Fossil amber reveals springtails' longstanding dispersal by social insects.

BACKGROUND: Dispersal is essential for terrestrial organisms living in disjunct habitats and constitutes a significant challenge for the evolution of wingless taxa. Springtails (Collembola), the sister-group of all insects (with Diplura), are reported since the Lower Devonian and are thought to have originally been subterranean. The order Symphypleona is reported since the early Cretaceous with genera distributed on every continent. This distribution implies an ability to disperse over oceans, however symphypleonan Collembola have never been reported in marine water contrary to other springtail orders. Despite being highly widespread, modern springtails are rarely reported in any kind of biotic association. Interestingly, the fossil record has provided occasional occurrences of Symphypleona attached by the antennae onto the bodies of larger arthropods. RESULTS: Here, we document the case of a ~ 16 Ma old fossil association: a winged termite and ant displaying not some, but 25 springtails attached or in close proximity to the body. The collembola exhibit rare features for fossils, reflecting their courtship and phoretic behaviours. By observing the modes of attachment of springtails on different arthropods, the sex representation and ratios in springtail antennal anatomies in new and previously reported cases, we infer a likely mechanism for dispersal in Symphypleona. By revealing hidden evidence of modern springtail associations with other invertebrates such as ants and termites, new compelling assemblages of fossil springtails, and the drastic increase of eusocial insects' abundance during the Cenozoic (ants/termites comprising more than a third of insects in Miocene amber), we stress that attachment on winged castes of ants and termites may have been a mechanism for the worldwide dispersal of this significant springtail lineage. Moreover, by comparing the general constraints applying to the other wingless soil-dwelling arthropods known to disperse through phoresy, we suggest biases in the collection and observation of phoretic Symphypleona related to their reflexive detachment and infer that this behaviour continues today. CONCLUSIONS: The specific case of tree resin entrapment represents the (so far) only condition uncovering the phoretic dispersal mechanism of springtails - one of the oldest terrestrial arthropod lineages living today.

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.

Phylogeny of the genus Willemia (Collembola: Hypogastruridae) and biogeography of the W. buddenbrocki-group with description of a new species from Ivory Coast (western Africa).

Willemia tondoh sp. nov. from the Ivory Coast (western Africa) is described and illustrated. The new species is the 14th in the buddenbrocki-group and is defined with two large globular sensilla placed in a cavity and covered in part by tegumental fold on antennal segment IV, 7 chaetae on antennal segment I, postantennal organ with 9 vesicles, s-chaetae subcylindrical and acuminate on abdominal terga and chaetae a1 absent on abdominal sternum IV. A phylogeny for all the 46 species of the genus Willemia is proposed. Based on the phylogentic framework, the biogeography of the buddenbrocki-group is discussed. An identification key for all 46 known species of the genus is provided.

A new group of species of the genus Megalothorax (Collembola, Neelidae) with Gondwanan distribution, and introducing an open interactive identification key of Megalothorax species.

Megalothorax Willem, 1900 is a genus of Neelidae (Collembola) with worldwide distribution. Three new species are described here: Megalothorax anterolenis sp. nov. (Patagonia, Chile), Megalothorax tasmanterolenis sp. nov. (Tasmania, Australia) and Megalothorax zealanterolenis sp. nov. (the South Island, New Zealand). New descriptive elements are also provided for Megalothorax rubidus. Two of the new species were sequenced (COI, 16S rDNA, 28S rDNA). Within the genus, the three new species form a new group of species characterised by the absence of secondary granulation dorsally on the head and the thorax, a reduced chaetotaxy of the basomedian field of labium, a bifurcate hair on the maxillary outer lobe and an enlarged S-chaeta (Sa2) on Ant. IV. The molecular based phylogeny further supports the sistership of the two sequenced species. The possible Gondwanan origin of the new group is discussed. Elements of discussion are also provided regarding the possible function of the incomplete coverage of secondary granulation. Finally, an open interactive identification key for the Megalothorax species of the world is introduced.

Wolbachia springs eternal: symbiosis in Collembola is associated with host ecology.

Wolbachia are endosymbiotic alpha-proteobacteria infecting a wide range of arthropods and nematode hosts with diverse interactions, from reproductive parasites to obligate mutualists. Their taxonomy is defined by lineages called supergroups (labelled by letters of the alphabet), while their evolutionary history is complex, with multiple horizontal transfers and secondary losses. One of the least recently derived, supergroup E, infects springtails (Collembola), widely distributed hexapods, with sexual and/or parthenogenetic populations depending on species. To better characterize the diversity of Wolbachia infecting springtails, the presence of Wolbachia was screened in 58 species. Eleven (20%) species were found to be positive, with three Wolbachia genotypes identified for the first time in supergroup A. The novel genotypes infect springtails ecologically and biologically different from those infected by supergroup E. To root the Wolbachia phylogeny, rather than distant other Rickettsiales, supergroup L infecting plant-parasitic nematodes was used here. We hypothesize that the ancestor of Wolbachia was consumed by soil-dwelling nematodes, and was transferred horizontally via plants into aphids, which then infected edaphic arthropods (e.g. springtails and oribatid mites) before expanding into most clades of terrestrial arthropods and filarial nematodes.

