Yang H et al. (2024) Proc Natl Acad Sci U S A "Glial expression of a steroidogenic enzyme underlies natural variation in hitchhiking behavior."

Cook DE, Kim H, Lee D, Lee J, Andersen EC, Yang H, Paik YK

[Proc Natl Acad Sci U S A, 2024]

Phoresy is an interspecies interaction that facilitates spatial dispersal by attaching to a more mobile species. Hitchhiking species have evolved specific traits for physical contact and successful phoresy, but the regulatory mechanisms involved in such traits and their evolution are largely unexplored. The nematode <i>Caenorhabditis elegans</i> displays a hitchhiking behavior known as nictation during its stress-induced developmental stage. Dauer-specific nictation behavior has an important role in natural <i>C. elegans</i> populations, which experience boom-and-bust population dynamics. In this study, we investigated the nictation behavior of 137 wild <i>C. elegans</i> strains sampled throughout the world. We identified species-wide natural variation in nictation and performed a genome-wide association mapping. We show that the variants in the promoter of <i>nta-1</i>, encoding a putative steroidogenic enzyme, underlie differences in nictation. This difference is due to the changes in <i>nta-1</i> expression in glial cells, which implies that glial steroid metabolism regulates phoretic behavior. Population genetic analysis and geographic distribution patterns suggest that balancing selection maintained two <i>nta-1</i> haplotypes that existed in ancestral <i>C. elegans</i> populations. Our findings contribute to further understanding of the molecular mechanism of species interaction and the maintenance of genetic diversity within natural populations.

Lee D et al. (2019) Nat Ecol Evol "Selection and gene flow shape niche-associated variation in pheromone response."

Kammenga JE, Zdraljevic S, Lee D, Riksen JAG, Wang J, Schroeder FC, Sterken MG, Frezal L, Felix MA, Cook DE, Andersen EC, Braendle C, Hsu JC

[Nat Ecol Evol, 2019]

From quorum sensing in bacteria to pheromone signalling in social insects, chemical communication mediates interactions among individuals in local populations. In Caenorhabditis elegans, ascaroside pheromones can dictate local population density; high levels of pheromones inhibit the reproductive maturation of individuals. Little is known about how natural genetic diversity affects the pheromone responses of individuals from diverse habitats. Here, we show that a niche-associated variation in pheromone receptor genes contributes to natural differences in pheromone responses. We identified putative loss-of-function deletions that impair duplicated pheromone receptor genes (srg-36 and srg-37), which were previously shown to be lost in population-dense laboratory cultures. A common natural deletion in srg-37 arose recently from a single ancestral population that spread throughout the world; this deletion underlies reduced pheromone sensitivity across the global C. elegans population. We found that many local populations harbour individuals with a wild-type or a deletion allele of srg-37, suggesting that balancing selection has maintained the recent variation in this pheromone receptor gene. The two srg-37 genotypes are associated with niche diversity underlying boom-and-bust population dynamics. We hypothesize that human activities likely contributed to the gene flow and balancing selection of srg-37 variation through facilitating the migration of species and providing a favourable niche for the recently arisen srg-37 deletion.

Richaud A et al. (2017) Genetics "The Local Co-existence Pattern of Selfing Genotypes in Caenorhabditis elegans Natural Metapopulations."

Lee J, Zhang G, Felix MA, Richaud A, Lee D

[Genetics, 2017]

To study the interplay of rare outcrossing and metapopulation structure, we focus on the nematode Caenorhabditis elegans Its remarkably low outcrossing rate is at the extreme end of the spectrum for facultative selfing organisms. At the demographic level, C. elegans natural populations undergo boom and bust dynamics on ephemeral resources, the dauer diapause larva acting as the dispersal form. Here we investigate the small-scale genetic structure of C. elegans populations in two localities over several years, using 2b-RAD (Restriction-Associated DNA) sequencing of nearly a thousand individuals. We find a remarkably small number of genome-wide haplotypes, almost exclusively in the homozygous state, confirming the low effective outcrossing rate. Most strikingly, the major haplotypes in a locality remain intact and do not effectively recombine over several years. From the spatial pattern of diversity, we estimate that each subpopulation or deme is seeded by a mean of 3-10 immigrating individuals. Populations are thus formed by clones that compete at two levels, within a subpopulation and at the metapopulation level. We test for the presence of local phenotypic variation in pathogen resistance and dauer larva nictation, which could possibly explain the maintenance of different genotypes by heterogeneous selection in different local environments or life cycles. This study is the first to address the local spatio-temporal genetic structure of C. elegans on feeding substrates. We conclude that these animals coexist as competing homozygous clones at the smallest population scale as well as in the metapopulation.

