E usociality, the reproductive division of labour with overlapping generations and cooperative brood care, is one of the major evolutionary transitions in biology 1 . Although rare, eusociality has been observed in a diverse range of organisms, including shrimps, mole rats and several insect lineages [2][3][4] . A particularly striking case of convergent evolution occurred within the holometabolous Hymenoptera and in the hemimetabolous termites (Isoptera), which are separated by over 350 Myr of evolution 5 . Termites evolved within the cockroaches around 150 Myr ago, towards the end of the Jurassic period 6,7 , about 50 Myr before the first bees and ants appeared 5 . Therefore, identifying the molecular mechanisms common to both origins of eusociality is crucial to understanding the fundamental signatures of these rare evolutionary transitions. While the availability of genomes from many eusocial and non-eusocial hymenopteran species 8 has allowed extensive research into the origins of eusociality within ants and bees [9][10][11] , a paucity of genomic data from cockroaches and termites has precluded large-scale investigations into the evolution of eusociality in this hemimetabolous clade.The conditions under which eusociality arose differ greatly between the two groups. Termites and cockroaches are hemimetabolous and so show a direct development, while holometabolous hymenopterans complete the adult body plan during metamorphosis. In termites, workers are immatures and only reproductive castes are adults 12 , while in Hymenoptera, adult workers and queens represent the primary division of labour. Moreover, termites are diploid and their colonies consist of both male and female workers, and usually a queen and king dominate reproduction. This is in contrast to the haplodiploid system found in Hymenoptera, in which all workers and dominant reproductives are female. It is therefore intriguing that strong similarities have evolved convergently within the termites and the hymenopterans, such as differentiated castes and a nest life with reproductive division of labour. The termites can be subdivided into wood-dwelling and foraging termites. The former belong to the lower termites and produce simple, small colonies with totipotent workers that can become reproductives. Foraging termites (some lower and all higher termites) form large, complex societies, in which worker castes can be irreversible 12 . For this reason, higher, but not lower, termites can be classed as superorganismal 13 . Similarly, within Hymenoptera, varying levels of eusociality exist.Here we provide insights into the molecular signatures of eusociality within the termites. We analysed the genomes of two lower and one higher termite species and compared them to the genome
BackgroundThe ever increasing availability of genomes makes it possible to investigate and compare not only the genomic complements of genes and proteins, but also of RNAs. One class of RNAs, the long noncoding RNAs (lncRNAs) and, in particular, their subclass of long intergenic noncoding RNAs (lincRNAs) have recently gained much attention because of their roles in regulation of important biological processes such as immune response or cell differentiation and as possible evolutionary precursors for protein coding genes. lincRNAs seem to be poorly conserved at the sequence level but at least some lincRNAs have conserved structural elements and syntenic genomic positions. Previous studies showed that transposable elements are a main contribution to the evolution of lincRNAs in mammals. In contrast, plant lincRNA emergence and evolution has been linked with local duplication events. However, little is known about their evolutionary dynamics in general and in insect genomes in particular.ResultsHere we compared lincRNAs between seven insect genomes and investigated possible evolutionary changes and functional roles. We find very low sequence conservation between different species and that similarities within a species are mostly due to their association with transposable elements (TE) and simple repeats. Furthermore, we find that TEs are less frequent in lincRNA exons than in their introns, indicating that TEs may have been removed by selection. When we analysed the predicted thermodynamic stabilities of lincRNAs we found that they are more stable than their randomized controls which might indicate some selection pressure to maintain certain structural elements. We list several of the most stable lincRNAs which could serve as prime candidates for future functional studies. We also discuss the possibility of de novo protein coding genes emerging from lincRNAs. This is because lincRNAs with high GC content and potentially with longer open reading frames (ORF) are candidate loci where de novo gene emergence might occur.ConclusionThe processes responsible for the emergence and diversification of lincRNAs in insects remain unclear. Both duplication and transposable elements may be important for the creation of new lincRNAs in insects.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-017-0985-0) contains supplementary material, which is available to authorized users.