Two high-quality de novo genomes from single ethanol-preserved specimens of tiny metazoans (Collembola).

BACKGROUND: Genome sequencing of all known eukaryotes on Earth promises unprecedented advances in biological sciences and in biodiversity-related applied fields such as environmental management and natural product research. Advances in long-read DNA sequencing make it feasible to generate high-quality genomes for many non-genetic model species. However, long-read sequencing today relies on sizable quantities of high-quality, high molecular weight DNA, which is mostly obtained from fresh tissues. This is a challenge for biodiversity genomics of most metazoan species, which are tiny and need to be preserved immediately after collection. Here we present de novo genomes of 2 species of submillimeter Collembola. For each, we prepared the sequencing library from high molecular weight DNA extracted from a single specimen and using a novel ultra-low input protocol from Pacific Biosciences. This protocol requires a DNA input of only 5 ng, permitted by a whole-genome amplification step. RESULTS: The 2 assembled genomes have N50 values >5.5 and 8.5 Mb, respectively, and both contain ∼96% of BUSCO genes. Thus, they are highly contiguous and complete. The genomes are supported by an integrative taxonomy approach including placement in a genome-based phylogeny of Collembola and designation of a neotype for 1 of the species. Higher heterozygosity values are recorded in the more mobile species. Both species are devoid of the biosynthetic pathway for ß-lactam antibiotics known in several Collembola, confirming the tight correlation of antibiotic synthesis with the species way of life. CONCLUSIONS: It is now possible to generate high-quality genomes from single specimens of minute, field-preserved metazoans, exceeding the minimum contig N50 (1 Mb) required by the Earth BioGenome Project.

An application of dynamic homology to morphological characters: direct optimization of setae sequences and phylogeny of the family Odontellidae (Poduromorpha, Collembola).

The concept of character and the definition of the attribute are two major theoretical issues of phylogenetics. Lately, great progress has been made in the conceptual development of attributes as historical individuals undergoing series of transformations. While operational application of this ideographic concept of character has been possible since the publication of the direct optimization algorithm and POY software, it has been restricted to molecular characters only. The present paper proposes the first application of direct optimization to morphological characters, in the case study of the phylogeny of Odontellidae. This new homology regime is compared to the traditional homology scheme. The theoretical and operational limitations of the application of direct optimization to morphological characters are discussed. Some thoughts on the basics of its generalization to all morphological characters analyzed in a dynamic homology phylogenetic framework are given. © The Willi Hennig Society 2009;.

Breakdown of coevolution between symbiotic bacteria Wolbachia and their filarial hosts.

Wolbachia is an alpha-proteobacterial symbiont widely distributed in arthropods. Since the identification of Wolbachia in certain animal-parasitic nematodes (the Onchocercidae or filariae), the relationship between arthropod and nematode Wolbachia has attracted great interest. The obligate symbiosis in filariae, which renders infected species susceptible to antibiotic chemotherapy, was held to be distinct from the Wolbachia-arthropod relationship, typified by reproductive parasitism. While co-evolutionary signatures in Wolbachia-arthropod symbioses are generally weak, reflecting horizontal transmission events, strict co-evolution between filariae and Wolbachia has been reported previously. However, the absence of close outgroups for phylogenetic studies prevented the determination of which host group originally acquired Wolbachia. Here, we present the largest co-phylogenetic analysis of Wolbachia in filariae performed to date including: (i) a screening and an updated phylogeny of Wolbachia; (ii) a co-phylogenetic analysis; and (iii) a hypothesis on the acquisition of Wolbachia infection. First, our results show a general overestimation of Wolbachia occurrence and support the hypothesis of an ancestral absence of infection in the nematode phylum. The accuracy of supergroup J is also underlined. Second, although a global pattern of coevolution remains, the signal is derived predominantly from filarial clades associated with Wolbachia in supergroups C and J. In other filarial clades, harbouring Wolbachia supergroups D and F, horizontal acquisitions and secondary losses are common. Finally, our results suggest that supergroup C is the basal Wolbachia clade within the Ecdysozoa. This hypothesis on the origin of Wolbachia would change drastically our understanding of Wolbachia evolution.

Evolution on a shaky piece of Gondwana: is local endemism recent in New Caledonia?