Piechulek A et al. (2017) Environ Pollut "Life span-resolved nanotoxicology enables identification of age-associated neuromuscular vulnerabilities in the nematode Caenorhabditis elegans."

Piechulek A, von Mikecz A

[Environ Pollut, 2017]

At present, the majority of investigations concerning nanotoxicology in the nematode C.elegans address short-term effects. While this approach allows for the identification of uptake pathways, exposition and acute toxicity, nanoparticle-organism interactions that manifest later in the adult life of C.elegans are missed. Here we show that a microhabitat composed of liquid S-medium and live bacteria in microtiter wells prolongs C.elegans longevity and is optimally suited to monitor chronic eNP-effects over the entire life span (about 34 days) of the nematode. Silver (Ag) nanoparticles reduced C.elegans life span in concentrations 10g/mL, whereas nano ZnO and CeO2 (1-160g/mL) had no effect on longevity. Monitoring of locomotion behaviors throughout the entire life span of C.elegans showed that Ag NPs accelerate the age-associated decline of swimming and increase of uncoordinated movements at concentrations of 10g/mL, whereas neuromuscular defects did not occur in response to ZnO and CeO2 NPs. By means of a fluorescing reporter worm expressing tryptophan hydroxylase-1::DsRed Ag NP-induced behavioral defects were correlated to axonal protein aggregation and neurodegeneration in single serotonergic HSN as well as sensory ADF neurons. Notably, serotonergic ADF neurons represented a sensitive target for Ag NPs in comparison to GABAergic neurons that showed no signs of degeneration under the same conditions. We conclude that due to its analogy to the jellylike boom culture of C.elegans on microbe-rich rotting plant material liquid S-medium culture in spatially confined microtiter wells represents a relevant as well as practical tool for comparative identification of age-resolved nanoparticle effects and vulnerabilities in a significant target organism. Consistent with this, specifically middle-aged nematodes showed premature neuromuscular defects after Ag NP-exposure.

Chapman H et al. (2024) BMC Ecol Evol "Colony level fitness analysis identifies a trade-off between population growth rate and dauer yield in Caenorhabditis elegans."

Rawlinson I, Galimov ER, Chapman H, Hsiung KC, Gems D

[BMC Ecol Evol, 2024]

BACKGROUND: In the evolution from unicellular to multicellular life forms, natural selection favored reduced cell proliferation and even programmed cell death if this increased organismal fitness. Could reduced individual fertility or even programmed organismal death similarly increase the fitness of colonies of closely-related metazoan organisms? This possibility is at least consistent with evolutionary theory, and has been supported by computer modelling. Caenorhabditis elegans has a boom and bust life history, where populations of nematodes that are sometimes&#xa0;near clonal subsist on and consume food patches, and then generate dauer larva dispersal propagules. A recent study of an in silico model of C. elegans predicted that one determinant of colony fitness (measured as dauer yield) is minimization of futile food consumption (i.e. that which does not contribute to dauer yield). One way to achieve this is to optimize colony population structure by adjustment of individual fertility. RESULTS: Here we describe development of a C. elegans colony fitness assay, and its use to investigate the effect of altering population structure on colony fitness after population bust. Fitness metrics measured were speed of dauer production, and dauer yield, an indirect measure of efficiency of resource utilization (i.e. conversion of food into dauers). We find that with increasing founder number, speed of dauer production increases (due to earlier bust) but dauer yield rises and falls. In addition, some dauer recovery was detected soon after the post-colony bust peak of dauer yield, suggesting possible bet hedging among dauers. CONCLUSIONS: These results suggest the presence of a fitness trade-off at colony level between speed and efficiency of resource utilization in C. elegans. They also provide indirect evidence that population structure is a determinant of colony level fitness, potentially by affecting level of futile food consumption.