4.4 Article

Experimental Evolution with Caenorhabditis Nematodes

Journal

GENETICS
Volume 206, Issue 2, Pages 691-716

Publisher

GENETICS SOCIETY AMERICA
DOI: 10.1534/genetics.115.186288

Keywords

adaptation; C. briggsae; C. elegans; C. remanei; domestication; experimental design; laboratory selection experiments; self-fertilization; reproduction systems; mutation accumulation; standing genetic variation; WormBook

Funding

  1. European Research Council [FP7/2007-2013/243285]
  2. Human Frontiers Science Program [RGP0045/2010]
  3. Agence Nationale de la Recherche [ANR-14-ACHN-0032-01]
  4. National Science Foundation [MCB-1330427]
  5. National Institutes of Health [R01GM102511, R01AG049396, R01GM107227]

Ask authors/readers for more resources

The hermaphroditic nematode Caenorhabditis elegans has been one of the primary model systems in biology since the 1970s, but only within the last two decades has this nematode also become a useful model for experimental evolution. Here, we outline the goals and major foci of experimental evolution with C. elegans and related species, such as C. briggsae and C. remanei, by discussing the principles of experimental design, and highlighting the strengths and limitations of Caenorhabditis as model systems. We then review three exemplars of Caenorhabditis experimental evolution studies, underlining representative evolution experiments that have addressed the: (1) maintenance of genetic variation; (2) role of natural selection during transitions from outcrossing to selfing, as well as the maintenance of mixed breeding modes during evolution; and (3) evolution of phenotypic plasticity and its role in adaptation to variable environments, including host-pathogen coevolution. We conclude by suggesting some future directions for which experimental evolution with Caenorhabditis would be particularly informative.

Authors

I am an author on this paper
Click your name to claim this paper and add it to your profile.

Reviews

Primary Rating

4.4
Not enough ratings

Secondary Ratings

Novelty
-
Significance
-
Scientific rigor
-
Rate this paper

Recommended

Article Multidisciplinary Sciences

The genomic basis of Red Queen dynamics during rapid reciprocal host-pathogen coevolution

Andrei Papkou, Thiago Guzella, Wentao Yang, Svenja Koepper, Barbara Pees, Rebecca Schalkowski, Mike-Christoph Barg, Philip C. Rosenstiel, Henrique Teotonio, Hinrich Schulenburg

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2019)

Article Evolutionary Biology

A large close relative of C. elegans is slow-developing but not long-lived

Gavin C. Woodruff, Erik Johnson, Patrick C. Phillips

BMC EVOLUTIONARY BIOLOGY (2019)

Article Multidisciplinary Sciences

The Stress-Chip: A microfluidic platform for stress analysis in Caenorhabditis elegans

Stephen A. Banse, Benjamin W. Blue, Kristin J. Robinson, Cody M. Jarrett, Patrick C. Phillips

PLOS ONE (2019)

Article Genetics & Heredity

Partial Selfing Can Reduce Genetic Loads While Maintaining Diversity During Experimental Evolution

Ivo M. Chelo, Bruno Afonso, Sara Carvalho, Ioannis Theologidis, Christine Goy, Ania Pino-Querido, Stephen R. Proulx, Henrique Teotonio

G3-GENES GENOMES GENETICS (2019)

Article Genetics & Heredity

Limits to Genomic Divergence Under Sexually Antagonistic Selection

Katja R. Kasimatis, Peter L. Ralph, Patrick C. Phillips

G3-GENES GENOMES GENETICS (2019)

Article Genetics & Heredity

Males, Outcrossing, and Sexual Selection in Caenorhabditis Nematodes

Asher D. Cutter, Levi T. Morran, Patrick C. Phillips

GENETICS (2019)

Article Genetics & Heredity

Chromosome-Level Assembly of the Caenorhabditis remanei Genome Reveals Conserved Patterns of Nematode Genome Organization

Anastasia A. Teterina, John H. Willis, Patrick C. Phillips

GENETICS (2020)

Article Genetics & Heredity

Rapid Self-Selecting and Clone-Free Integration of Transgenes into Engineered CRISPR Safe Harbor Locations inCaenorhabditis elegans

