Symmetry breakage in the development of one-armed gonads in nematodes

Whereas the hermaphrodite gonad of Caenorhabditis elegans has two symmetric arms (didelphy), the female/hermaphrodite gonad of many nematode species features a single anterior arm (monodelphy). We examined how gonadal cell lineages and intercellular signalling evolve to generate these diverse structures. In C. elegans, the two arms develop symmetrically from two somatic precursor cells, Z1 (anterior) and Z4 (posterior). Each first gives rise to one distal tip cell (which promotes arm growth and germ line proliferation), two ovary precursors and three uterine precursors in the center of the developing gonad. In monodelphic species, Z1 and Z4 have different fates. The first visible asymmetry between them is in the relative timing of their divisions, followed by asymmetric cell movements. The putative posterior distal tip cell is then eliminated in all but one species by programmed cell death. In some species the posterior ovary precursors form a small vestigial posterior arm, the post-vulval sac; in other species, they stay undivided, or die. In Cephalobus sp. PS1197, the specific fate of Z4 progeny is induced by Z1 (or its daughters). In the uterus in C. elegans, symmetric lateral signalling between Z1.ppp and Z4.aaa renders them equally likely to become the anchor cell, which links the uterus to the vulva. In the different monodelphic species, anchor cell specification is biased, or fully fixed, to a descendant of either Z1 or Z4. Replacement regulation upon anchor cell ablation is conserved in some species, but lost in others, leading to a mosaic-type development. Differentiation between Z1 and Z4 is thus manifested at this later stage in the breakage of symmetry of cell interactions in the ventral uterus

Robustness and evolution: concepts, insights and challenges from a developmental model system.

International audienceRobustness, the persistence of an organismal trait under perturbations, is a ubiquitous property of complex living systems. We here discuss key concepts related to robustness with examples from vulva development in the nematode Caenorhabditis elegans. We emphasize the need to be clear about the perturbations a trait is (or is not) robust to. We discuss two prominent mechanistic causes of robustness, namely redundancy and distributed robustness. We also discuss possible evolutionary causes of robustness, one of which does not involve natural selection. To better understand robustness is of paramount importance for understanding organismal evolution. Part of the reason is that highly robust systems can accumulate cryptic variation that can serve as a source of new adaptations and evolutionary innovations. We point to some key challenges in improving our understanding of robustness.Heredity advance online publication, 13 December 2006; doi:10.1038/sj.hdy.6800915

High local genetic diversity and low outcrossing rate in Caenorhabditis elegans natural populations

Background: Caenorhabditis elegans is a major model system in biology, yet very little is known about its biology outside the laboratory. Especially, its unusual mode of reproduction with self-fertile hermaphrodites and facultative males raises the question of its frequency of outcrossing in natural populations. Results: We describe the first analysis of C. elegans individuals sampled directly from natural populations. C. elegans is found predominantly in the dauer stage and with a very low frequency of males compared with hermaphrodites. While C. elegans was previously shown to display a low worldwide genetic diversity, we find by comparison a surprisingly high local genetic diversity of C. elegans populations; this local diversity is contributed in great part by immigration of new alleles rather than by mutation. Our results on heterozygote frequency, male frequency and linkage disequilibrium furthermore show that selfing is the predominant mode of reproduction in C. elegans natural populations, yet that infrequent outcrossing events occur, at a rate of approximately 1%. Conclusions: Our results give a first insight in the biology of C. elegans in the natural populations. They demonstrate that local populations of C. elegans are genetically diverse and that a low frequency of outcrossing allows for the recombination of these locally diverse genotypes

THE NATURAL HISTORY OF MODEL ORGANISMS C. elegans outside the Petri dish

International audienceThe roundworm Caenorhabditis elegans has risen to the status of a top model organism for biological research in the last fifty years. Among laboratory animals, this tiny nematode is one of the simplest and easiest organisms to handle. And its life outside the laboratory is beginning to be unveiled. Like other model organisms, C. elegans has a boom-and-bust lifestyle. It feasts on ephemeral bacterial blooms in decomposing fruits and stems. After resource depletion, its young larvae enter a migratory diapause stage, called the dauer. Organisms known to be associated with C. elegans include migration vectors (such as snails, slugs and isopods) and pathogens (such as microsporidia, fungi, bacteria and viruses). By deepening our understanding of the natural history of C. elegans, we establish a broader context and improved tools for studying its biology