New Caledonia is well known as a hot spot of biodiversity whose origin as a land mass can be traced back to the Gondwanan supercontinent. The local flora and fauna, in addition to being remarkably rich and endemic, comprise many supposedly relictual groups. Does the New Caledonian biota date back to Gondwanan times, building up its richness and endemism over 100 Myr or does it result from recent diversifications after Tertiary geological catastrophic events? Here we use a molecular phylogenetic approach to answer this question with the study of the Neocaledonian cockroach genus Angustonicus belonging to the subfamily Tryonicinae from Australia and New Caledonia. Both geological and molecular dating show that the diversification of this group is less than two million years old, whatever the date of its origin itself. This dating is not consistent with hypotheses of Gondwanan richness and endemism in New Caledonian biota. In other terms, local richness and endemism at the specific level are not necessarily related to an old Gondwanan origin of the Neocaledonian groups.

Were the first springtails semi-aquatic? A phylogenetic approach by means of 28S rDNA and optimization alignment.

Emergence from an aquatic environment to the land is one of the major evolutionary transitions within the arthropods. It is often considered that the first hexapods, and in particular the first springtails, were semi-aquatic and this assumption drives evolutionary models towards particular conclusions. To address the question of the ecological origin of the springtails, phylogenetic analyses by optimization alignment were performed on D1 and D2 regions of the 28S rDNA for 55 collembolan exemplars and eight outgroups. Relationships among the orders Symphypleona, Entomobryomorpha and Poduromorpha are inferred. More specifically, a robust hypothesis is provided for the subfamilial relationships within the order Poduromorpha. Contrary to previous statements, the semi-aquatic species Podura aquatica is not basal or 'primitive', but well nested in the Poduromorpha. The analyses performed for the 24 different weighting schemes yielded the same conclusion: semi-aquatic ecology is not ancestral for the springtails. It is a derived condition that evolved independently several times. The adaptation for semi-aquatic life is better interpreted as a step towards independence from land, rather than indication of an aquatic origin.

Is Psammophily an Evolutionary Dead End? A Phylogenetic Test in the Genus Willemia (Collembola: Hypogastruridae).

The law of the unspecialized states that specialized taxa have evolved from more generalized ancestors. Moreover, it is usually assumed that ecological specialization is irreversible and hence leads to extinction. This study aims to test these assumptions using a phylogenetic framework in a case study within the springtail genus Willemia and its diverse life habits. This genus is represented mostly by loam-dwelling species (generalized condition), but some species are psammophilous, living in sandy habitats (specialized condition). Fifty-two morphological characters were examined in 34 of the 36 species of the genus and in three outgroups. The cladistic analysis yielded two most parsimonious trees (tree length 124 steps; consistency index 0.56; retention index 0.86). The evolution of psammophily versus loam-confined life is compared to the cladogram: unexpectedly, psammophily is not an evolutionary innovation that occurred once in a monophyletic group; the evolutionary scenario that parsimoniously fits the phylogeny suggests that psammophily is ancestral to the genus Willemia and reversed twice to loam-confined life. These results demonstrate that habitat generalists can evolve from habitat specialists and therefore that habitat specializations are not necessarily an evolutionary dead end. Many other seemingly specialized characters may be shown to be equally malleable.

The geometric mean length, a new statistic to describe the distribution of character steps on a tree.

The geometric mean length (GML) is proposed as a new statistic aimed at describing the evenness of character changes on a tree for a given set of character optimizations. It is the geometric mean of the number of steps on each branch of the tree, varying between a maximum value when all branch lengths are equal, and a minimum value when all branches but one have only one character step. It can be scaled according to its theoretical maximum value, thus indicating a relative GML that allows a comparison of the evenness of character steps between different tree topologies.

Mapping characters on a tree with or without the outgroups.

A character of special interest in evolutionary studies is usually optimized on a phylogenetic tree, with or without the outgroups employed in that analysis. Both practices are never justified and look like arbitrary choices. Focusing on one example, we draw the conclusion that authors retain or remove outgroups depending on the way these outgroups sample the diversity of states of the character(s) of special interest. The topology without outgroups is often used by authors when different outgroup taxa non-exhaustively sample the different states of the character of interest outside of the ingroup. This can make the analysis incoherent, because its different steps are not based on the same data matrix (outgroups are removed in the last step). It can provide several incoherent and possibly different patterns for a same character of interest, one issuing from the first step of phylogeny construction and the other resulting from the a posteriori optimization on the truncated topology. Phylogenetic analyses should be designed to minimize this problem, selecting outgroup and ingroup taxa whose diversity of character states is needed for reconstructing the evolutionary history of the character of interest.

Mitochondrial genome data alone are not enough to unambiguously resolve the relationships of Entognatha, Insecta and Crustacea sensu lato (Arthropoda).

