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Spinning gland transcriptomics from two main clades of spiders (order: Araneae)--insights on their molecular, anatomical and behavioral evolution.

ABSTRACT: Characterized by distinctive evolutionary adaptations, spiders provide a comprehensive system for evolutionary and developmental studies of anatomical organs, including silk and venom production. Here we performed cDNA sequencing using massively parallel sequencers (454 GS-FLX Titanium) to generate ?80,000 reads from the spinning gland of Actinopus spp. (infraorder: Mygalomorphae) and Gasteracantha cancriformis (infraorder: Araneomorphae, Orbiculariae clade). Actinopus spp. retains primitive characteristics on web usage and presents a single undifferentiated spinning gland while the orbiculariae spiders have seven differentiated spinning glands and complex patterns of web usage. MIRA, Celera Assembler and CAP3 software were used to cluster NGS reads for each spider. CAP3 unigenes passed through a pipeline for automatic annotation, classification by biological function, and comparative transcriptomics. Genes related to spider silks were manually curated and analyzed. Although a single spidroin gene family was found in Actinopus spp., a vast repertoire of specialized spider silk proteins was encountered in orbiculariae. Astacin-like metalloproteases (meprin subfamily) were shown to be some of the most sampled unigenes and duplicated gene families in G. cancriformis since its evolutionary split from mygalomorphs. Our results confirm that the evolution of the molecular repertoire of silk proteins was accompanied by the (i) anatomical differentiation of spinning glands and (ii) behavioral complexification in the web usage. Finally, a phylogenetic tree was constructed to cluster most of the known spidroins in gene clades. This is the first large-scale, multi-organism transcriptome for spider spinning glands and a first step into a broad understanding of spider web systems biology and evolution.

SUBMITTER: Prosdocimi F

PROVIDER: S-EPMC3126850 | biostudies-literature | 2011

REPOSITORIES: biostudies-literature

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Spinning gland transcriptomics from two main clades of spiders (order: Araneae)--insights on their molecular, anatomical and behavioral evolution.

Prosdocimi Francisco F Bittencourt Daniela D da Silva Felipe Rodrigues FR Kirst Matias M Motta Paulo C PC Rech Elibio L EL

PloS one 20110629 6

Characterized by distinctive evolutionary adaptations, spiders provide a comprehensive system for evolutionary and developmental studies of anatomical organs, including silk and venom production. Here we performed cDNA sequencing using massively parallel sequencers (454 GS-FLX Titanium) to generate ∼80,000 reads from the spinning gland of Actinopus spp. (infraorder: Mygalomorphae) and Gasteracantha cancriformis (infraorder: Araneomorphae, Orbiculariae clade). Actinopus spp. retains primitive cha ...[more]

PMID: 21738742

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Project description:BackgroundHabronattus is a diverse clade of jumping spiders with complex courtship displays and repeated evolution of Y chromosomes. A well-resolved species phylogeny would provide an important framework to study these traits, but has not yet been achieved, in part because the few genes available in past studies gave conflicting signals. Such discordant gene trees could be the result of incomplete lineage sorting (ILS) in recently diverged parts of the phylogeny, but there are indications that introgression could be a source of conflict.ResultsTo infer Habronattus phylogeny and investigate the cause of gene tree discordance, we assembled transcriptomes for 34 Habronattus species and 2 outgroups. The concatenated 2.41 Mb of nuclear data (1877 loci) resolved phylogeny by Maximum Likelihood (ML) with high bootstrap support (95-100%) at most nodes, with some uncertainty surrounding the relationships of H. icenoglei, H. cambridgei, H. oregonensis, and Pellenes canadensis. Species tree analyses by ASTRAL and SVDQuartets gave almost completely congruent results. Several nodes in the ML phylogeny from 12.33 kb of mitochondrial data are incongruent with the nuclear phylogeny and indicate possible mitochondrial introgression: the internal relationships of the americanus and the coecatus groups, the relationship between the altanus, decorus, banksi, and americanus group, and between H. clypeatus and the coecatus group. To determine the relative contributions of ILS and introgression, we analyzed gene tree discordance for nuclear loci longer than 1 kb using Bayesian Concordance Analysis (BCA) for the americanus group (679 loci) and the VCCR clade (viridipes/clypeatus/coecatus/roberti groups) (517 loci) and found signals of introgression in both. Finally, we tested specifically for introgression in the concatenated nuclear matrix with Patterson's D statistics and DFOIL. We found nuclear introgression resulting in substantial admixture between americanus group species, between H. roberti and the clypeatus group, and between the clypeatus and coecatus groups.ConclusionsOur results indicate that the phylogenetic history of Habronattus is predominantly a diverging tree, but that hybridization may have been common between phylogenetically distant species, especially in subgroups with complex courtship displays.

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Dataset Information

Spinning gland transcriptomics from two main clades of spiders (order: Araneae)--insights on their molecular, anatomical and behavioral evolution.

Publications

Spinning gland transcriptomics from two main clades of spiders (order: Araneae)--insights on their molecular, anatomical and behavioral evolution.

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