Social biology of the wood-feeding cockroach genus <Emphasis Type="Italic">Salganea</Emphasis> (Dictyoptera,Blaberidae, Panesthiinae): did ovoviviparity prevent the evolution of eusociality in the lineage?

Recent phylogenetic studies indicating that termites are eusocial cockroaches closely related to the genus Cryptocercus have generated fresh interest in wood-feeding Blattaria. Here we summarize the social biology of the wood-feeding genus Salganea (Blaberidae: Panesthiinae). As in Cryptocercus, Salganea exhibits long term, biparental care that includes the defense and feeding of young nymphs. Unlike Cryptocercus, however, Salganea is iteroparous: most studied species reproduce periodically over their lifetime. These divergent reproductive strategies are likely related to parental costs associated with their differing reproductive modes: Cryptocercus is oviparous, while Salganea is ovoviviparous. The pattern of parental investment associated with ovoviviparous reproduction may be one reason why Salganea and other ovoviviparous wood-feeding cockroach lineages did not evolve eusociality. Received 21 August 2007; revised 25 January 2008; accepted 22 Feburary 2008.     

Uplift-driven diversification revealed by the historical biogeography of the cockroach Cryptocercus Scudder (Blattodea: Cryptocercidae) in eastern Asia

Cryptocercus Scudder is a genus of wingless cockroaches, which spend their lives feeding within rotting wood in old-growth montane forests. Their dispersal capability is likely to be limited because they depend on the succession of temperate forests, but their distribution exhibits intercontinental disjunctions. Although the natural history and conservation biology of the North American species of the genus have received much attention, the evolution of the eastern Asian lineages remains enigmatic. To resolve the geographic patterns and evolutionary history of Cryptocercus in eastern Asia, we analysed genetic data of species from China (27 species), Korea (one species) and the Russian Far East (one species). We performed phylogenetic analyses of seven genes to infer the evolutionary relationships among species of Asian Cryptocercus. We then used Bayesian molecular dating to estimate the evolutionary timescale of the genus. Ancestral geographic distributions were reconstructed in rasp using statistical dispersal-vicariance analysis and statistical dispersal-extinction-cladogenesis. Our maximum-likelihood and Bayesian phylogenetic trees supported four major lineages of Cryptocercus, revealing a clear geographical pattern. The divergence of American and Asian lineages was inferred to have occurred 74.8 Ma (95% credibility interval: 51.1–103.8 Ma), with the diversification of Asian taxa beginning at 30.7 Ma (95% credibility interval: 22.9–40.3 Ma). The most recent common ancestor of Asian Cryptocercus taxa was inferred to have had a broad distribution in Asia. The uplift of the Qinghai-Tibet Plateau in the Palaeogene and Neogene, along with climatic oscillations in the Quaternary, probably had substantial effects on the formation of the disjunction pattern in the Cryptocercus lineages found in the Hengduan Mountains and Qin-Daba Mountains of China. We propose that the distribution of Cryptocercus has been strongly influenced by habitat fragmentation and subsequent allopatric speciation.     

Morphology,Phylogeny, and Diversity of Trichonympha (Parabasalia: Hypermastigida) of the Wood‐Feeding Cockroach Cryptocercus punctulatus

ABSTRACT. Trichonympha is one of the most complex and visually striking of the hypermastigote parabasalids—a group of anaerobic flagellates found exclusively in hindguts of lower termites and the wood‐feeding cockroach Cryptocercus—but it is one of only two genera common to both groups of insects. We investigated Trichonympha of Cryptocercus using light and electron microscopy (scanning and transmission), as well as molecular phylogeny, to gain a better understanding of its morphology, diversity, and evolution. Microscopy reveals numerous new features, such as previously undetected bacterial surface symbionts, adhesion of post‐rostral flagella, and a distinctive frilled operculum. We also sequenced small subunit rRNA gene from manually isolated species, and carried out an environmental polymerase chain reaction (PCR) survey of Trichonympha diversity, all of which strongly supports monophyly of Trichonympha from Cryptocercus to the exclusion of those sampled from termites. Bayesian and distance methods support a relationship between Trichonympha species from termites and Cryptocercus, although likelihood analysis allies the latter with Eucomonymphidae. A monophyletic Trichonympha is of great interest because recent evidence supports a sister relationship between Cryptocercus and termites, suggesting Trichonympha predates the Cryptocercus‐termite divergence. The monophyly of symbiotic bacteria of Trichonympha raises the intriguing possibility of three‐way co‐speciation among bacteria, Trichonympha, and insect hosts.     

