The genomes of two key bumblebee species with primitive eusocial organization

Background: The shift from solitary to social behavior is one of the major evolutionary transitions. Primitively eusocial bumblebees are uniquely placed to illuminate the evolution of highly eusocial insect societies. Bumblebees are also invaluable natural and agricultural pollinators, and there is widespread concern over recent population declines in some species. High-quality genomic data will inform key aspects of bumblebee biology, including susceptibility to implicated population viability threats. Results: We report the high quality draft genome sequences of Bombus terrestris and Bombus impatiens, two ecologically dominant bumblebees and widely utilized study species. Comparing these new genomes to those of the highly eusocial honeybee Apis mellifera and other Hymenoptera, we identify deeply conserved similarities, as well as novelties key to the biology of these organisms. Some honeybee genome features thought to underpin advanced eusociality are also present in bumblebees, indicating an earlier evolution in the bee lineage. Xenobiotic detoxification and immune genes are similarly depauperate in bumblebees and honeybees, and multiple categories of genes linked to social organization, including development and behavior, show high conservation. Key differences identified include a bias in bumblebee chemoreception towards gustation from olfaction, and striking differences in microRNAs, potentially responsible for gene regulation underlying social and other traits. Conclusions: These two bumblebee genomes provide a foundation for post-genomic research on these key pollinators and insect societies. Overall, gene repertoires suggest that the route to advanced eusociality in bees was mediated by many small changes in many genes and processes, and not by notable expansion or depauperation

The first myriapod genome sequence reveals conservative arthropod gene content and genome organisation in the centipede Strigamia maritima.

Myriapods (e.g., centipedes and millipedes) display a simple homonomous body plan relative to other arthropods. All members of the class are terrestrial, but they attained terrestriality independently of insects. Myriapoda is the only arthropod class not represented by a sequenced genome. We present an analysis of the genome of the centipede Strigamia maritima. It retains a compact genome that has undergone less gene loss and shuffling than previously sequenced arthropods, and many orthologues of genes conserved from the bilaterian ancestor that have been lost in insects. Our analysis locates many genes in conserved macro-synteny contexts, and many small-scale examples of gene clustering. We describe several examples where S. maritima shows different solutions from insects to similar problems. The insect olfactory receptor gene family is absent from S. maritima, and olfaction in air is likely effected by expansion of other receptor gene families. For some genes S. maritima has evolved paralogues to generate coding sequence diversity, where insects use alternate splicing. This is most striking for the Dscam gene, which in Drosophila generates more than 100,000 alternate splice forms, but in S. maritima is encoded by over 100 paralogues. We see an intriguing linkage between the absence of any known photosensory proteins in a blind organism and the additional absence of canonical circadian clock genes. The phylogenetic position of myriapods allows us to identify where in arthropod phylogeny several particular molecular mechanisms and traits emerged. For example, we conclude that juvenile hormone signalling evolved with the emergence of the exoskeleton in the arthropods and that RR-1 containing cuticle proteins evolved in the lineage leading to Mandibulata. We also identify when various gene expansions and losses occurred. The genome of S. maritima offers us a unique glimpse into the ancestral arthropod genome, while also displaying many adaptations to its specific life history.This work was supported by the following grants: NHGRIU54HG003273 to R.A.G; EU Marie Curie ITN #215781 “Evonet” to M.A.; a Wellcome Trust Value in People (VIP) award to C.B. and Wellcome Trust graduate studentship WT089615MA to J.E.G; Marine rhythms of Life” of the University of Vienna, an FWF (http://www.fwf.ac.at/) START award (#AY0041321) and HFSP (http://www.hfsp.org/) research grant (#RGY0082/2010) to KT-­‐R; MFPL Vienna International PostDoctoral Program for Molecular Life Sciences (funded by Austrian Ministry of Science and Research and City of Vienna, Cultural Department -­‐Science and Research to T.K; Direct Grant (4053034) of the Chinese University of Hong Kong to J.H.L.H.; NHGRI HG004164 to G.M.; Danish Research Agency (FNU), Carlsberg Foundation, and Lundbeck Foundation to C.J.P.G.; U.S. National Institutes of Health R01AI55624 to J.H.W.; Royal Society University Research fellowship to F.M.J.; P.D.E. was supported by the BBSRC via the Babraham Institute;This is the final version of the article. It first appeared from PLOS via http://dx.doi.org/10.1371/journal.pbio.100200

The first myriapod genome sequence reveals conservative arthropod gene content and genome organisation in the centipede Strigamia maritima.

