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The success of neopteran insects, with 1 million species described, is associated with developmental innovations such as holometaboly and the evolution from short to long germband embryogenesis. To unveil the mechanisms underlining these innovations, we compared gene expression during the ontogeny of two extreme neopterans, the cockroach Blattella germanica (polyneopteran, hemimetabolan, and short germband species) and the fly Drosophila melanogaster (endopterygote, holometabolan, and long germband species). Results revealed that genes associated with metamorphosis are predominantly expressed in late nymphal stages in B. germanica and in the early-mid embryo in D. melanogaster. In B. germanica the maternal to zygotic transition (MZT) concentrates early in embryogenesis, when juvenile hormone factors are significantly expressed. In D. melanogaster, the MZT extends throughout embryogenesis, during which time juvenile hormone factors appear to be unimportant. These differences possibly reflect broad trends in the evolution of development within neopterans, related to the germband type and the metamorphosis mode. ; This work was supported by the Spanish Ministry of Economy and Competitiveness (grants CGL2012-36251 and CGL2015-64727-P to X.B., including FEDER funds), Spanish Ministry of Science and Innovation (grants BFU2011–22404 and CGL2016–76011-R to M.-D.P., including FEDER funds), and Catalan Government (grants 2014 SGR 619 and 2017 SGR 1030). ; Peer reviewed

[Background]: Do miRNAs contribute to specify the germ-band type and the body structure in the insect embryo? Our goal was to address that issue by studying the changes in miRNA expression along the ontogeny of the German cockroach Blattella germanica, which is a short germ-band and hemimetabolan species. [Results]: We sequenced small RNA libraries representing 11 developmental stages of B. germanica ontogeny (with especial emphasis on embryogenesis) and the changes in miRNA expression were examined. Data were compared with equivalent data for two long germ-band holometabolan species Drosophila melanogaster and Drosophila virilis, and the short germ-band holometabolan species Tribolium castaneum. The identification of B. germanica embryo small RNA sequences unveiled miRNAs not detected in previous studies, such as those of the MIR-309 family and 54 novel miRNAs. Four main waves of miRNA expression were recognized (with most miRNA changes occurring during the embryonic stages): the first from day 0 to day 1 of embryogenesis, the second during mid-embryogenesis (days 0-6), the third (with an acute expression peak) on day 2 of embryonic development, and the fourth during post-embryonic development. The second wave defined the boundaries of maternal-to-zygotic transition, with maternal mRNAs being cleared, presumably by Mir-309 and associated scavenger miRNAs. [Conclusion]: miRNAs follow well-defined patterns of expression over hemimetabolan ontogeny, patterns that are more diverse during embryonic development than during the nymphal stages. The results suggest that miRNAs play important roles in the developmental transitions between the embryonic stages of development (starting with maternal loading), during which they might influence the germ-band type and metamorphosis mode. ; This work was supported by the Spanish Ministry of Economy and Competitiveness (grants CGL2012–36251 and CGL2015–64727-P to X.B.), the Spanish Ministry of Science and Innovation (grants BFU2011–22404 and CGL2016–76011-R to M.D.P.) and the Catalan Government (2014 SGR 619). It also received financial assistance from the European Fund for Economic and Regional Development (FEDER funds to X.B. and M.D.P.). ; We acknowledge support of the publication fee by the CSIC Open Access Publication Support Initiative through its Unit of Information Resources for Research (URICI). ; Peer Reviewed

Is there a correlation between miRNA diversity and levels of organismic complexity? Exhibiting extraordinary levels of morphological and developmental complexity, insects are the most diverse animal class on earth. Their evolutionary success was in particular shaped by the innovation of holometabolan metamorphosis in endopterygotes. Previously, miRNA evolution had been linked to morphological complexity, but astonishing variation in the currently available miRNA complements of insects made this link unclear. To address this issue, we sequenced the miRNA complement of the hemimetabolan Blattella germanica and reannotated that of two other hemimetabolan species, Locusta migratoria and Acyrthosiphon pisum, and of four holometabolan species, Apis mellifera, Tribolium castaneum, Bombyx mori and Drosophila melanogaster. Our analyses show that the variation of insect miRNAs is an artefact mainly resulting from poor sampling and inaccurate miRNA annotation, and that insects share a conserved microRNA toolkit of 65 families exhibiting very low variation. For example, the evolutionary shift toward a complete metamorphosis was accompanied only by the acquisition of three and the loss of one miRNA families. ; This work was supported by the Spanish Ministry of Economy and Competitiveness (grants CGL2012-36251 and CGL2015-64727-P to X.B.), Spanish Ministry of Science and Innovation (grant BFU2011-22404 to M.D.P.) and Catalan Government (2014 SGR 619). The research has also benefited from European Fund for Economic and Regional Development (FEDER) funds. B.F. was supported by the South-Eastern Norway Regional Health Authority grant #2014041. ; Peer reviewed