Interspecific morphological variation in the wood-feeding cockroach, Cryptocercus (Dictyoptera: Cryptocercidae)

Appalachian species of Cryptocercus (Dictyoptera: Cryptocercidae) display considerable genetic variation, but little morphological variation has been reported. We employed light and scanning electron microscopy to investigate variation in male and female reproductive structures among four species of Cryptocercus. Our results indicated consistent, species-specific differences exist in the genitalia of the four species. Males exhibit moderate interspecific differences in the shape of the subgenital plate and third left phallomere hook. Females display consistent interspecific differences in the size of setae on the basivalvula and great differences in size, number, and pattern of setae on the base of the second valves. Together, the interspecific variation in female reproductive structures can be used to identify each of the four Cryptocercus species that occur in the Appalachian Mountains.     

Analysis of Extensive [FeFe] Hydrogenase Gene Diversity Within the Gut Microbiota of Insects Representing Five Families of Dictyoptera

We have designed and utilized degenerate primers in the phylogenetic analysis of [FeFe] hydrogenase gene diversity in the gut ecosystems of roaches and lower termites. H₂ is an important free intermediate in the breakdown of wood by termite gut microbial communities, reaching concentrations in some species exceeding those measured for any other biological system. The primers designed target with specificity the largest group of enzymatic H domain proteins previously identified in a termite gut metagenome. “Family 3” hydrogenase sequences were amplified from the guts of lower termites, Incisitermes minor, Zootermopsis nevadensis, and Reticulitermes hesperus, and two roaches, Cryptocercus punctulatus and Periplaneta americana. Subsequent analyses revealed that all termite and Cryptocercus sequences were phylogenetically distinct from non-termite-associated hydrogenases available from public databases. The abundance of unique sequence operational taxonomic units (as many as 21 from each species) underscores the previously demonstrated physiological importance of H₂ to the gut ecosystems of these wood-feeding insects. The diversity of sequences observed might be reflective of multiple niches that the enzymes have been evolved to accommodate. Sequences cloned from Cryptocercus and the lower termite samples, all of which are wood feeding insects, clustered closely with one another in phylogenetic analyses to the exclusion of alleles from P. americana, an omnivorous cockroach, also cloned during this study. We present primers targeting a family of termite gut [FeFe] hydrogenases and provide results that are consistent with a pivotal role for hydrogen in the termite gut ecosystem and point toward unique evolutionary adaptations to the gut ecosystem.     

Molecular phylogeny of cockroaches (Blattaria) based on mitochondrial COII gene sequences

Phylogenetic relationships among five cockroach families (Cryptocercidae, Polyphagidae, Blattidae, Blattellidae and Blaberidae) using seventeen species, were estimated based on the DNA sequences of the mitochondrial cytochrome oxidase subunit II (COII) gene. A cladogram inferred using the neighbour‐joining method indicated that Polyphagidae and Cryptocercidae are closely related to each other, and that these two groups are a sister group to the remaining cockroach families. The monophyly of this clade, however, was not strongly supported in terms of bootstrap percentages. Blaberidae and Blattellidae were shown to be sister groups as previously proposed, with Blattidae as a sister group to that clade. Non‐weighted and weighted parsimony analyses were also performed following analyses of nucleotide substitution patterns that indicated saturation of the COII gene among these taxa had occurred. These parsimonious cladograms suggested that Polyphagidae was the basal family, and Polyphaginae, including Cryptocercus as proposed by Grandcolas 1994a ), was not monophyletic. The inferred relationships among cockroach families (Polyphagidae, Cryptocercidae + (Blattidae + (Blattellidae + Blaberidae))) is partly in agreement with some previously published analyses. Additionally, based on molecular data, Asian and American Cryptocercus are suggested to have diverged from one another before the Oligocene (～20 mya).     