Myriapods (e.g., centipedes and millipedes) display a simple homonomous body plan relative to other arthropods. All members of the class are terrestrial, but they attained terrestriality independently of insects. Myriapoda is the only arthropod class not represented by a sequenced genome. We present an analysis of the genome of the centipede Strigamia maritima. It retains a compact genome that has undergone less gene loss and shuffling than previously sequenced arthropods, and many orthologues of genes conserved from the bilaterian ancestor that have been lost in insects. Our analysis locates many genes in conserved macro-synteny contexts, and many small-scale examples of gene clustering. We describe several examples where S. maritima shows different solutions from insects to similar problems. The insect olfactory receptor gene family is absent from S. maritima, and olfaction in air is likely effected by expansion of other receptor gene families. For some genes S. maritima has evolved paralogues to generate coding sequence diversity, where insects use alternate splicing. This is most striking for the Dscam gene, which in Drosophila generates more than 100,000 alternate splice forms, but in S. maritima is encoded by over 100 paralogues. We see an intriguing linkage between the absence of any known photosensory proteins in a blind organism and the additional absence of canonical circadian clock genes. The phylogenetic position of myriapods allows us to identify where in arthropod phylogeny several particular molecular mechanisms and traits emerged. For example, we conclude that juvenile hormone signalling evolved with the emergence of the exoskeleton in the arthropods and that RR-1 containing cuticle proteins evolved in the lineage leading to Mandibulata. We also identify when various gene expansions and losses occurred. The genome of S. maritima offers us a unique glimpse into the ancestral arthropod genome, while also displaying many adaptations to its specific life history

Multifaceted biological insights from a draft genome sequence of the tobacco hornworm moth, <i>Manduca sexta</i>

Manduca sexta, known as the tobacco hornworm or Carolina sphinx moth, is a lepidopteran insect that is used extensively as a model system for research in insect biochemistry, physiology, neurobiology, development, and immunity. One important benefit of this species as an experimental model is its extremely large size, reaching more than 10 g in the larval stage. M. sexta larvae feed on solanaceous plants and thus must tolerate a substantial challenge from plant allelochemicals, including nicotine. We report the sequence and annotation of the M. sexta genome, and a survey of gene expression in various tissues and developmental stages. The Msex_1.0 genome assembly resulted in a total genome size of 419.4 Mbp. Repetitive sequences accounted for 25.8% of the assembled genome. The official gene set is comprised of 15,451 protein-coding genes, of which 2498 were manually curated. Extensive RNA-seq data from many tissues and developmental stages were used to improve gene models and for insights into gene expression patterns. Genome wide synteny analysis indicated a high level of macrosynteny in the Lepidoptera. Annotation and analyses were carried out for gene families involved in a wide spectrum of biological processes, including apoptosis, vacuole sorting, growth and development, structures of exoskeleton, egg shells, and muscle, vision, chemosensation, ion channels, signal transduction, neuropeptide signaling, neurotransmitter synthesis and transport, nicotine tolerance, lipid metabolism, and immunity. This genome sequence, annotation, and analysis provide an important new resource from a well-studied model insect species and will facilitate further biochemical and mechanistic experimental studies of many biological systems in insects

Presence and absence of immunity genes in different arthropods.

