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. 2013 Feb 26;14(2):R20.
doi: 10.1186/gb-2013-14-2-r20.

Transcriptome analyses of primitively eusocial wasps reveal novel insights into the evolution of sociality and the origin of alternative phenotypes

Pedro G Ferreira, Solenn Patalano, Ritika Chauhan, Richard Ffrench-Constant, Toni Gabaldón, Roderic Guigó, Seirian Sumner

Transcriptome analyses of primitively eusocial wasps reveal novel insights into the evolution of sociality and the origin of alternative phenotypes

Pedro G Ferreira et al. Genome Biol. .

Abstract

Background: Understanding how alternative phenotypes arise from the same genome is a major challenge in modern biology. Eusociality in insects requires the evolution of two alternative phenotypes - workers, who sacrifice personal reproduction, and queens, who realize that reproduction. Extensive work on honeybees and ants has revealed the molecular basis of derived queen and worker phenotypes in highly eusocial lineages, but we lack equivalent deep-level analyses of wasps and of primitively eusocial species, the latter of which can reveal how phenotypic decoupling first occurs in the early stages of eusocial evolution.

Results: We sequenced 20 Gbp of transcriptomes derived from brains of different behavioral castes of the primitively eusocial tropical paper wasp Polistes canadensis. Surprisingly, 75% of the 2,442 genes differentially expressed between phenotypes were novel, having no significant homology with described sequences. Moreover, 90% of these novel genes were significantly upregulated in workers relative to queens. Differential expression of novel genes in the early stages of sociality may be important in facilitating the evolution of worker behavioral complexity in eusocial evolution. We also found surprisingly low correlation in the identity and direction of expression of differentially expressed genes across similar phenotypes in different social lineages, supporting the idea that social evolution in different lineages requires substantial de novo rewiring of molecular pathways.

Conclusions: These genomic resources for aculeate wasps and first transcriptome-wide insights into the origin of castes bring us closer to a more general understanding of eusocial evolution and how phenotypic diversity arises from the same genome.

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Figures

Figure 1
Figure 1
Phenotypes produced through the life cycle of the tropical paper wasp Polistes canadensis. Queens and workers show specific behaviors - reproduction or provisioning, respectively. Foundresses show both worker and queen behaviors, and additionally build new nests, whilst callows (newly emerged females; <2 days old) exhibit none of these behaviors. Colonies are founded, and males and females produced, throughout the year with no seasonal diapause.
Figure 2
Figure 2
Sequence and expression characterization of the transcripts with and without detected homologs. (a) Length and longest ORF length statistics. (b) Percentage of transcripts with known protein domains. (c) Distribution of GC-content. (d) Potential to be protein coding. (e) Distribution of the median expression across all the castes. (f) Codon-usage frequencies. RPKM, reads per kilobase per million.
Figure 3
Figure 3
Phylogenetic relationships across hymenopterans with sequenced genomes or transcriptomes. (a) Phylogeny inferred from a maximum-likelihood analysis of a set of 93 conserved proteins (see Materials and methods). The coleopteran Tribolium castaneum and the crustacean Daphnia pulex are used as out-groups. P. canadensis (blue) appears basal to a clade formed by ants (yellow) and bees (red), suggesting Vespoidea (ants + aculeate wasps) are not monophyletic. Non-maximal support values are indicated in the corresponding branches, and are based on Shimodaira-Hasegawa-like approximate likelihood ratio tests. This topology is statistically more supported than the alternative scenario in which Polistes is the sister group of ants (see Materials and methods). (b) Consensus tree from the Bayesian analysis places Polistes as sister group to the ants, supporting the classical scenario. All nodes received maximal posterior probability except the one supporting the monophyly of Vespoidea. Other differences between the maximum-likelihood and Bayesian analyses concern the internal branching order within bees and ants.
Figure 4
Figure 4
Differentially expressed genes in the four phenotypes. Distribution of gene expression (log10 transformed RPKMs (reads per kilobase per million)) between one phenotype versus the others, with differentially expressed transcripts highlighted. Colours represent different probability values. Darker regions represent higher transcript density. Number of differently expressed transcripts at different NOISeq [59] probability values are also presented.
Figure 5
Figure 5
Differentially expressed genes in queen versus worker comparison and GO terms over-represented in each caste. Only the most specific terms, as obtained from the Blast2Go analysis, are represented. See Additional file 5 for the expanded set.
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