Origin of termite eusociality: trophallaxis integrates the social,nutritional, and microbial environments

1. Numerous cladistic analyses have converged: termites are a monophyletic clade embedded within the paraphyletic cockroaches, and sister group to the biparental, wood‐feeding cockroach Cryptocercus. The latter is, therefore, an appropriate model for testing assumptions regarding early termite evolution. 2. The ground plan of the termite ancestor is reviewed based on shared characters of ecology, life history, and behaviour in Cryptocercus and incipient termite colonies, and includes two levels of dependence: a reliance of all individuals on gut microbiota, and dependence of early instars on parental care. Both these conditions co‐evolved with parent‐to‐offspring proctodeal trophallaxis. 3. The termite ancestor lived in a single log serving as food and nest. This ‘one‐piece’ nesting ecology prioritises nitrogen conservation and strongly influences interacting social, nutritional, and microbial environments. Each of these environments individually and in combination profoundly affect cockroach development. 4. Proctodeal trophallaxis integrates the social, nutritional, and microbial environments. A change in trophallactic behaviour, from parental to alloparental, can, therefore, shift developmental trajectories, ultimately adding a third level of dependence. The death of gut protists during the host molting period and consequent interdependence of family members shifted the hierarchical level at which selection acted; fixation of eusociality quickly followed. 5. The basic nesting ecology did not change when termites evolved eusociality, the change occurred in the allocation and use of existing resources within the social group, driven by nitrogen scarcity, mediated by trophallaxis, and made possible by a strongly lineage‐specific set of life history characteristics.     

Ecological niche conservation and differentiation in the wood-feeding cockroaches, Cryptocercus, in the United States

The distribution of a species is determined by a set of ecological correlates (biotic and abiotic factors) and historical phenomena that define and constrain its ecological niche. By examining the geographical projection of the ecological niche, it is possible to identify areas that are suitable for the species ecologically but that are not actually inhabited. Previous studies have used such discords to anticipate the existence of undescribed species; the absence of species may also result from historical barriers that have prevented colonization of the area. Thus, discords between potential and realized niches of a species may result from aspects of the species’s biology (e.g. lack of dispersal ability, specific habitat requirements) or from barriers to dispersal. In this study, we developed ecological niche models of the five Nearctic species of wood‐feeding cockroaches in the genus Cryptocercus. One species, C. clevelandi, occurs in the western USA and four (C. darwini, C. garciai, C. punctulatus, C. wrighti) are distributed in the Appalachian Mountains in the eastern USA. In general, modelled niches for all species showed ecological restriction relative to the total range of available conditions. Niche models for the eastern USA species predicted the geographical distributions of the other eastern USA species, with the exception of C. garciai, suggesting general overall conservatism in ecological characteristics. Some interspecific differences in modelled niches were also apparent. In general, C. clevelandi was predicted to occupy cooler and drier areas relative to the eastern USA species; among the eastern USA species, C. darwini and C. garciai were predicted to inhabit warmer areas relative to C. punctulatus and C. wrighti. Interspecific differences and similarities were consistent with the phylogenetic relationships among Cryptocercus species previously reported. © 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 90 , 457–466.     

Relationships among the major lineages of Dictyoptera: the effect of outgroup selection on dictyopteran tree topology