<p>Counts of immune genes are shown for <i>S. maritima</i>, <i>D. pulex</i><a href="http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002005#pbio.1002005-McTaggart1" target="_blank">[131]</a>, <i>A. mellifera</i><a href="http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002005#pbio.1002005-Evans1" target="_blank">[86]</a>, <i>T. castaneum</i>, <i>Anopheles gambiae</i>, and <i>D. melanogaster</i><a href="http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002005#pbio.1002005-Dasmahapatra1" target="_blank">[132]</a>. ∼, identity of the gene is uncertain; -, not investigated.</p

Ancestral protein kinases are extensively lost during arthropod evolution.

<p><i>S. maritima</i> is an exception and retains the largest number of ancestral kinases. Numbers of kinase subfamilies in selected species are shown in parentheses after species names. The gains, losses, and inferred content of common ancestors are listed on internal branches. Kinases found in at least two species from human, <i>C. elegans</i> and <i>Nematostella vectenesis</i> were used as an outgroup.</p

Homeobox gene clusters.

<p>(A) The Hox gene cluster of <i>S. maritima</i> compared to the cluster that can be deduced for the ancestral arthropod. <i>S. maritima</i> provides the first instance of an arthropod Hox cluster with tight linkage of an <i>Even-skipped (Eve)</i> gene (see text). Hox3 is the only gene missing from the <i>S. maritima</i> Hox cluster, but may be present elsewhere in the genome on a separate scaffold (see main text and <a href="http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002005#pbio.1002005.s072" target="_blank">Text S1</a> for details). The <i>S. maritima</i> cluster is drawn approximately to scale and spans 457 kb from the start codon of <i>labial (lab)</i> to the start codon of <i>Eve-b</i>. Arrows denote the transcriptional orientation. (B) Remains of clustering and linkage of ANTP class genes in <i>S. maritima</i>. The blue boxes are genes belonging to the ANTP class. The brown box is a gene belonging to the HNF class. The orange box is a gene belonging to the SINE class. The intergenic distances are indicated in kb. (C) Clusters of non-ANTP class homeobox genes in <i>S. maritima</i>. The green boxes are genes belonging to the TALE class. The red boxes are genes belonging to the PRD class. The intergenic distances are indicated in kb, except in the case of Rx-Hbn as these genes are overlapping but with opposite transcriptional orientations. All scaffold numbers are indicated in brackets.</p

Plot showing that DNA from a male individual contains a distinct fraction of scaffolds that is underrepresented (black arrow), and presumably derives from heterogametic sex chromosomes.

<p>No such fraction is present in the sequenced DNA of two individual females. The data underlying this plot is presented in <a href="http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002005#pbio.1002005.s068" target="_blank">File S4</a>.</p

Expansion of chemosensory receptor families.

<p>(A) Phylogenetic relationships among <i>S. maritima</i> (Smar), <i>I. scapularis</i> (Isca), <i>D. pulex</i> (Dpul), and a few insect GRs that encode for sugar, fructose, and carbon dioxide receptors (Dmel, <i>D. melanogaster</i>, and Amel, <i>A. mellifera</i>). (B) Phylogenetic relationships among <i>S. maritima</i>, <i>I. scapularis</i>, and a few <i>D. melanogaster</i> IRs and IgluR genes (the suffix at the end of the protein names indicates: i, incomplete and p, pseudogene).</p

Conserved macro synteny signal between <i>S. maritima</i> and the chordate lancelet <i>B. floridae</i> clustered into ancestral linkage groups.

<p>Each dot represents a pair of genes, one in <i>B. floridae</i>, one in <i>S. maritima</i>, assigned to the same gene family by our orthology analysis. The ancestral linkage group identifiers refer to groups of scaffolds from the <i>S. maritima</i> (SmALG) or <i>B. floridae</i> (BfALG) assemblies, as detailed in <a href="http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002005#pbio.1002005.s066" target="_blank">File S2</a>. The identification of ALGs is described in the SI. Note that two <i>S. maritima</i> scaffolds were divided across ALGs, and so appear multiple times in <a href="http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002005#pbio.1002005.s066" target="_blank">File S2</a>.</p