Capturing changes to animal complexity from quantifiable patterns in genomic data

A prevailing problem in evolutionary biology is elucidating the "genotype-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 non-regulatory "housekeeping genes" in 32 species belonging to a wide variety of animal phyla, altogether encapsulating a number of varying genomic characteristics and morphological diversities. A principal component analysis of these four non-overlapping 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 gene regulatory networks that govern animal development rather than gaining or losing specific sets of regulatory genes. However, using both phylogenetically correlated as well as phylogenetically uncorrelated statistical tests, we find a strong relationship between the loss of all considered gene types and the advent of some parasitic taxa, as well as 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 over time through alterations in their genomic components. SIGNIFICANCE STATEMENTVariation in morphological form can be measured by considering either disparity (i.e., the amount of variance in morphological form) or complexity (i.e., the difference in the number of their "parts" including genes or cells). To date, discerning the genomic basis of either has remained largely unknown. Here, we compile the regulatory genome of the last common ancestor of bilaterian metazoans, including its transcription factors, RNA-binding proteins and microRNA families, and ask how changes to these repertoires potentially reflects changes in either disparity or complexity. We find that although there is no relationship between the regulatory genome and disparity, there is a robust relationship between the loss of regulatory genes relative to housekeeping genes, especially in parasitic taxa. Further, there is a strong relationship between increases to microRNAs and complexity, which likely reflects the unique role microRNAs play in increasing both the accuracy and the precision of gene expression during development.