Abstract Dictyoptera, comprising Blattaria, Isoptera, and Mantodea, are diverse in appearance and life history, and are strongly supported as monophyletic. We downloaded COII, 16S, 18S, and 28S sequences of 39 dictyopteran species from GenBank. Ribosomal RNA sequences were aligned manually with reference to secondary structure. We included morphological data (maximum of 175 characters) for 12 of these taxa and for an additional 15 dictyopteran taxa (for which we had only morphological data). We had two datasets, a 59‐taxon dataset with five outgroup taxa, from Phasmatodea (2 taxa), Mantophasmatodea (1 taxon), Embioptera (1 taxon), and Grylloblattodea (1 taxon), and a 62‐taxon dataset with three additional outgroup taxa from Plecoptera (1 taxon), Dermaptera (1 taxon) and Orthoptera (1 taxon). We analysed the combined molecular?morphological dataset using the doublet and MK models in Mr Bayes , and using a parsimony heuristic search in paup . Within the monophyletic Mantodea, Mantoida is recovered as sister to the rest of Mantodea, followed by Chaeteessa; the monophyly of most of the more derived families as defined currently is not supported. We recovered novel phylogenetic hypotheses about the taxa within Blattodea (following Hennig, containing Isoptera). Unique to our study, one Bayesian analysis places Polyphagoidea as sister to all other Dictyoptera; other analyses and/or the addition of certain orthopteran sequences, however, place Polyphagoidea more deeply within Dictyoptera. Isoptera falls within the cockroaches, sister to the genus Cryptocercus. Separate parsimony analyses of independent gene fragments suggest that gene selection is an important factor in tree reconstruction. When we varied the ingroup taxa and/or outgroup taxa, the internal dictyopteran relationships differed in the position of several taxa of interest, including Cryptocercus, Polyphaga, Periplaneta and Supella. This provides further evidence that the choice of both outgroup and ingroup taxa greatly affects tree topology.     

Effects of parental care on offspring growth in the Korean wood-feeding cockroach, <Emphasis Type="Italic">Cryptocercus kyebangensis</Emphasis>

The objective of this study was to measure the possible effects of prolonged parental care on offspring growth in Korean wood-feeding cockroaches, Cryptocercus kyebangensis. In the field-caught subsocial woodroaches of C. kyebangensis, offspring with both parents were greater in both head width and body weight than those with single parents. Manipulation experiments showed that offspring separated from their parents could survive independently without parents, but they grew more rapidly when they remained with their parents. In particular, the effects of parental care on offspring growth were found to be stronger in groups with both parents than those with single parents. These results suggest that the prolonged parental care evolved in Cryptocercus has a significant impact on offspring growth. Electronic Publication     

Involvement of the hyperglycemic neurohormone family in the control of reproduction in decapod crustaceans

Summary

In the last few years, (bio)chemical and molecular biological studies have shown that several members of the hyperglycemic hormone family are present in different molecular forms. In vivo and in vitro bioassays revealed that some of these isoforms also play a role in the control of reproduction in decapod crustaceans. This communication gives a review of the cytological aspects of the eyestalk X-organ sinus gland complex, responsible for the synthesis, storage and release of these neuropeptides, and the molecular and functional aspects of those members involved in the control of reproduction. Finally, the role of the hyperglycemic hormone family in the regulation of reproduction in the female lobster is described as an example of the (possible) interactions of the members of the hyperglycemic hormone family with other (neuro)endocrine factors in the reproductive process of crustaceans.     

The extent and costs of reproductive interference among four species of true bug

Reproductive interference arises when individuals of one species engage in reproductive activities with individuals of another, leading to fitness costs in one or both species. Reproductive interference (RI) therefore has two components. First, there must be mis-directed mating interactions. Second, there must be costs associated with these mis-directed interactions. Here we consider RI between four species of true bug in the family Lygaeidae, focusing in particular on the fitness consequences to Lygaeus equestris. The species we consider vary in their relationships with each other, including species in the same or different genus, and with or without natural overlap in their geographic ranges. First we show that inter-specific mating interactions, although not a certain outcome, are common enough to perhaps influence mating behaviour in these species (arising in up to 10 % of inter-specific pairings). Second, we show that reproductive interference can seriously reduce female fitness in L. equestris. Importantly, different species impose different costs of RI on L. equestris, with interactions with male Spilostethus pandurus inflicting fitness costs of similar magnitude to the costs of mating with con-specifics. On the other hand, mating interactions with male Oncopeltus fasciatus appear to have no effect on female fitness. In a follow-up experiment, when we allowed competition amongst just females of S. pandurus and L. equestris, the fitness of the latter was not reduced, arguing more strongly for the role of reproductive interference. However, in our final experiments under mass mating conditions with extended ecological interactions (including scope for competition for resources and cannibalism), the costs of RI were less apparent. Our data therefore suggest that the costs of RI will be context-specific and may act in concert with, or be swamped by, other ecological effects. We suggest that comparative studies of this sort that both mimic naturally occurring reproductive interference events, and also artificially generate new ones, will be necessary if we are to better understand the ecological and evolutionary significance of reproductive interference.     