The evolution of division of labor between sterile and fertile individuals represents one of the major transitions in biological complexity. A fascinating gradient in eusociality evolved among the ancient hemimetabolous insects, ranging from noneusocial cockroaches through the primitively social lower termites-where workers retain the ability to reproduce-to the higher termites, characterized by lifetime commitment to worker sterility. Juvenile hormone (JH) is a prime candidate for the regulation of reproductive division of labor in termites, as it plays a key role in insect postembryonic development and reproduction. We compared the expression of JH pathway genes between workers and queens in two lower termites (Zootermopsis nevadensis and Cryptotermes secundus) and a higher termite (Macrotermes natalensis) to that of analogous nymphs and adult females of the noneusocial cockroach Blattella germanica. JH biosynthesis and metabolism genes ranged from reproductive female-biased expression in the cockroach to predominantly worker-biased expression in the lower termites. Remarkably, the expression profile of JH pathway genes sets the higher termite apart from the two lower termites, as well as the cockroach, indicating that JH signaling has undergone major changes in this eusocial termite. These changes go beyond mere shifts in gene expression between the different castes, as we find evidence for positive selection in several termite JH pathway genes. Thus, remodeling of the JH pathway may have played a major role in termite social evolution, representing a striking case of convergent molecular evolution between the termites and the distantly related social hymenoptera.
Around 150 million years ago, eusocial termites evolved from within the cockroaches, 50 million years before eusocial Hymenoptera, such as bees and ants, appeared. Here, we report the first, 2GB genome of a cockroach, Blattella germanica, and the 1.3GB genome of the drywood termite, Cryptotermes secundus. We show evolutionary signatures of termite eusociality by comparing the genomes and transcriptomes of three termites and the cockroach against the background of 16 other eusocial and non-eusocial insects. Dramatic adaptive changes in genes underlying the production and perception of pheromones confirm the importance of chemical communication in the termites. These are accompanied by major changes in gene regulation and the molecular evolution of caste determination.Many of these results parallel molecular mechanisms of eusocial evolution in Hymenoptera. However, the specific solutions are remarkably different, thus revealing a striking case of convergence in one of the major evolutionary transitions in biological complexity.Eusociality, the reproductive division of labour with overlapping generations and cooperative brood care, 1 is one of the major evolutionary transitions in biology.1 Although rare, eusociality has been observed 2 in a diverse range of organisms, including shrimps, mole-rats and several insect lineages. bees and ants appeared. 5 Therefore, identifying the molecular mechanisms common to both origins of 7 eusociality is crucial to understanding the fundamental signatures of these rare evolutionary transitions. 8While the availability of genomes from many eusocial and non-eusocial hymenopteran species 8 has allowed 9 extensive research into the origins of eusociality within ants and bees, 9, 10, 11 a paucity of genomic data 10 from cockroaches and termites has precluded large-scale investigations into the evolution of eusociality 11 in this hemimetabolous clade. 12The conditions under which eusociality arose differ greatly between the two groups. peer-reviewed) is the author/funder. All rights reserved. No reuse allowed without permission.The copyright holder for this preprint (which was not . http://dx.doi.org/10.1101/181909 doi: bioRxiv preprint first posted online Aug. 29, 2017; lower and all higher termites) form large, complex societies, in which worker castes can be irreversible. 12 24For this reason, higher, but not lower, termites can be classed as superorganismal.13 Similarly, within 25Hymenoptera, varying levels of eusociality exist. 26Here we provide insights into the molecular signatures of eusociality within the termites. We analysed 27 the genomes of two lower and one higher termite species and compared them to the first cockroach genome, 28as a closely-related non-eusocial outgroup. Furthermore, differences in expression between nymphs and 29 adults of the cockroach were compared to differences in expression between workers and reproductives of Material) and large expansions in many manually annotated gene families offer high confidence in the 52 accuracy of this proteome size....
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