Whether coding or regulatory sequence change is more important to the evolution of phenotypic novelty is one of
biology’s major unresolved questions. The field of evo–devo has shown that in early development changes to regulatory
regions are the dominant mode of genetic change, but whether this extends to the evolution of novel phenotypes in
the adult organism is unclear. Here, we conduct ten RNA-Seq experiments across both novel and conserved tissues in the
honey bee to determine to what extent postdevelopmental novelty is based on changes to the coding regions of
genes. We make several discoveries. First, we show that with respect to novel physiological functions in the adult
animal, positively selected tissue-specific genes of high expression underlie novelty by conferring specialized cellular
functions. Such genes are often, but not always taxonomically restricted genes (TRGs). We further show that positively
selected genes, whether TRGs or conserved genes, are the least connected genes within gene expression networks. Overall,
this work suggests that the evo–devo paradigm is limited, and that the evolution of novelty, postdevelopment,
follows additional rules. Specifically, evo–devo stresses that high network connectedness (repeated use of the same
gene in many contexts) constrains coding sequence change as it would lead to negative pleiotropic effects.
Here, we show that in the adult animal, the converse is true: Genes with low network connectedness (TRGs and
tissue-specific conserved genes) underlie novel phenotypes by rapidly changing coding sequence to perform
new-specialized functions.
Whether coding or regulatory sequence change is more important to the evolution of phenotypic novelty is one ofbiology’s major unresolved questions. The field of evo–devo has shown that in early development changes to regulatoryregions are the dominant mode of genetic change, but whether this extends to the evolution of novel phenotypes inthe adult organism is unclear. Here, we conduct ten RNA-Seq experiments across both novel and conserved tissues in thehoney bee to determine to what extent postdevelopmental novelty is based on changes to the coding regions ofgenes. We make several discoveries. First, we show that with respect to novel physiological functions in the adultanimal, positively selected tissue-specific genes of high expression underlie novelty by conferring specialized cellularfunctions. Such genes are often, but not always taxonomically restricted genes (TRGs). We further show that positivelyselected genes, whether TRGs or conserved genes, are the least connected genes within gene expression networks. Overall,this work suggests that the evo–devo paradigm is limited, and that the evolution of novelty, postdevelopment,follows additional rules. Specifically, evo–devo stresses that high network connectedness (repeated use of the samegene in many contexts) constrains coding sequence change as it would lead to negative pleiotropic effects.Here, we show that in the adult animal, the converse is true: Genes with low network connectedness (TRGs andtissue-specific conserved genes) underlie novel phenotypes by rapidly changing coding sequence to perform
new-specialized functions.
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