and extinction periods for a given group. The causes and consequences of extinction must be studied beyond mass-extinction events alone to gain a broader understanding of how clades wax and wane.

The Increasing Disconnection of Primary Biodiversity Data from Specimens: How Does It Happen and How to Handle It?

Primary biodiversity data represent the fundamental elements of any study in systematics and evolution. They are, however, no longer gathered as they used to be and the mass-production of observation-based (OB) occurrences is overthrowing the collection of specimen-based (SB) occurrences. Although this change in practice is a major upheaval with significant consequences in the study of biodiversity, it remains understudied and has not attracted yet the attention it deserves. Analyzing 536 million occurrences from the Global Biodiversity Information Facility (GBIF) mediated data, we show that this spectacular change affects the 24 eukaryote taxonomic classes we targeted: from 1970 to 2016 the proportion of occurrences marked as traceable to tangible material (i.e., SB occurrences) fell from 68% to 18%; moreover, most of those specimen based-occurrences cannot be readily traced back to a specimen because the necessary information is missing. Ethical, practical or legal reasons responsible for this shift are known, and this situation appears unlikely to be reversed. Still, we urge scholars to acknowledge this dramatic change, embrace it and actively deal with it. Specifically, we emphasize why SB occurrences must be gathered, as a warrant to allow both repeating evolutionary studies and conducting rich and diverse investigations. When impossible to secure, voucher specimens must be replaced with OB occurrences combined with ancillary data (e.g., pictures, recordings, samples, DNA sequences). Ancillary data are instrumental for the usefulness of biodiversity occurrences and we show that, despite improving technologies to collate them, they remain rarely shared. The consequences of such a change are not yet clear but we advocate collecting material evidence or ancillary data to ensure that primary biodiversity data collected lately do not partly become obsolete when doubtful.

The evolution of sociality in termites from cockroaches: A taxonomic and phylogenetic perspective.

Despite multiple studies and advances, sociality still puzzles evolutionary biologists in numerous ways, which might be partly addressed with the advent of sociogenomics. In insects, the majority of sociogenomic studies deal with Hymenoptera, one of the two groups that evolved eusociality with termites. But, to fully grasp the evolution of sociality, studies must obviously not restrict to eusocial lineages. Multiple kinds of social system transitions have been recorded and they all bring complementary insights. For instance, cockroaches, the closest relatives to termites, display a wide range of social interactions and evolved convergently subsocial behaviors (i.e., brood care). In this context, we emphasize the need for natural history, taxonomic, and phylogenetic studies. Natural history studies provide the foundations on which building hypotheses, whereas taxonomy provides the taxa to sample to test these hypotheses, and phylogenetics brings the historical framework necessary to test evolutionary scenarios of sociality evolution.

A complete insect from the Late Devonian period.

After terrestrialization, the diversification of arthropods and vertebrates is thought to have occurred in two distinct phases, the first between the Silurian and the Frasnian stages (Late Devonian period) (425-385 million years (Myr) ago), and the second characterized by the emergence of numerous new major taxa, during the Late Carboniferous period (after 345 Myr ago). These two diversification periods bracket the depauperate vertebrate Romer's gap (360-345 Myr ago) and arthropod gap (385-325 Myr ago), which could be due to preservational artefact. Although a recent molecular dating has given an age of 390 Myr for the Holometabola, the record of hexapods during the Early-Middle Devonian (411.5-391 Myr ago, Pragian to Givetian stages) is exceptionally sparse and based on fragmentary remains, which hinders the timing of this diversification. Indeed, although Devonian Archaeognatha are problematic, the Pragian of Scotland has given some Collembola and the incomplete insect Rhyniognatha, with its diagnostic dicondylic, metapterygotan mandibles. The oldest, definitively winged insects are from the Serpukhovian stage (latest Early Carboniferous period). Here we report the first complete Late Devonian insect, which was probably a terrestrial species. Its 'orthopteroid' mandibles are of an omnivorous type, clearly not modified for a solely carnivorous diet. This discovery narrows the 45-Myr gap in the fossil record of Hexapoda, and demonstrates further a first Devonian phase of diversification for the Hexapoda, as in vertebrates, and suggests that the Pterygota diversified before and during Romer's gap.

