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Solving the 250-year-old mystery of the origin and global spread of the German cockroach, Blattella germanica.

The origin of the German cockroach, Blattella germanica, is enigmatic, in part because it is ubiquitous worldwide in human-built structures but absent from any natural habitats. The first historical records of this species are from ca. 250 years ago (ya) from central Europe (hence its name). However, recent research suggests that the center of diversity of the genus is Asian, where its closest relatives are found. To solve this paradox, we sampled genome-wide markers of 281 cockroaches from 17 countries across six continents. We confirm that B. germanica evolved from the Asian cockroach Blattella asahinai approximately 2,100 ya, probably by adapting to human settlements in India or Myanmar. Our genomic analyses reconstructed two primary global spread routes, one older, westward route to the Middle East coinciding with various Islamic dynasties (~1,200 ya), and another younger eastward route coinciding with the European colonial period (~390 ya). While Europe was not central to the early domestication and spread of the German cockroach, European advances in long-distance transportation and temperature-controlled housing were likely important for the more recent global spread, increasing chances of successful dispersal to and establishment in new regions. The global genetic structure of German cockroaches further supports our model, as it generally aligns with geopolitical boundaries, suggesting regional bridgehead populations established following the advent of international commerce.

Animals

Sex pheromone communication and its regulation by the sex determination pathway in cockroaches.

Sexual communication in animals orchestrates a series of interactive behaviors from locating and recognizing potential partners to courtship and final mating decisions and is thus critical for sexual reproduction and population fitness. Highly efficient communication between the sexes requires not only the production and emission of species-specific signals but also their precise detection and interpretation by the receiving individuals. Cockroaches, as one of the most evolutionarily ancient and successful group of insects, are quintessential chemical communicators that rely heavily on sex pheromones for sexual communication. They have long served as excellent model organisms in studies of chemical ecology. Although the biochemical characterization of sex pheromones in several species was largely accomplished during the last century, the past two decades have witnessed remarkable progress in understanding the molecular genetics of sex pheromone communication and its regulation, particularly driven by functional genomics. This review first provides an updated comparative survey of the pheromone components identified across distinct taxa. We then synthesize, but not limited to, recent advances in identification of key molecules controlling sex pheromone production, characterization of candidate chemosensory receptors and their neural processing pathways, and the regulatory roles of the sex determination cascade in shaping sexually dimorphic traits in both pheromone production and perception. Finally, we highlight key scientific questions that remain unsolved and propose future directions aimed at extending our mechanistic understanding of cockroach pheromone communication, as well as at developing behavior-based pest management strategies.

biosynthetic pathway

One-time duplication and ongoing loss of mitochondrial tRNA genes in Cryptocercus cockroaches.

Mitochondrial genome is a popular marker in phylogenetics and species diversity estimations. Mitogenome is relatively compact and conserved, while gene rearrangements were found in some species across various organisms. Models to explain the origin and evolution of gene rearrangement have been proposed but seldom demonstrated; empirical evidence from closely related species is particularly scarce. Here, through an intensive case study of the cockroach genus Cryptocercus Scudder, 1862, we elucidate the evolution of mitochondrial gene order. This study utilized 51 new samples and re-assembled raw reads of 26 published samples. A diversity of rearrangement patterns is recovered, especially in the tRNA gene cluster between ND3 and ND5, which is effectively explained by the duplication - random loss model. Specifically, the entire tRNA gene cluster was duplicated; this duplication is potentially facilitated by chance binding between the 3' end of ND5 gene and the ND3-trnA region during DNA replication. Furthermore, we reveal that one of the gene copies degenerated stochastically across lineages, directly contributing to the observed diversity in gene arrangement. Gene rearrangement patterns are apomorphies for certain clades, providing additional evidence for the inferred phylogeny and serving as potential indicators of species. This study underscores the importance of intensive sampling and rigorous data curation for deciphering the evolutionary mechanisms.

Duplication–random loss model

Taxonomic revision of the genus Methanobrevibacter, description of Methanomonile shimae gen. nov. sp. nov., and proposal of Methanobrevibacteraceae fam. nov.

Recent phylogenomic analyses revealed that the genus Methanobrevibacter, which consists almost exclusively of representatives from the intestinal tract of animals, is severely underclassified. Based on the large relative evolutionary divergence between individual subclades, members of the genus Methanobrevibacter have been reclassified into eight novel genera as new combinations proposed under the rules of the Code of Nomenclature of Prokaryotes Described from Sequence Data. Here, we validly publish the new names for all taxa with type strains also under the rules of the International Code of Nomenclature of Prokaryotes. This includes members of the genera Methanacia, Methanobaculum, Methanobinarius, Methanocatella and Methanoflexus. Moreover, we propose to place Methanobrevibacter acididurans, whose genome was only recently sequenced, in the new genus Methanobotrus and describe a new isolate from the gut of a cockroach as Methanomonile shimae gen. nov. sp. nov. Based on the large evolutionary distance from the remaining members of Methanobacteriaceae, we propose to reclassify all genera within the radiation of Methanobrevibacter sensu lato into their own family, Methanobrevibacteraceae fam. nov. In addition, we reclassify Methanothermobacter tenebrarum as Methanothermobaculum tenebrarum gen. nov. comb. nov. into a new family, Methanothermobaculaceae (Methanobacteriales) and provide emended descriptions for the phylum Methanobacteriota and the classes Methanobacteria and Methanococci.

Phylogeny

Evolutionary conservation of heat shock proteins in Blattodea and their roles in wing morphogenesis and ovarian development of Blattella germanica.

Heat shock proteins (Hsps) are essential molecular chaperones for protein homeostasis and stress responses. However, the Hsp repertoires and functions in Blattodea remain underexplored. Our genome-scale survey of nine Blattodea species revealed 37-46 conserved Hsp90, Hsp70, and DNAJ (Hsp40) genes, with DNAJ the most abundant and Hsp90 the least. Phylogenetic analysis confirmed the evolutionary conservation of three Hsp90, seven Hsp70, and 29 DNAJ subclades in Blattodea. Selection pressure analysis revealed predominant purifying selection (dN/dS ≪ 1) across lineages, strongest in DNAJ and highest in Hsp90 conservation. In Blattella germanica, expression of six representative BgHsp genes progressively increased during development, peaking in fifth-instar nymphs. Tissue expression profiling revealed that BgHspA1-2/3/4 were predominantly expressed in legs, BgDNAJB5 and BgHsp90AB1-2 were enriched in the fat body, and BgHsp90AB1 was highly expressed in the head. dsRNA injection targeting conserved Hsp gene regions achieved 61.9-94.1% knockdown of all six target genes. RNAi knockdown of six BgHsp genes disrupted wing morphogenesis, causing distinct phenotypes: wing whitening (56.7%, dsBgHspA1-4), unequal length (66.7%, dsBgHspA1-3; 76.7%, dsBgDNAJB5), and wing wrinkling (70%, dsBgHspA1-2; 63.3%, dsBgHsp90AB1; 76.7%, dsBgHsp90AB1-2). During ovarian formation, the developmental delay was most severe in the dsBgHsp90AB1 group, moderate in the dsBgHsp90AB1-2 and dsBgHspA1-2/3/4 groups, and weakest in the dsBgDNAJB5 group. Besides, knockdown significantly downregulated key developmental genes (apterous-a, nubbin, scalloped, ultrabithorax, wingless, and vitellogenin). These findings provide a reference for understanding the evolutionary patterns of Hsps in Blattodea, and offer mechanistic insights into the developmental regulation mediated by Hsps in this important public-health pest.

Animals