Enhanced Mutation Rate,Relaxed Selection,and the “Domino Effect” are associated with Gene Loss in Blattabacterium,A Cockroach Endosymbiont

Intracellular endosymbionts have reduced genomes that progressively lose genes at a timescale of tens of million years. We previously reported that gene loss rate is linked to mutation rate in Blattabacterium, however, the mechanisms causing gene loss are not yet fully understood. Here, we carried out comparative genomic analyses on the complete genome sequences of a representative set of 67 Blattabacterium strains, with sizes ranging between 511 and 645 kb. We found that 200 of the 566 analyzed protein-coding genes were lost in at least one lineage of Blattabacterium, with the most extreme case being one gene that was lost independently in 24 lineages. We found evidence for three mechanisms influencing gene loss in Blattabacterium. First, gene loss rates were found to increase exponentially with the accumulation of substitutions. Second, genes involved in vitamin and amino acid metabolism experienced relaxed selection in Cryptocercus and Mastotermes, possibly triggered by their vertically inherited gut symbionts. Third, we found evidence of epistatic interactions among genes leading to a “domino effect” of gene loss within pathways. Our results highlight the complexity of the process of genome erosion in an endosymbiont.     

Competitive strategies between Anastrepha fraterculus and Anastrepha obliqua (Diptera: Tephritidae) regulating the use of host fruits

Interspecific competition between individuals of different species can result in reductions in their fecundity, growth or survival, reflecting differential exploitation of resources that become intensified due to spatial co-occurrence, ecological similarity and increased population densities. As two species cannot occupy the same niche, coexistence is only possible if the available resources are used in non-overlapping manners such as niche partitioning or the use of refuges. Among agricultural insect pests, such as fruit flies of the family Tephritidae, competitive interactions can result in competitive displacement, host changes, or the expansion or restriction of the numbers of hosts utilized that can have negative consequences for human agricultural activities. We evaluated the competitive interactions between two fruit fly species of the genus Anastrepha, Anastrepha obliqua (Macquart, 1835) and Anastrepha fraterculus (Wiedmann, 1830), on their respective preferred hosts (mangoes and guava). Experiments of larval competition and competition for ovipositioning sites by adult females were performed to compare the parameters of larval development time, numbers of pupae and emerged adults and numbers of ovipositions in the presence or absence of interspecific competition. We observed that the interactions between those species were asymmetrical and hierarchical, and our results suggest a competitive displacement of A. fraterculus by A. obliqua when those two species are present on the same fruit, whether mangoes or guavas.     

Functional Roles of Centridini Oil Bees and Malpighiaceae Oil Flowers in Biome‐wide Pollination Networks

Interactions between oil‐collecting bees and oil‐producing flowers are a very specialized mutualism, whose natural history is well known at the organism and population levels. In this study, we assessed these interactions at the biome level with a network approach, and hypothesized that widespread bee and plant species would occupy different ecological functional roles (Eltonian niches) in different biomes. Furthermore, we expected the most important functional roles in each network to be occupied more frequently by Byrsonima oil flowers and Centris oil bees, which share the longest coevolutionary history in the Neotropics. By compiling data from 40 articles on oil flower interactions within the Malpighiaceae family, we built six networks for different Brazilian biomes. We assessed the ecological functional role of each species in pollination networks of oil flowers through the metric known as ‘network functional role’. Although 90 percent of the species occupied peripheral roles in each network, some were found to occupy highly central roles. Oil flowers of the genera Byrsonima and Banisteriopsis and oil bees of the genera Centris and Epicharis were the most important species in all networks, as they made a disproportionally high number of interactions (hubs), or helped bind together different modules (connectors). Our findings suggest that functional roles vary geographically and seem to be affected by local conditions in different biomes. Furthermore, coevolutionary history seems to play an important role in determining functional roles in oil flower networks, although other factors are probably also important, especially the degree of specialization in this kind of interaction.     

