Adaptive evolution in the SRZ chemoreceptor families of Caenorhabditis elegans and Caenorhabditis briggsae

Abstract

We investigated the possibility of positive selection acting on members of the putative seven-pass chemoreceptor superfamily in Caenorhabditis elegans, which comprises Ϸ1,300 genes encoding seven-pass G protein-coupled receptors (GPCRs). Using a maximum-likelihood approach, we conducted statistical tests for evidence of codon sites where the ratio of nonsynonymous substitutions per nonsynonymous site to synonymous substitutions per synonymous site (d N͞dS) was >1. Evidence for positive selection was found only for the srz family, about which virtually nothing specific is known. We extended the annotation of the srz gene family, establishing gene models for 60 srz genes in C. elegans and 28 srz genes in Caenorhabditis briggsae. d N͞dS ratios varied dramatically in different regions of the SRZ proteins, peaking in predicted extracellular regions. These regions included 23 sites where evidence of positive selection was highly significant, corresponding remarkably well with regions implicated in ligand binding in other GPCR family members. We interpret these results as indicating that the srz family is under positive selection, probably driven by ligand binding.positive selection ͉ ligand binding ͉ maximum likelihood ͉ synonymous ͉ nonsynonymous C aenorhabditis elegans has Ϸ1,300 predicted genes that encode members of putative chemosensory receptors and together define the seven-pass receptor (SR) superfamily (1-4), which belongs to the broader class of G protein-coupled receptors (GPCRs). Based on sequence alignment and phylogenetic analysis, SR superfamily members fall into about a dozen families. These families range in size from the large srh and str families (a few hundred genes each) to the modestly sized sra and srv families (Ϸ30 genes each). Each SR family appears to have arisen by gene duplication and divergence from a founder gene. These duplications have occurred sporadically over a long evolutionary period, giving rise to complex relationships. Near one extreme, str-5 and str-6 result from a recent duplication and differ by only two nucleotides in their coding regions. Near the other extreme, the str-1 and str-47 proteins are only 19% identical and presumably arose from an ancient duplication. Members of different SR families are even more distantly related, with the most distant pairs barely alignable.Proteins in the SR superfamily appear to be more rapidly diverging than the average gene (2, 3, 5, 6). For example, the average ortholog pair between C. elegans and Caenorhabditis briggsae has 80% amino acid identity (5), whereas the average str pair from the same data set has 59% identity (J.H.T., unpublished data). Rapidly diverging proteins may result from relaxed selective constraints, in which changes in protein sequence are relatively well tolerated. Alternatively, they may result from selective pressure for changes in amino acid sequence (positive selection or diversifying selection). In extreme cases, positive selection acts on all or most of a protein and can be detected in pairwise d N ͞d S ratio...

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Comparative Genomics and Adaptive Selection of the ATP-Binding-Cassette Gene Family in Caenorhabditis Species

“…For cases in which the additional d N /d S ratio assigned by model 8 was .1, significance was tested by a x 2 test (with 2 d.f.) on twice the negative of the log-likelihood difference between models 7 and 8 (Thomas et al 2005). Specific sites under positive selection were those with probability .0.85 as determined by Bayes Empirical Bayes (BEB) analysis .…”

“…Recently developed codon-based models take into account variations of the ratio among sites (Nielsen and Yang 1998;Yang et al 2000). Detecting adaptive selection has played a critical role in understanding the mechanisms of molecular evolution of different gene families (Thomas et al 2005). ABC proteins are able to transport an unusually broad range of substrates.…”

Adaptive evolution in two large families of ubiquitin-ligase adapters in nematodes and plants

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“…Lack of sufficient population sequence data and the absence of close sibling species eliminate two of the methods used to detect positive selection. However, recent paralogous gene duplicates can be analyzed for evidence of positive selection acting on the paralogs relative to each other (Thomas et al 2005). To apply this method systematically, I clustered the entire gene complement of C. elegans to define 544 paralog groups and analyzed each paralog group for positive selection by the maximum-likelihood method of Yang and Nielsen (Yang 1997;.…”