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Wasp Transcriptome Analysis Hints at Evolution of Social Behavior

NEW YORK (GenomeWeb News) – Worker wasps have a more active transcriptome than queen wasps do, Seirian Sumner, a senior lecturer at the University of Bristol, and her colleagues reported in Genome Biology yesterday.

Workers, queens, and other social wasp castes share the same genome, but how that genome leads to alternative phenotypes like workers and queens is not fully known, especially as social wasps, and other social insects, are derived from non-social, solitary ancestors. In social wasps, queen wasps are responsibly mainly for reproduction while workers care for the offspring.

"Extensive work on honeybees and ants has revealed the molecular basis of derived queen and worker phenotypes in highly eusocial lineages," Sumner and her colleagues wrote, "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."

The researchers focused their analysis on the tropical paper wasp, Polistes canadensis, which is a primitively eusocial insect.

To ascertain whether there is differential gene expression in the brains of tropical paper wasps belonging to different castes, the researchers delved into 20 gigabases of transcripts, finding a number of novel genes that are up-regulated in worker wasps. Additionally, only a few genes known to be expressed in castes of other social insects appeared to be expressed by tropical paper wasp castes. The researchers also examined the phylogenetic relationship between ants, bees, and wasps using their transcriptome data.

Sumner and her colleagues first developed a genome-wide catalog of expressed wasp genes by assembling 2.1 million 454 reads from 37 wasps — including queens, workers, foundresses, and callows — into a reference transcriptome of 26,284 isogroups. The researchers noted that about 37 percent of the P. canadensis genes have known homologs, while 62 percent did not.

The researchers then turned to RNA-seq, examining the transcriptome of the four different wasp castes by sequencing 3 gigabases of brain cDNA with the Illumina platform. Just over 9 percent of the 26,284 P. canadensis genes, or 2,442 genes, were found to be differentially expressed.

Workers, the researchers noted, up-regulated a particularly high proportion of genes. As compared to queens, workers up-regulated nearly 1800 of the 1909 genes whose expression varied between workers and queens; queens up-regulated 112 of those genes.

"These results support the emerging picture that much of phenotypic evolution occurs in workers, rather than queens, and provide the first suggestion that molecular evolution of the worker caste is in place early in social evolution," Sumner and her colleagues said in the paper.

Most down-regulated genes, the researchers also reported, were found in callows and foundresses. They added that this implies that callows are neither worker-like nor queen-like. Further, foundresses, which have been thought to be sort of hopeful queens in that they co-found nests, may in fact be different from queens. "Taken together, these results highlight how the definition of a phenotype in this species is more complex than a simple distinction between queens and workers," the researchers noted.

Both known and novel genes appear to play a role in the development of wasp social behavior. About a quarter of the 2,442 differentially expressed genes have homologs, though about 80 percent of genes up-regulated in workers appeared to be novel, while about 17 percent of genes up-regulated in queens were. The researchers also found that a number of those up-regulated genes appeared to be long, noncoding RNAs, which are thought to influence gene regulation.

Meanwhile, Sumner and her colleagues also examined whether a conserved set of genes related to caste evolution in other social insects is active in wasps. They found, however, little connection between caste-related genes in honeybees or fire ants and ones in paper wasps, indicating that genes underlying castes may differ between lineages.

Additionally, Sumner and her colleagues drew on their transcriptome analysis to examine the phylogenetic relationships between ants, bees, and wasps. Fossil and other analyses have placed ants and wasps in the same clade, called Vespopoidea, and bees in a separate group. However, in this paper, the researchers' maximum-likelihood analysis of 93 conserved orthologs put Polsities as a basal sister group to ants and bees.

If primitive eusocial wasps belong to a basal sister group to ants and bees, "this finding would have important general implications for our understanding of eusociality as it would suggest that bees and ants shared an aculeate wasp-like ancestor, that ants are wingless wasps, and that bees are wasps that lost predacious behaviors," Sumner said in a statement.