Abstract

Evolutionary developmental biology focuses on understanding the origin and evolution of extant biological variation, and the genetic basis for this variation. The genetic toolkit appears largely finite across animals, such that a combination of regulatory evolution, gene recruitment (co-option) and genetic modularity often allow morphological and developmental diversity to arise. Here we summarize a number of observations from across animals, which together suggest that many genes and gene product interaction “modules” originally characterized for their role in the germ line also have neural roles. We explore potential explanations for this observation, noting that in the context of the germ line, these genes appear to have molecular and biochemical properties that make them well-suited to breaking symmetry within cells. The resulting asymmetry is often caused by gene products co-localizing asymmetrically to sub-cellular, non-membrane-bound, electron dense compartments known as ribonucleoprotein (RNP) granules. RNP granules contain high concentrations of translationally quiescent messenger RNAs and proteins and are thought to act as hubs of localized translational control. We propose that the use of strict translational control, which may be achieved molecular processes important for RNP granule formation and/or small RNA-related processes, is an important property of and a commonality between the germ line and nervous tissues, and help explain, at least in part, the close relationship between these two tissue types.

Highlights

  • Understanding the genomic basis of extant biological variation over evolutionary time scales has been the main focus of modern evolutionary developmental biology research

  • Pleiotropy is widespread in genomes, can contribute to phenotypic variation, and may occur through a variety of molecular mechanisms (Guillaume and Otto, 2012), including alternative splicing, different substrate or binding partner affinities, localization to different cellular compartments or tissues, or the same gene product having more than one distinct biochemical property

  • Because we aim to point out conserved molecular interactions reported in both cell types, we discuss those genes with more abundant co-IP and other interaction data in both germ line and nervous system first, and end with genes for which data are available primarily for only one tissue type

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Summary

Introduction

Understanding the genomic basis of extant biological variation over evolutionary time scales has been the main focus of modern evolutionary developmental biology (evo-devo) research. In other cases, conserved genes have been co-opted for additional, distinct biological roles, leading to pleiotropic gene functions (e.g., distalless, yellow) (Panganiban et al, 1997; Gompel et al, 2005; Moczek and Rose, 2009; Khila et al, 2012). Both scenarios contribute to morphological diversity between species, within species, and between cell types within an organism, underpinned by a combination of differences in developmental gene regulation and modularity. Barring the extreme cases of “housekeeping” genes (usually ubiquitously expressed) and socalled “luxury” genes (expressed in only one tissue type) (King et al, 2013), most animal genes likely exhibit some degree of pleiotropy (Hodgkin, 1998)

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