High nucleotide divergence in developmental regulatory genes contrasts with the structural elements of olfactory pathways in caenorhabditis

Abstract

Almost all organismal function is controlled by pathways composed of interacting genetic components. The relationship between pathway structure and the evolution of individual pathway components is not completely understood. For the nematode Caenorhabditis elegans, chemosensory pathways regulate critical aspects of an individual's life history and development. To help understand how olfaction evolves in Caenorhabditis and to examine patterns of gene evolution within transduction pathways in general, we analyzed nucleotide variation within and between species across two well-characterized olfactory pathways, including regulatory genes controlling the fate of the cells in which the pathways are expressed. In agreement with previous studies, we found much higher levels of polymorphism within C. remanei than within the related species C. elegans and C. briggsae. There are significant differences in the rates of nucleotide evolution for genes across the two pathways but no particular association between evolutionary rate and gene position, suggesting that the evolution of functional pathways must be considered within the context of broader gene network structure. However, developmental regulatory genes show both higher levels of divergence and polymorphism than the structural genes of the pathway. These results show that, contrary to the emerging paradigm in the evolution of development, important structural changes can accumulate in transcription factors.

Figure 1.—

Olfactory pathways mediated by the neurons AWA and AWC within Caenorhabditis elegans. Each pathway corresponds to one of the two main types of olfactory pathways found in invertebrates and vertebrates. AWA activates a TRPV channel and AWC activates a cyclic nucleotide-gated channel. The nuclear receptor odr-7 controls the identity of the AWA neurons, by inducing AWA-specific genes and repressing AWC-specific genes. The homeobox ceh-36 controls the identity of the AWC neurons.

Figure 2.—

Maximum likelihood estimates of the rates of amino acid replacements (d_N) and synonymous changes (d_S), and the corresponding ratio (d_N/d_S), across the phylogenetic tree including C. elegans, C. briggsae, and C. remanei. The genes are listed in order of their relative position within the pathways. The degree of divergence varies along the AWA and AWC pathways. With the exception of the G protein gpa-5 and the guanylyl cyclase daf-11, the transcription factors odr-7 and ceh-36 exhibit more interspecific divergence than the structural component of the two pathways. TF, transcription factor; STR, seven-transmembrane receptor; G protein, guanine nucleotide binding protein; GCY, guanylyl cyclase.

Figure 3.—

The transcription factors controlling the differentiation of the AWA and AWC neurons evolve on average faster than structural olfactory genes. Divergence is measured across the phylogenetic tree including C. elegans, C. briggsae, and C. remanei.

Figure 4.—

Frequency distribution of nonsynonymous and synonymous polymorphisms in C. remanei. Amino acid replacement polymorphism is strongly skewed toward rare variants, suggesting that slightly deleterious mutations segregate in C. remanei.