Fifteen Years of Evolutionary Genomics inCaenorhabditis 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.

Reproductive Mode and the Evolution of Genome Size and Structure in Caenorhabditis Nematodes

“…Within-species polymorphism across Caenorhabditis varies by several orders of magnitude, with selfing species being relatively depauperate of variation [ 16 ] and outcrossing species being among the most polymorphic animals yet observed [ 18 ]. At least one likely reason for these dramatic differences in polymorphism are differences in effective population size among species, which has been estimated as <10,000 in C. elegans [ 48 ], <60,000 in C. briggsae [ 49 ] and >1,000,000 in C. remanei [ 17 ].…”

“…Males capable of mating with the hermaphrodites are also present at low frequencies within these species, but importantly, hermaphrodites are incapable of mating with each other. The genome sizes in Caenorhabditis nematodes are smaller by 20–40% for self-fertile hermaphrodites ( C. elegans , 100.4Mb; C. briggsae , 108Mb; C. tropicalis , 79Mb) than the flow-cytometry estimated genome sizes of the larger N e outcrossers ( C. remanei , 131Mb; C. brenneri , 135Mb; C. japonica , 135Mb)[ 14 – 16 ]. A similar pattern of genome reduction has been observed in multiple self-reproducing plant species as well [ 9 ], which raises the possibility that genome size reduction may be a general syndrome associated with the transition to self reproduction.…”

OUTBREEDING DEPRESSION WITH LOW GENETIC VARIATION IN SELFINGCAENORHABDITISNEMATODES

“…11 is coupled with surprisingly little neutral genetic differentiation among populations inferred from molecular sequence data. More generally, this species has very little nucleotide polymorphism, qualitatively similar to other selfing species ( C. elegans and C. briggsae ) but quantitatively the lowest diversity observed to date for any species of Caenorhabditis (Cutter et al , ; Jovelin et al ). Although differences in mutation rates could contribute to differences in population variation, current estimates of single nucleotide mutation rate do not differ significantly between C. elegans and C. briggsae (Denver et al ).…”

Selfing is the safest sex forCaenorhabditis tropicalis

“…The chromosome-scale genome allows testing of the generality of chromosomal evolution in the Caenorhabditis genus, including a lack of large-scale structural variation that could contribute to outbreeding depression (Cutter et al, 2009;Fierst et al, 2015;Hillier et al, 2007;Jovelin et al, 2013;Kanzaki et al, 2018;Teterina et al, 2020) . To examine patterns of macrosynteny, we established orthology relationships for canonical proteins across the five species (Figure 3).…”