Ten false ideas about New Caledonia biogeography.

The biogeographical paradigm of New Caledonia has recently changed. Although this island is now considered by many as oceanic, its study is still often impeded by some old misconceptions concerning either regional geology or phylogenetic analysis of evolution and biogeography. I discuss ten points that I feel are especially detrimental, to help focus on the real debate and the real questions: (1) its geological history cannot be understood from the basement only; (2) the island submergence was not due simply to sea-level variation; (3) Zealandia/Tasmantis is not a lost continent; (4) short-distance dispersal is not equivalent to permanence on land; (5) long-distance dispersal is not the sole event opposing vicariance, but short-distance dispersal as well; (6) the occurrence of relicts does not prove biota permanence; (7) a major fault system was not observed in New Caledonia; (8) terranes are not rafts; (9) forest climatic refuges do not necessarily equate to centres of endemism or centres of diversity; and (10) New Caledonia is not only a sink but also a source. Study of New Caledonia will need to focus on old and non-relict clades and there is a need to improve the local fossil record.

Laying the foundations of evolutionary and systematic studies in crickets (Insecta, Orthoptera): a multilocus phylogenetic analysis.

Orthoptera have been used for decades for numerous evolutionary questions but several of its constituent groups, notably crickets, still suffer from a lack of a robust phylogenetic hypothesis. We propose the first phylogenetic hypothesis for the evolution of crickets sensu lato, based on analysis of 205 species, representing 88% of the subfamilies and 71% tribes currently listed in the database Orthoptera Species File (OSF). We reconstructed parsimony, maximum likelihood and Bayesian phylogenies using fragments of 18S, 28SA, 28SD, H3, 12S, 16S, and cytb (~3600 bp). Our results support the monophyly of the cricket clade, and its subdivision into two clades: mole crickets and ant-loving crickets on the one hand, and all the other crickets on the other (i.e. crickets sensu stricto). Crickets sensu stricto form seven monophyletic clades, which support part of the OSF families, "subfamily groups", or subfamilies: the mole crickets (OSF Gryllotalpidae), the scaly crickets (OSF Mogoplistidae), and the true crickets (OSF Gryllidae) are recovered as monophyletic. Among the 22 sampled subfamilies, only six are monophyletic: Gryllotalpinae, Trigonidiinae, Pteroplistinae, Euscyrtinae, Oecanthinae, and Phaloriinae. Most of the 37 tribes sampled are para- or polyphyletic. We propose the best-supported clades as backbones for future definitions of familial groups, validating some taxonomic hypotheses proposed in the past. These clades fit variously with the morphological characters used today to identify crickets. Our study emphasizes the utility of a classificatory system that accommodates diagnostic characters and monophyletic units of evolution. Moreover, the phylogenetic hypotheses proposed by the present study open new perspectives for further evolutionary research, especially on acoustic communication and biogeography.

Inside the Melanoplinae: new molecular evidence for the evolutionary history of the Eurasian Podismini (Orthoptera: Acrididae).

The Podismini are melanopline grasshoppers with a Holarctic distribution and well represented in the Eurasian fauna. To investigate their controversial taxonomy and evolutionary history, we studied 86%, 78% and 33% respectively of the Eurasian, European and Asian Palaearctic genera (Otte, 1995; Eades et al., 2013). We reconstructed parsimony, maximum likelihood and Bayesian phylogenies using fragments of four genes (ITS1, 16S, 12S, CO2). We applied a Bayesian molecular clock to estimate the times of species divergence, and the event-based parsimony method to depict the biogeographic framework of the diversification. Our results suggest that the selected Eurasian Podismini constitute a monophyletic group inside the Melanoplinae, provided it includes the North American genus Phaulotettix. The clades proposed by the present study inside the Podismini do not fit the older morphological or cytological classifications, but are in agreement with more recent proposals. Furthermore, our results can be explained by a plausible biogeographic history in which the present geographical distribution of the Eurasian Podismini resulted from known changes, to the Cenozoic climate and vegetation, induced by major geological events including the genesis of high mountain chains (e.g., Himalayas, Altay, Alps) and large deserts (e.g., Gobi, Karakoum, Taklamakan), and the opening of marginal seas (e.g., Bering, Japanese and Yellow Seas).

