Caenorhabditis phylogeny predicts convergence of hermaphroditism and extensive intron loss

Abstract

Despite the prominence of Caenorhabditis elegans as a major developmental and genetic model system, its phylogenetic relationship to its closest relatives has not been resolved. Resolution of these relationships is necessary for studying the steps that underlie life history, genomic, and morphological evolution of this important system. By using data from five different nuclear genes from 10 Caenorhabditis species currently in culture, we find a well resolved phylogeny that reveals three striking patterns in the evolution of this animal group: (i) Hermaphroditism has evolved independently in C. elegans and its close relative Caenorhabditis briggsae; (ii) there is a large degree of intron turnover within Caenorhabditis, and intron losses are much more frequent than intron gains; and (iii) despite the lack of marked morphological diversity, more genetic disparity is present within this one genus than has occurred within all vertebrates.C aenorhabditis elegans is an important model system that allows great depth of study into how the genome is translated into a developing, functioning animal (1). To generalize from this model, a phylogenetic context and information about related species are essential. The genome of a close relative, Caenorhabditis briggsae, was recently sequenced, providing an important comparative genomics tool for annotating the C. elegans genome (2). However, genome comparisons for multiple species that are closely related can provide substantially more analytical power, as demonstrated recently by genome comparisons among several closely related yeast species (3). A well resolved phylogeny for closely related species provides the basis for selecting appropriate representatives for such comparisons, for distinguishing orthologous from paralogous genes, and for distinguishing ancestral versus derived states for characters (4).Comparisons among phylogenetically closely related species, as opposed to comparisons among distantly related groups, are more likely to reveal finer detail about the steps that underlie life history, genomic, and morphological evolution. For example, in the absence of a phylogeny that includes additional closely related species, a feature that is actually convergent between two species may appear to be homologous, as we show below for the case of hermaphroditic reproduction. Also, the time and the frequency at which evolutionary events occurred, like the loss and gain of introns, may be obscured by comparing distantly related species or anciently duplicated genes. We therefore aimed to resolve the phylogenetic relationships of all Caenorhabditis species currently in culture by using gene sequence data.Previous analyses with morphological (5) and small subunit (SSU) rRNA gene data (6) supported a monophyletic group called the Elegans group, consisting of C. elegans, C. briggsae, Caenorhabditis remanei, and an undescribed Caenorhabditis species (strain CB5161). However, the relationships of the Elegans group species to each other remained unresolved in these studies. Other mo...

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

“…Of the 53 ABC orthologous trios among the three nematode species, 39 C. briggsae and C. remanei ABC genes cluster with each other with the C. elegans ABC gene as an outgroup (Figure 1; supplemental Figure 1 at http://www.genetics.org/supplemental/), implying that C. briggsae and C. remanei are more related to each other than to C. elegans. This result is consistent with the recently resolved Caenorhabditis phylogeny using five different nuclear genes from 10 species (Kiontke et al 2004) as well as other studies that used genes only from the same three species used here (Haag et al 2002;Rudel and Kimble 2002). Further evidence came from comparison of the intron evolution of Y39E4B.1, an extremely conserved ABC gene and the single member of the ABCE subfamily.…”

“…In agreement with this, exon/intron structures of the highly conserved ABCE proteins are more similar to each other between C. remanei and C. briggse than between either of the species and C. elegans, suggesting a closer relationship between C. briggsae and C. remanei than between either of the species and C. elegans. This agrees well with what has been reported (Kiontke et al 2004), suggesting that the evolution pattern of ABC genes can provide useful insight for phylogeny. Divergence of ABC genes between nematode species: Despite frequent one-to-one orthology among the three nematode species, varying patterns of divergence among ABC genes are apparent.…”

“…In contrast, C. elegans Y39E4B.1 has five exons and four introns (Figure 3). Given relatively frequent intron loss within the nematode species (Kiontke et al 2004), it is possible that Y39E4B.1 lost an intron in exon 3 because its size is equal to the combined sizes of exon 3 and 4 of brjY39E4B.1 or rmjY39E4B.1. In addition, the sizes of the remaining exons are also different between C. elegans and C. briggsae/C.…”

Conspecific and Interspecific Interactions Between the FEM-2 and the FEM-3 Sex-Determining Proteins Despite Rapid Sequence Divergence

“…One possibility, which we have discussed previously (Stothard et al 2002), is that the TRA-2/TRA-1 is used instead of the FEM complex in the germline of C. briggsae and C. remanei. Since the phylogenetic relationships of these three species suggest that hermaphroditism evolved independently in C. elegans and C. briggsae (Kiontke et al 2004), parsimony suggests that a role for the FEM proteins in germline sex determination may be a derived trait in C. elegans. Such a modification could be imagined to occur as a consequence of the same selective forces that led to the rapid protein coevolution.…”

“…We and others have begun to compare the C. elegans sex-determination pathway with the pathways that regulate sex in other nematode species such as C. briggsae and C. remanei (Stothard and Pilgrim 2003;Nayak et al 2005;Cutter and Ward 2005). Recent phylogenies for the various Caenorhabditis species have concluded that C. briggsae and C. elegans, which are both hermaphrodite/male species, diverged independently from gonochoristic (male/female) ancestors, and most of the closely related species, such as C. remanei, have retained that sex determining mechanism (Kiontke et al 2004;Cho et al 2004). This implies that the changes that led to hermaphroditism also evolved independently in C. elegans and C. briggsae, and may involve different regulatory controls.…”