An analysis of the relationships of the major arthropod groups was undertaken using mitochondrial genome data to examine the hypotheses that Hexapoda is polyphyletic and that Collembola is more closely related to branchiopod crustaceans than insects. We sought to examine the sensitivity of this relationship to outgroup choice, data treatment, gene choice and optimality criteria used in the phylogenetic analysis of mitochondrial genome data. Additionally we sequenced the mitochondrial genome of an archaeognathan, Nesomachilis australica, to improve taxon selection in the apterygote insects, a group poorly represented in previous mitochondrial phylogenies. The sister group of the Collembola was rarely resolved in our analyses with a significant level of support. The use of different outgroups (myriapods, nematodes, or annelids + mollusks) resulted in many different placements of Collembola. The way in which the dataset was coded for analysis (DNA, DNA with the exclusion of third codon position and as amino acids) also had marked affects on tree topology. We found that nodal support was spread evenly throughout the 13 mitochondrial genes and the exclusion of genes resulted in significantly less resolution in the inferred trees. Optimality criteria had a much lesser effect on topology than the preceding factors; parsimony and Bayesian trees for a given data set and treatment were quite similar. We therefore conclude that the relationships of the extant arthropod groups as inferred by mitochondrial genomes are highly vulnerable to outgroup choice, data treatment and gene choice, and no consistent alternative hypothesis of Collembola's relationships is supported. Pending the resolution of these identified problems with the application of mitogenomic data to basal arthropod relationships, it is difficult to justify the rejection of hexapod monophyly, which is well supported on morphological grounds.

A new species and first record of the genus Triacanthella Schäffer, 1897 (Collembola, Poduromorpha, Hypogastruridae) for Africa.

The first species of the genus Triacanthella to be recorded from Africa is described. Triacanthella madibasp. n. belongs to the Southern Hemisphere group of the genus. It is morphologically closely related to Triacanthella vogeli Weiner & Najt, 1997 from Chile, and appears to be a gondwanian relict. The new species is also the first Triacanthella recorded from a guano habitat.

The evolutionary transition from subsocial to eusocial behaviour in Dictyoptera: phylogenetic evidence for modification of the "shift-in-dependent-care" hypothesis with a new subsocial cockroach.

Cockroaches have always been used to understand the first steps of social evolution in termites because they are close relatives with less complex and integrated social behaviour. Termites are all eusocial and ingroup comparative analysis would be useless to infer the origin of their social behaviour. The cockroach genus Cryptocercus was used as a so-called "prototermite" model because it shows key-attributes similar to the termites (except Termitidae): wood-feeding, intestinal flagellates and subsocial behaviour. In spite of these comparisons between this subsocial cockroach and eusocial termites, the early and remote origin of eusocial behaviour in termites is not well understood yet and the study of other relevant "prototermite" models is however needed. A molecular phylogenetic analysis was carried out to validate a new "prototermite" model, Parasphaeria boleiriana which shows a peculiar combination of these key-attributes. It shows that these attributes of Parasphaeria boleiriana have an independent origin from those of other wood-eating cockroaches and termites. The case of P. boleiriana suggests that a short brood care was selected for with life on an ephemeral wood resource, even with the need for transmission of flagellates. These new phylogenetic insights modify evolutionary hypotheses, contradicting the assumption made with Cryptocercus model that a long brood care is necessary for cooperation between broods in the "shift-in-dependent-care" hypothesis. An ephemeral wood resource is suggested to prompt generation overlap and the evolution of cooperation, even if brood care is shortened.

[Hexapoda phylogeny: implications for an aquatic origin hypothesis]. / Phylogénie des hexapodes et implications pour l'hypothèse de leur origine aquatique.

Emergence from an aquatic environment to the land is one of the major evolutionary transitions within the arthropods. It is often considered that the first hexapods, and especially the first Collembola, went from the sea through intermediate freshwater environments to colonize fully terrestrial ecosystems. To understand the ancestral ecology of hexapods, a phylogenetic framework is used. By mapping ecological attributes onto the phylogeny, it is shown that hexapods colonized terrestrial environments directly from marine environment without a transition through freshwater. An edaphic life-style is the basal state for Collembola and more generally for hexapods as a whole. Aquatic ecology is inferred to be a secondary change that occurred several times independently, particularly in some group of Collembola and Pterygota. The answer is ambiguous for Pterygota, whether the first Pterygota had aquatic larvae and reversed toward fully terrestrial in Neoptera, or aquatic larvae appeared independently in Odonata and Ephemeroptera. Subsequently, aquatic larvae were secondarily acquired in various groups independently (e.g. Plecoptera, Trichoptera, Coleoptera).