The influence of DNA methylation on gene behavior and its consequent phenotypic effects appear to be very important, but the details are not well understood. Insects offer a diversity of DNA methylation modes, making them an excellent lineage for comparative analyses. However, functional studies have tended to focus on quite specialized holometabolan species, such as wasps, bees, beetles, and flies. Here, we have studied DNA methylation in the hemimetabolan insect Blattella germanica. In this cockroach, a gene involved in DNA methylation, DNA methyltransferase 1 (DNMT1), is expressed in early embryogenesis. In our experiments, RNAi of DNMT1 reduces DNA methylation and impairs blastoderm formation. Using reduced representation bisulfite sequencing and transcriptome analyses, we observed that methylated genes are associated with metabolism and are highly expressed, whereas unmethylated genes are related to signaling and show low expression. Moreover, methylated genes show greater expression change and less expression variability than unmethylated genes.Developmental Genetics; Molecular Biology ; This work was supported by the Spanish Ministry of Economy and Competitiveness (grants CGL2012- 36251, CGL2015-64727-P and PID2019-104483GB-I00 to XB, including FEDER funds), the CSIC (grant 2019AEP029), and the Catalan Government (grants 2014 SGR 619 and 2017 SGR 1030).

The Piwi‐interacting RNA (piRNA) system is an evolutionarily conserved mechanism involved in the control of transposable elements and maintenance of genomic stability, especially in germ line cells and in early embryo stages. However, relevant particularities, both in mechanism and function, exist across species among metazoans and even within the insect class. As a member of the scarcely studied hemimetabolan group, Blattella germanica can be a suitable reference model to study insect evolution. We present the results of a stringent process of identification and study of expressed piRNAs for B. germanica across 11 developmental stages, ranging from unfertilized egg to nymphs and adult female. Our results confirm the dual origin of piRNA in this species, with a majority of them being generated from the primary pathway, and a smaller but highly expressed set of sequences participating in the secondary ("ping‐pong") reamplification pathway. An intriguing partial complementarity in expression is observed between the piRNA of the two biogenesis pathways, with those generated in the secondary pathway being quite restricted to early embryo stages. In addition, many piRNAs are exclusively expressed in late embryo and nymphal stages. These observations point at piRNA functions beyond the role of transposon control in early embryogenesis. Our work supports the view of a more complex scenario, with different sets of piRNAs acting in different times and having a range of functions wider than previously thought. ; This work was supported by the Spanish Ministry of Economy and Competitiveness (grants CGL2012-36251 and CGL2015-64727-P to X.B.; and CGL2016-76011-R to M.D.P.), the Spanish Ministry of Science and Innovation (grant BFU2011-22404) and the Catalan Government (2014 SGR 619). It also received financial assistance from the European Fund for Economic and Regional Development (FEDER funds to X.B. and M.D.P.). ; Peer reviewed

The German cockroach, Blattella germanica, is a worldwide pest that infests buildings, including homes, restaurants, and hospitals, often living in unsanitary conditions. As a disease vector and producer of allergens, this species has major health and economic impacts on humans. Factors contributing to the success of the German cockroach include its resistance to a broad range of insecticides, immunity to many pathogens, and its ability, as an extreme generalist omnivore, to survive on most food sources. The recently published genome shows that B. germanica has an exceptionally high number of protein coding genes. In this study, we investigate the functions of the 93 significantly expanded gene families with the aim to better understand the success of B. germanica as a major pest despite such inhospitable conditions. We find major expansions in gene families with functions related to the detoxification of insecticides and allelochemicals, defense against pathogens, digestion, sensory perception, and gene regulation. These expansions might have allowed B. germanica to develop multiple resistance mechanisms to insecticides and pathogens, and enabled a broad, flexible diet, thus explaining its success in unsanitary conditions and under recurrent chemical control. The findings and resources presented here provide insights for better understanding molecular mechanisms that will facilitate more effective cockroach control. ; We thank the Deutsche Forschungsgemeinschaft for providing funding for this research to M.C.H. via grant BO2544/11‐1 to E.B.B., and acknowledge United States National Science Foundation grant IOS1557864 to C.S. X.B. & M.‐D.P. were supported by the Spanish Ministry of Economy and Competitiveness (grants CGL2015‐64727‐P to X.B. and CGL2016‐76011‐R to M.‐D.P., both with FEDER funds) and Catalan Government (grant 2017 SGR 1030). ; Peer reviewed