Phylogenetic analyses of termite post-embryonic sequences illuminate caste and developmental pathway evolution.

Termites are highly eusocial insects with a caste polyphenism (i.e., discontinuous morphological differences between castes) and elaborated behaviors. While the developmental pathways leading to caste occurrence are well-known in many species, the evolutionary origin of these pathways is still obscure. Recent molecular phylogenetic studies suggest multiple independent origins of sterile castes in termites, reviving a 30 years old debate. We demonstrate here that diploid sterile castes ("true" workers) evolved several times independently in this group and that this caste was lost at least once in a lineage with developmentally more flexible workers called pseudergates or "false" workers. We also infer that flexibility in post-embryonic development was acquired multiple times independently during termite evolution. We suggest that focusing on detailed developmental pathways in phylogenetic analyses is essential for elucidating the origin of caste polyphenism in termites.

Mechanisms of high-frequency song generation in brachypterous crickets and the role of ghost frequencies.

Sound production in crickets relies on stridulation, the well-understood rubbing together of a pair of specialised wings. As the file of one wing slides over the scraper of the other, a series of rhythmic impacts causes harmonic oscillations, usually resulting in the radiation of pure tones delivered at low frequencies (2-8 kHz). In the short-winged crickets of the Lebinthini tribe, acoustic communication relies on signals with remarkably high frequencies (>8 kHz) and rich harmonic content. Using several species of the subfamily Eneopterinae, we characterised the morphological and mechanical specialisations supporting the production of high frequencies, and demonstrated that higher harmonics are exploited as dominant frequencies. These specialisations affect the structure of the stridulatory file, the motor control of stridulation and the resonance of the sound radiator. We placed these specialisations in a phylogenetic framework and show that they serve to exploit high-frequency vibrational modes pre-existing in the phylogenetic ancestor. In Eneopterinae, the lower frequency components are harmonically related to the dominant peak, suggesting they are relicts of ancestral carrier frequencies. Yet, such ghost frequencies still occur in the wings' free resonances, highlighting the fundamental mechanical constraints of sound radiation. These results support the hypothesis that such high-frequency songs evolved stepwise, by a form of punctuated evolution that could be related to functional constraints, rather than by only the progressive increase of the ancestral fundamental frequency.

Revisiting Nature's "Unifying Patterns": A Biological Appraisal.

Effective bioinspiration requires dialogue between designers and biologists, and this dialogue must be rooted in a shared scientific understanding of living systems. To support learning from "nature's overarching design lessons" the Biomimicry Institute has produced ten "Unifying Patterns of Nature". These patterns have been developed to engage with those interested in finding biologically inspired solutions to human challenges. Yet, although well-intentioned and appealing, they are likely to dishearten biologists. The aim of this paper is to identify why and propose alternative principles based on evolutionary theory.

Eusocial Transition in Blattodea: Transposable Elements and Shifts of Gene Expression.

(1) Unravelling the molecular basis underlying major evolutionary transitions can shed light on how complex phenotypes arise. The evolution of eusociality, a major evolutionary transition, has been demonstrated to be accompanied by enhanced gene regulation. Numerous pieces of evidence suggest the major impact of transposon insertion on gene regulation and its role in adaptive evolution. Transposons have been shown to be play a role in gene duplication involved in the eusocial transition in termites. However, evidence of the molecular basis underlying the eusocial transition in Blattodea remains scarce. Could transposons have facilitated the eusocial transition in termites through shifts of gene expression? (2) Using available cockroach and termite genomes and transcriptomes, we investigated if transposons insert more frequently in genes with differential expression in queens and workers and if those genes could be linked to specific functions essential for eusocial transition. (3) The insertion rate of transposons differs among differentially expressed genes and displays opposite trends between termites and cockroaches. The functions of termite transposon-rich queen- and worker-biased genes are related to reproduction and ageing and behaviour and gene expression, respectively. (4) Our study provides further evidence on the role of transposons in the evolution of eusociality, potentially through shifts in gene expression.