Plasticity and Errors of a Robust Developmental System in Different Environments

SummaryMany developmental processes generate invariant phenotypes in a wide range of ecological conditions. Such robustness to environmental variation is a fundamental biological property, yet its extent, limits, and adaptive significance have rarely been assessed empirically. Here we tested how environmental variation affects vulval formation in Caenorhabditis nematodes. In different environments, a correct vulval pattern develops with high precision, but rare deviant patterns reveal the system's limits and how its mechanisms respond to environmental challenges. Key features of the apparent robustness are functional redundancy among vulval precursor cells and tolerance to quantitative variation in Ras, Notch, and Wnt pathway activities. The observed environmental responses and precision of vulval patterning vary within and between Caenorhabditis species. These results highlight the complex response of developmental systems to the environment and illustrate how a robust and invariant phenotype may result through cellular and molecular processes that are highly plastic—across environments and evolution

Temporal Dynamics and Linkage Disequilibrium in Natural C. elegans Populations.

International audienceCaenorhabditis elegans is a major laboratory model system yet a newcomer to the field of population genetics, and relatively little is known of its biology in the wild. Recent studies of natural populations at a single timepoint revealed strong spatial population structure and suggested that these populations may be very dynamic. We have therefore studied several natural C. elegans populations over time and genotyped them at polymorphic microsatellite loci. While some populations appear to be genetically stable over the course of observation, others seem to go extinct, with full replacement of multilocus genotypes upon population regrowth. The frequency of heterozygotes indicates that outcrossing occurs at a mean frequency of 1.7% and is variable between populations. However, in genetically stable populations, linkage disequilibrium between different chromosomes can be maintained over several years, at a level much higher than expected from the heterozygote frequency. C. elegans seems to follow metapopulation dynamics, and the maintenance of linkage disequilibrium despite a low yet significant level of outcrossing suggests that selection may act against the progeny of outcrossings

Sex Determination: Ways to Evolve a Hermaphrodite

Most species of the nematode genus Caenorhabditis reproduce through males and females; C. elegans and C. briggsae, however, produce self-fertile hermaphrodites instead of females. These transitions to hermaphroditism evolved convergently through distinct modifications of germline sex determination mechanisms

Noda-like RNA viruses infecting Caenorhabditis nematodes: Sympatry, diversity, and reassortment

Three RNA viruses related to nodaviruses were previously described to naturally infect the nematod

Control of Vulval Cell Division Number in the Nematode Oscheius/Dolichorhabditis sp. CEW1

Spatial patterning of vulval precursor cell fates is achieved through a different two-stage induction mechanism in the nematode Oscheius/Dolichorhabditis sp. CEW1 compared with Caenorhabditis elegans. We therefore performed a genetic screen for vulva mutants in Oscheius sp. CEW1. Most mutants display phenotypes unknown in C. elegans. Here we present the largest mutant category, which affects division number of the vulva precursors P(4-8).p without changing their fate. Among these mutations, some reduce the number of divisions of P4.p and P8.p specifically. Two mutants omit the second cell cycle of all vulval lineages. A large subset of mutants undergo additional rounds of vulval divisions. We also found precocious and retarded heterochronic mutants. Whereas the C. elegans vulval lineage mutants can be interpreted as overall (homeotic) changes in precursor cell fates with concomitant cell cycle changes, the mutants described in Oscheius sp. CEW1 do not affect overall precursor fate and thereby dissociate the genetic mechanisms controlling vulval cell cycle and fate. Laser ablation experiments in these mutants reveal that the two first vulval divisions in Oscheius sp. CEW1 appear to be redundantly controlled by a gonad-independent mechanism and by a gonadal signal that operates partially independently of vulval fate induction