Exploring the Genotype-to-Phenotype Map Using Quantifiable Patterns in Metazoan Genomic and Morphological Data

AbstractA prevailing problem in evolutionary biology is elucidating the genotype-to-phenotype map that characterizes how genomic activities regulate different aspects of organismal morphology and their variability in both space and time. Here, we explore potential causality between genome content and both morphological complexity and disparity by compiling the regulatory components (i.e., transcription factors, RNA-binding proteins, and microRNA families) as well as a representative set of nonregulatory housekeeping genes in 32 species belonging to a wide variety of animal phyla spanning a range of morphological, ecological, and genomic characteristics. A principal component analysis of these four nonoverlapping genomic components from each of these 32 species in relation to their last common ancestor revealed that no relationship exists between genome space and disparity, as changes to animal body plans appear to be largely the result of changes to the regulatory networks that govern animal development rather than gaining or losing specific sets of regulatory genes. However, using both phylogenetically correlated and phylogenetically uncorrelated statistical tests, we find a strong relationship between the loss of all considered gene types in some parasitic taxa, an exacerbation of a trend that characterizes animal genomes in general. We also find a strong correlation, and a likely causal relationship, between microRNA innovations and organismal complexity. While this analysis of genomic features suggests how complexity and disparity are each encoded in the genome, further analysis of the regulatory networks in which they participate should provide a more comprehensive description of how organisms diversify their morphologies through time.