Mapping extrinsic traits such as extinction risks or modelled bioclimatic niches on phylogenies: does it make sense at all?

An increasing variety of extrinsic traits are used in comparative studies aimed at testing evolutionary hypotheses. After briefly reviewing the relevant literature, it appears that three different problems are implied by this trend. Some extrinsic traits are only surrogates for phenotypic traits, and should be redefined to better fit the requisites for phylogenetic analysis, such as selective regimes and extinction risks. Some others are already adequately defined and cannot be made less extrinsic, such as taxon age, geographical distribution, associates (parasites, symbionts, etc.), and bioclimatic modelled niches. Because they are not heritable, they should not be analysed by optimization onto a tree, but are better considered in sister-group comparisons or within a reconciliation procedure, as already done for areas of biogeography. © The Willi Hennig Society 2010.

Comparison of the gut microbiota from soldier and worker castes of the termite Reticulitermes grassei.

The bacterial microbiota from the whole gut of soldier and worker castes of the termite Reticulitermes grassei was isolated and studied. In addition, the 16S rDNA bacterial genes from gut DNA were PCR-amplified using Bacteria-selective primers, and the 16S rDNA amplicons subsequently cloned into Escherichia coli. Sequences of the cloned inserts were then used to determine closest relatives by comparison with published sequences and with sequences from our previous work. The clones were found to be affiliated with the phyla Spirochaetes, Proteobacteria, Firmicutes, Bacteroidetes, Actinobacteria, Synergistetes, Verrucomicrobia, and candidate phyla Termite Group 1 (TG1) and Termite Group 2 (TG2). No significant differences were observed with respect to the relative bacterial abundances between soldier and worker phylotypes. The phylotypes obtained in this study were compared with reported sequences from other termites, especially those of phylotypes related to Spirochaetes, Wolbachia (an Alphaproteobacteria), Actinobacteria, and TG1. Many of the clone phylotypes detected in soldiers grouped with those of workers. Moreover, clones CRgS91 (soldiers) and CRgW68 (workers), both affiliated with 'Endomicrobia', were the same phylotype. Soldiers and workers also seemed to have similar relative protist abundances. Heterotrophic, poly-ß-hydroxyalkanoate-accumulating bacteria were isolated from the gut of soldiers and shown to be affiliated with Actinobacteria and Gammaproteobacteria. We noted that Wolbachia was detected in soldiers but not in workers. Overall, the maintenance by soldiers and workers of comparable axial and radial redox gradients in the gut is consistent with the similarities in the prokaryotes and protists comprising their microbiota.

Insect decline: immediate action is needed.

Insects appeared more than 400 million years ago and they represent the richest and most diverse taxonomic group with several million species. Yet, under the combined effect of the loss of natural habitats, the intensification of agriculture with massive use of pesticides, global warming and biological invasions, insects show alarming signs of decline. Although difficult to quantify, species extinction and population reductions are confirmed for many ecosystems. This results in a loss of services such as the pollination of plants, including food crops, the recycling of organic matter, the supply of goods such as honey and the stability of food webs. It is therefore urgent to halt the decline of Insects. We recommend implementing long-term monitoring of populations, tackling the causes of insect decline by reducing the use of synthetic insecticides, preserving natural habitats, and reinventing a positive relationship between humans and insects.