Dynamic expression of the LAP family of genes during early development of <Emphasis Type="Italic">Xenopus tropicalis</Emphasis>

The leucine-rich repeats and PDZ (LAP) family of genes are crucial for the maintenance of cell polarity as well as for epithelial homeostasis and tumor suppression in both vertebrates and invertebrates. Four members of this gene family are known: densin, erbin, scribble and lano. Here, we identified the four members of the LAP gene family in Xenopus tropicalis and studied their expression patterns during embryonic development. The Xenopus LAP proteins show a conserved domain structure that is similar to their homologs in other vertebrates. In Xenopus embryos, these genes were detected in animal cap cells at the early gastrula stage. At later stages of development, they were widely expressed in epithelial tissues that are highly polar in nature, including the neural epithelia, optic and otic vesicles, and in the pronephros. These data suggest that the roles of the Xenopus LAP genes in the control of cell polarity and morphogenesis are conserved during early development. Erbin and lano show similar expression patterns in the developing head, suggesting potential functional interactions between the two molecules in vivo.     

Exchangeability of the flagellin (FliC) and the cap protein (FliD) among different species in flagellar assembly

Flagellar filament self‐assembles from the component protein, flagellin or FliC, with the aid of the capping protein, HAP2 or FliD. Depending on the helical parameters of filaments, flagella from various species are divided into three groups, family I, II, and III. Each family coincides with the traditional classification of flagella, peritrichous flagella, polar flagella, and lateral flagella, respectively. To elucidate the physico‐chemical properties of flagellin to separate families, we chose family I flagella and family II flagella and examined how well the exchangeability of a combination of FliC and/or FliD from different families is kept in filament formation. FliC or FliD of Salmonella enterica serovar Typhimurium (Salty; family I) were exchanged with those of Escherichia coli (Escco; family I) or Pseudomonas aeruginosa (Pseae; family II). In a Salty fliC deletion mutant, Escco FliC formed short filaments, but Pseae FliC did not form filaments. In a Salty fliD deletion mutant, both Escco FliD and Pseae FliD allowed Salty FliC to polymerize into short filaments. In conclusion, FliC can be exchanged among the same family but not between different families, while FliD serves as the cap protein even in different families, confirming that FliC is essential for determining families, but FliD plays a subsidiary role in filament formation. © 2012 Wiley Periodicals, Inc.     

Characterization of Argonaute family members in the silkworm,Bombyx mori

Abstract The Argonaute protein family is a highly conserved group of proteins, which have been implicated in RNA silencing in both plants and animals. Here, four members of the Argonaute family were systemically identified based on the genome sequence of Bombyx mori. Based on their sequence similarity, BmAgo1 and BmAgo2 belong to the Ago subfamily, while BmAgo3 and BmPiwi are in the Piwi subfamily. Phylogenetic analysis reveals that silkworm Argonaute family members are conserved in insects. Conserved amino acid residues involved in recognition of the 5′ end of the small RNA guide strand and of the conserved (aspartate, aspartate and histidine [DDH]) motif present in their PIWI domains suggest that these four Argonaute family members may have conserved slicer activities. The results of microarray expression analysis show that there is a low expression level for B. mori Argonaute family members in different tissues and different developmental stages, except for BmPiwi. All four B. mori Argonaute family members are upregulated upon infection with B. mori nucleopolyhedrovirus. The complete coding sequence of BmPiwi, the homolog of Drosophila piwi, was cloned and its expression occurred mainly in the area where spermatogonia and spermatocytes appear. Our results provide an overview of the B. mori Argonaute family members and suggest that they may have multiple roles. In addition, this is also the first report, to our knowledge, of the response of RNA silencing machinery to DNA virus infection in insects.