Fifteen Years of Evolutionary Genomics in Caenorhabditis elegans

Abstract

The nematode worm Caenorhabditis elegans, introduced by Sydney Brenner for the genetic analysis of nervous system formation, is now a powerful model organism for studying nearly all aspects of biology, from development to diseases to evolution. Sequencing and analysis of the worm genome revealed intriguing nonrandom patterns of genome organisation and unusual features such as abundant operons. Surprising upon first discovery, worms and humans have a similar number of genes that are comprised of a similar proportion of transcription factors to regulate their genomes. However, differences in small ribonucleic acid content may contribute to differences in organismal complexity. In nature, the bacterivorous C. elegans is found primarily on rotting vegetation in temperate regions across the world. Natural selection, combined with the low effective recombination rate associated with selfing, strongly reduces nucleotide variation across the genome, yielding similarly low polymorphism to other selfing hermaphrodite species of Caenorhabditis. The genus Caenorhabditis provides a superb model system for ecological and evolutionary genetics, benefiting from C. elegans tools and information when applied to investigations of species with a higher polymorphism and better known ecological context.

Key Concepts:

  • The nematode Caenorhabditis elegans, introduced by Sydney Brenner for the genetic analysis of nervous system development, was the first metazoan to have a complete sequenced genome and is now a model organism for nearly all fields of biology.

  • Many genomic features are not randomly distributed along C. elegans chromosomes and are prevalent either in the chromosome arms or in its centre.

  • An unusually large fraction of protein‐coding genes is organised in operons, possibly optimising transcriptional resources during recovery from developmental arrest.

  • Gene duplication and alternative splicing contribute to extensive diversification of gene function, with 10.5% of protein‐coding genes having paralogs and 25% of genes being alternatively spliced.

  • The ratio of transcription factors to protein‐coding genes is similar in worms and humans but the two species differ greatly in their microRNA content.

  • The differences in chromatin states contribute to phenotypic variation and the transgenerational epigenetic inheritance suggests a role for epigenetic information in evolution.

  • The rate of duplication is two orders of magnitude greater than the nucleotide mutation rate, highlighting the role of gene duplication in the evolution of the C. elegans genome.

  • Caenorhabditis is not a soil nematode but instead proliferates and feeds on bacteria in rotting vegetation.

  • Population genetic variation is strongly affected by the mating system of Caenorhabditis, with very low polymorphism in selfing hermaphroditic species relative to outcrossing gonochoristic species.

Keywords: Caenorhabditis; genome evolution; operons; gene regulation; mating systems; epigenetics; polymorphism

Figure 1.

Nonrandom patterns in the organisation of the C. elegans genome. Chromosomes are typically partitioned into arms (yellow) and centres (blue) that differ by the relative distribution of several genomic features. Each domain makes ∼30% of the chromosome length, although arms are asymmetric relative to centre and the position of centres varies among chromosomes. Here, features are mapped to a chromosome domain (grey line), arm or centre, when their abundance in this domain is greater than on the other domain. For instance, protein‐coding genes are preferentially distributed in chromosome centres and recombination occurs more frequently in chromosome arms. Note that the distribution of genomic features in the arms does not differentiate between left and right ends (see Cutter et al., and references therein; Gerstein et al., ).

Figure 2.

The base substitution rate (per nucleotide and per generation) is similar within and between C. elegans and C. briggsae for the mitochondrial genome (a) and the nuclear genome (b). In both species the mitochondrial mutation rate is 100‐fold larger than the nuclear mutation rate (note the scale difference of the y‐axis in (a) and (b)). Means are represented with ±1 standard error of the mean, in red for C. briggsae (Cbr) and in yellow for C. elegans (Cel). Data for the mutation rate in the mitochondrial genome of C. elegans is from Denver et al. () and from Howe et al. () for C. briggsae. In (b), the mutation rate for each C. elegans and C. briggsaeMA lines (Denver et al., ) is also pooled to obtain an average estimate for each species.

Figure 3.

A selfing mode of reproduction has evolved independently three times (in red) from a gonochoristic ancestor in the genus Caenorhabditis (left). The level of nucleotide variation is strongly affected by the mating type and is greater in gonochoristic outcrossing Caenorhabditis species (blue) than in hermaphroditic selfing species (yellow) (right). The average level of neutral site diversity (at silent or synonymous sites) is plotted for each species. Error bars indicate the standard error of the mean with values smaller than the symbol size not shown. Updated from Cutter et al. with data for C. briggsae (Félix et al., ), Caenorhabditis sp. 23 (Dey et al., ), and Caenorhabditis sp. 11 (Gimond et al., personal communication). The 5% threshold identifies hyperdiverse species (Cutter et al., ).

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Further Reading

Cutter AD, Jovelin R and Dey A (2013) Molecular hyperdiversity and evolution in very large populations. Molecular Ecology. doi:10.1111/mec.12281.

Felix MA and Braendle C (2010) The natural history of Caenorhabditis elegans. Current Biology 20: R965–R969.

Gaertner BE and Phillips PC (2010) Caenorhabditis elegans as a platform for molecular quantitative genetics and systems biology of natural variation. Genetical Research 92: 331–348.

Wenzel D, Palladino F and Jedrusik‐Bode M (2011) Epigenetics in C. elegans: facts and challenges. Genesis 49: 647–661.

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Jovelin, Richard, Dey, Alivia, and Cutter, Asher D(May 2013) Fifteen Years of Evolutionary Genomics in Caenorhabditis elegans. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0022897]