Apparus il y a plus de 400 millions d'années, les Insectes représentent le groupe taxonomique le plus riche et diversifié, avec plusieurs millions d'espèces. Sous l'effet de la disparition des habitats, de l'intensification de l'agriculture avec l'usage massif des pesticides, du réchauffement climatique et des invasions biologiques, les Insectes montrent des signes alarmants de déclin. Bien que difficiles à quantifier, la disparition des espèces et la réduction de leurs populations sont avérées et communes à de nombreux écosystèmes. Elles se traduisent par une perte des services rendus, comme la pollinisation des plantes vivrières, le recyclage de la matière organique, la fourniture de biens comme le miel, et l'équilibre des réseaux trophiques. Il est donc urgent de freiner le déclin des Insectes. Pour cela, il faut mettre en œuvre des suivis à long terme des populations, réduire l'usage des insecticides de synthèse, préserver les habitats naturels, et réinventer la relation de l'Homme à l'Insecte en revalorisant son image et ses usages.

New fossil discoveries illustrate the diversity of past terrestrial ecosystems in New Caledonia.

New Caledonia was, until recently, considered an old continental island harbouring a rich biota with outstanding Gondwanan relicts. However, deep marine sedimentation and tectonic evidence suggest complete submergence of the island during the latest Cretaceous to the Paleocene. Molecular phylogenies provide evidence for some deeply-diverging clades that may predate the Eocene and abundant post-Oligocene colonisation events. Extinction and colonization biases, as well as survival of some groups in refuges on neighbouring paleo-islands, may have obscured biogeographic trends over long time scales. Fossil data are therefore crucial for understanding the history of the New Caledonian biota, but occurrences are sparse and have received only limited attention. Here we describe five exceptional fossil assemblages that provide important new insights into New Caledonia's terrestrial paleobiota from three key time intervals: prior to the submersion of the island, following re-emergence, and prior to Pleistocene climatic shifts. These will be of major importance for elucidating changes in New Caledonia's floristic composition over time.

Reconciling the concepts and measures of diversity, rarity and originality in ecology and evolution.

The concept of biological diversity, or biodiversity, is at the core of evolutionary and ecological studies. Many indices of biodiversity have been developed in the last four decades, with species being one of the central units of these indices. However, evolutionary and ecological studies need a precise description of species' characteristics to best quantify inter-species diversity, as species are not equivalent and exchangeable. One of the first concepts characterizing species in biodiversity studies was abundance-based rarity. Abundance-based rarity was then complemented by trait- and phylo-based rarity, called species' trait-based and phylogenetic originalities, respectively. Originality, which is a property of an individual species, represents a species' contribution to the overall diversity of a reference set of species. Originality can also be defined as the rarity of a species' characteristics such as the state of a functional trait, which is often assumed to be represented by the position of the species on a phylogenetic tree. We review and compare various approaches for measuring originality, rarity and diversity and demonstrate that (i) even if attempts to bridge these concepts do exist, only a few ecological and evolutionary studies have tried to combine them all in the past two decades; (ii) phylo- and trait-based diversity indices can be written as a function of species rarity and originality measures in several ways; and (iii) there is a need for the joint use of these three types of indices to understand community assembly processes and species' roles in ecosystem functioning in order to protect biodiversity efficiently.

The phylogeny of termites (Dictyoptera: Isoptera) based on mitochondrial and nuclear markers: Implications for the evolution of the worker and pseudergate castes, and foraging behaviors.

A phylogenetic hypothesis of termite relationships was inferred from DNA sequence data. Seven gene fragments (12S rDNA, 16S rDNA, 18S rDNA, 28S rDNA, cytochrome oxidase I, cytochrome oxidase II and cytochrome b) were sequenced for 40 termite exemplars, representing all termite families and 14 outgroups. Termites were found to be monophyletic with Mastotermes darwiniensis (Mastotermitidae) as sister group to the remainder of the termites. In this remainder, the family Kalotermitidae was sister group to other families. The families Kalotermitidae, Hodotermitidae and Termitidae were retrieved as monophyletic whereas the Termopsidae and Rhinotermitidae appeared paraphyletic. All of these results were very stable and supported with high bootstrap and Bremer values. The evolution of worker caste and foraging behavior were discussed according to the phylogenetic hypothesis. Our analyses suggested that both true workers and pseudergates ("false workers") were the result of at least two different origins. Our data support a traditional hypothesis of foraging behavior, in which the evolutionary transition from a one-piece type to a separate life type occurred through an intermediate behavioral form.

