Evolutionary genetics of phenotypic novelty
The evolutionary genetic basis of phenotypic novelty is one of the major unresolved questions in evolutionary biology. In short, changes to the coding sequences of genes, changes to the regulatory DNA controlling gene expression (temporal and spatial), gene duplications, and taxonomically restricted genes (TRGs) can all contribute to phenotypic novelty, but the relative roles played by each in various contexts are poorly understood. Previously, we conducted a study showing that orphan genes, the most taxonomically restricted of TRGs (genes found in only one species) may be important for social evolution in honey bees (Johnson and Tsutsui 2011). We followed up on this study with a large scale RNA-Seq and comparative genomics study to comprehensively explore the contribution of TRGs to novel social phenotypes in the honey bee (Jasper et al 2014). We looked at both novel tissues used for social functions (missing in solitary bee ancestors) and tissues conserved between solitary and social bees. In all, we conducted RNA-Seq across 10 tissues in two honey bee life-history phases.
We made several significant discoveries, but chiefly we found that TRGs contribute disproportionately to the functional basis of all the novel tissues we examined. Fig 1 illustrates some of the results for a subset of tissues. For specialized novel structures like the sting gland and the hypopharyngeal gland (HPG) the percentage of highly expressed genes that are TRGs does not match the percentage of expression coming from TRGs (the categories in the legend represent various groups of TRGs and conserved genes). Essentially, expression stemming from TRGs is strikingly high and TRGs are exerting a disproportionate influence on the function of these novel structures. For conserved tissues, like muscle and malpighian tubules, in contrast, the percentage of highly expressed genes that are TRGs matches the percentage of expression that comes from such genes. TRGs therefore do not contribute disproportionately to the function of such tissues.
In a nutshell, the function of cells having undergone cell-line differentiation into specialized tissues is associated with extremely high expression of genes conferring tissue specific functions. Essentially, more effort goes into specialized functions rather than housekeeping functions in many tissues in the adult organism. We have found that genes conferring specialized functions are often TRGs or conserved genes with high rates of coding sequence change. We also find that key TRGs (and positively selected genes in general) tend to be distal branches of gene networks. They are hence free to change radically in their coding sequence without incurring negative pleiotropic effects. Hence, TRGs, and coding sequence change in general, are fundamental to the evolution of novelty in the adult organism. This is in strong contrast to what happens in development (evo-devo), where coding sequence change (via TRGs or positive selection of conserved genes) is thought to be less significant. Readers can find the complete results in Jasper et al (2014).
Current work in our lab on this topic is focused on extending these results to other groups of insects and on determining how changes to TRGs work together with changes to conserved regulatory genes in novel tissues.