Taxonomically restricted genes are associated with the evolution of sociality in the honey bee

Abstract

BackgroundStudies have shown that taxonomically restricted genes are significant in number and important for the evolution of lineage specific traits. Social insects have gained many novel morphological and behavioral traits relative to their solitary ancestors. The task repertoire of an advanced social insect, for example, can be 40-50 tasks, about twice that of a solitary wasp or bee. The genetic basis of this expansion in behavioral repertoire is still poorly understood, and a role for taxonomically restricted genes has not been explored at the whole genome level.ResultsHere we present comparative genomics results suggesting that taxonomically restricted genes may have played an important role in generating the expansion of behavioral repertoire associated with the evolution of eusociality. First, we show that the current honey bee official gene set contains about 700 taxonomically restricted genes. These are split between orphans, genes found only in the Hymenoptera, and genes found only in insects. Few of the orphans or genes restricted to the Hymenoptera have been the focus of experimental work, but several of those that have are associated with novel eusocial traits or traits thought to have changed radically as a consequence of eusociality. Second, we predicted that if taxonomically restricted genes are important for generating novel eusocial traits, then they should be expressed with greater frequency in workers relative to the queen, as the workers exhibit most of the novel behavior of the honey bee relative to their solitary ancestors. We found support for this prediction. Twice as many taxonomically restricted genes were found amongst the genes with higher expression in workers compared to those with higher expression in queens. Finally, we compiled an extensive list of candidate taxonomically restricted genes involved in eusocial evolution by analyzing several caste specific gene expression data sets.ConclusionsThis work identifies a large number of candidate taxonomically restricted genes that may have played a role in eusocial evolution. This work thus lays the foundation for future functional genomics work on the evolution of novelty in the context of social behavior. We also present preliminary evidence, based on biased patterns of gene expression, that taxonomically restricted genes may have played a role in the evolution of caste systems, a characteristic lineage specific social trait.

Genome-wide identification of lineage-specific genes within Caenorhabditis elegans

“…After the identification, we characterized the genetic features of SSGs, GSGs, and ECs. Our results illustrated significant differences in the gene length, protein length, exon number, and GC content, the averages of which were consistent with those found in previous studies [5,11,13]. Compared with ECs, the shorter gene size, fewer exons, and fewer transcript supports of SSGs and GSGs may suggest that these LSGs within C. elegans might be evolutionarily young genes.…”

“…According to our results, the averages of the above features of the three gene sets are significantly different from each other (one-way ANOVA; p b 0.01). Similarly, SSGs exhibit the lowest values for each genetic feature, as observed in other species, such as Arabidopsis thaliana [5], zebrafish [13], and honey bee [11]. In contrast, the average GC content of the SSGs was the highest, which is similar to the results obtained in zebrafish [13] but opposite to those found in A. thaliana [5] and honey bee [11].…”

“…Similarly, SSGs exhibit the lowest values for each genetic feature, as observed in other species, such as Arabidopsis thaliana [5], zebrafish [13], and honey bee [11]. In contrast, the average GC content of the SSGs was the highest, which is similar to the results obtained in zebrafish [13] but opposite to those found in A. thaliana [5] and honey bee [11]. The transcriptional analysis based on EST and full-length cDNA revealed that 38.68% of SSGs, 60.27% of GSGs, and 82.74% of ECs have transcripts (t-test, p b 0.01).…”

“…However, study of these genes is helpful to aid in the comprehensive understanding of a species. With the increasing development of sequencing technologies, we have gained access to a number of genomes and transcriptomes from a wide range of species, which has aided the extensive study of the LSGs within mammals [8][9][10], insects [2,11,12], fish [13], plants [5,[14][15][16], and microbial species [17][18][19][20]. However, the LSGs in C. elegans have not yet been researched through genomewide methods.…”

Social insect genomes exhibit dramatic evolution in gene composition and regulation while preserving regulatory features linked to sociality

“…We found an abundance of taxonomically restricted genes (TRGs) in ants as well as a higher rate in the emergence of TRGs in ants compared with flies, suggesting functional ties to eusocial adaptations. In other systems, TRGs can comprise 10%-33% of a species' protein-coding gene complement and have been linked both to morphological adaptations (Khalturin et al 2009;Tautz and Domazet-Lošo 2011) and to eusocial traits, including caste differentiation (Kamakura 2011) and complex behavioral repertoires ( Johnson and Tsutsui 2011). Importantly, while TRGs likely play important roles involved in the elaboration of social adaptations in individual lineages, TRGs that are critical for early eusocial evolution or the maintenance of eusociality should be conserved in multiple ant genomes.…”