Taxonomic revision of the genus Monastria Saussure, 1864 (Blattodea: Blaberidae, Blaberinae) from the South American Atlantic forest, with the descriptions of five new species.

 The genus Monastria Saussure, 1864 includes medium to large sized (40-55 mm) dark brown or black cockroaches found in the understory of the Neotropical Atlantic Forest from the Northeast of Brazil to Paraguay and Argentina. The genus shows evident sexual dimorphism: males are elongated with fully developed wings extending beyond the apex of cerci and females are oval and brachypterous. This study is a revision of the genus with redescription of the three already known species, Monastria biguttata (Thunberg, 1826), Monastria similis (Serville, 1838) and Monastria angulata Saussure, 1864, and description of five new ones, Monastria itubera sp. n. and Monastria itabuna sp. n. from state of Bahia, Monastria cabocla sp. n. from state of Sergipe, Monastria kaingangue sp. n. from state of São Paulo and Monastria sagittata sp. n. from state of Minas Gerais. The morphology of the genus and all species is described in details, including male genitalia. Based on this revision, we proposed a new combination for Hiereoblatta papillosa (Thunberg, 1826) comb. n., excluding it from the genus Monastria. For the first time, the juvenile stages of Monastria are characterized and compared to other genera of Blaberinae of the Atlantic forest. Three determination keys are provided. The two first are aimed at identifying the adults and juvenile stages of the five genera of the Blaberinae radiation endemic to the Atlantic forest, respectively. The third concerns the identification of the species of the genus Monastria. A map indicating the localities where species were sampled is also provided.

The informative value of museum collections for ecology and conservation: A comparison with target sampling in the Brazilian Atlantic forest.

Since two decades the richness and potential of natural history collections (NHC) were rediscovered and emphasized, promoting a revolution in the access on data of species occurrence, and fostering the development of several disciplines. Nevertheless, due to their inherent erratic nature, NHC data are plagued by several biases. Understanding these biases is a major issue, particularly because ecological niche models (ENMs) are based on the assumption that data are not biased. Based on it, a recent body of research have focused on searching adequate methods for dealing with biased data and proposed the use of filters in geographical and environmental space. Although the strength of filtering in environmental space has been shown with virtual species, nothing has yet been tested with a real dataset including field validation. In order to contribute to this task, we explore this issue by comparing a dataset from NHC to a recent targeted sampling of the cockroach genus Monastria Saussure, 1864 in the Brazilian Atlantic forest. We showed that, despite strong similarities, the area modeled with NHC data was much smaller. These differences were due to strong climate biases, which increased model's specificity and reduced sensitivity. By applying two forms of rarefaction in the environmental space, we showed that deleting points at random in the most biased climate class is a powerful way for increasing model's sensitivity, so making predictions more suitable to the reality.

Parsimony analysis and ecological communities, phytosociology, nested subsets analysis, forest fragmentation: a reply to Giannini and Keller.

We suggested using parsimony analysis to study community evolution in terms of species composition and to apply these results in the context of forest fragmentation as a replacement for the so-called "nested subsets analysis" or other phenetic synecological or phytosociological methods (Pellens et al., 2005). Giannini and Keller (2007) took issue with this new application on the basis of three misunderstandings. We re-emphasize that communities themselves are analyzed, not landscape parts such as forest fragments. Therefore, it must be clear that communities are analogous to taxa and landscape parts such as fragments are analogous to distributions of taxa. Community evolution is the change in community composition by immigration, emigration and local extinction. Thus, gains and losses of species should not be confused with horizontal transfer. Parsimony analysis does not necessarily group communities based on shared absences of rare species. Rare species are not necessarily absent in the same communities and these absences are not necessarily inferred to be synapomorphies after rooting. This is the main advance expected when cladistics is used instead of the previously cited phenetic methods working with overall similarity.