Zachary C. Stevenson, Megan J. Moerdyk-Schauwecker, Brennen Jamison, Patrick C. Phillips

G3-GENES GENOMES GENETICS (2020)

Article Genetics & Heredity

Complex pleiotropic genetic architecture of evolved heat stress and oxidative stress resistance in the nematode Caenorhabditis remanei

Christine H. O'Connor, Kristin L. Sikkink, Thomas C. Nelson, Janna L. Fierst, William A. Cresko, Patrick C. Phillips

Summary: The study used experimental evolution to dissect the genetic architecture of acute heat stress and oxidative stress response in the nematode C. remanei, finding that these traits are polygenic and complex, involving hundreds of genomic regions. Contrary to expectation, the genetic bases of acute heat stress and oxidative stress response in C. remanei appear to be largely independent, suggesting that rapid adaptation can be generated by changes at multiple sites in the genome.

G3-GENES GENOMES GENETICS (2021)

Article Ecology

Testing the adaptive value of sporulation in budding yeast using experimental evolution

Kelly M. Thomasson, Alexander Franks, Henrique Teotonio, Stephen R. Proulx

Summary: Saccharomyces yeast undergoes sporulation in response to starvation, producing haploid cells enclosed in a protective ascus. Passage through insect guts selects for increased spore production, with wild-derived strains showing a more rapid and extreme shift towards sporulation. Domesticated strains exhibit a weaker response, suggesting genetic canalization of the sporulation initiation response.

EVOLUTION (2021)

Article Genetics & Heredity

Post-insemination selection dominates pre-insemination selection in driving rapid evolution of male competitive ability

Katja R. Kasimatis, Megan J. Moerdyk-Schauwecker, Ruben Lancaster, Alexander Smith, John H. Willis, Patrick C. Phillips

Summary: Sexual reproduction is a complex process that contributes to differences between the sexes and divergence between species. This study investigates the role of pre- and post-insemination sexual selection in the evolution of male reproductive success using an experimental evolution approach. The results show that enhanced post-insemination competition is more effective than pre-insemination competition in driving the evolution of male reproductive success. Surprisingly, enhanced pre-insemination competition hinders selection and slows down the rate of evolution. Post-insemination selection leads to a strong polygenic response at the whole-genome level.

PLOS GENETICS (2022)

Article Genetics & Heredity

Selection on modifiers of genetic architecture under migration load

Stephen R. Proulx, Henrique Teotonio

Summary: Gene flow between populations adapting to different environmental conditions might have costs, and the selection on modifiers of genetic architecture depends on different genetic mechanisms.

PLOS GENETICS (2022)

Article Genetics & Heredity

Variation in mutational (co)variances

Francois Mallard, Luke Noble, Charles F. Baer, Henrique Teotonio

Summary: Due to pleiotropy, mutations affect multiple traits, making it important to investigate variations in the mutational M matrix between genotypes. This study estimated the M matrix for locomotion behavior traits in two genotypes of C. elegans. There were significant mutational variances, but no detectable differences in size or orientation between genotypes. Furthermore, the M matrix differed from the G matrix, indicating that selection does not shape the M matrix in the short-term and suggesting that hybridization of C. elegans genotypes allows selection on new phenotypic dimensions.

G3-GENES GENOMES GENETICS (2023)

Article Biology

High-throughput library transgenesis in Caenorhabditis elegans via Transgenic Arrays Resulting in Diversity of Integrated Sequences (TARDIS)

Zachary C. Stevenson, Megan J. Moerdyk-Schauwecker, Stephen A. Banse, Dhaval S. Patel, Hang Lu, Patrick C. Phillips

Summary: High-throughput transgenesis using synthetic DNA libraries is a powerful method for exploring genetic function. However, the need for library transgenesis has restricted its application to single-cell models. In this study, we present TARDIS, a method that overcomes these limitations and enables large-scale transgenesis in multicellular systems. We demonstrate its utility in Caenorhabditis elegans and show that transformation yields can be increased up to approximately 1000-fold compared to current methods.

ELIFE (2023)

Article Genetics & Heredity

Evaluating human autosomal loci for sexually antagonistic viability selection in two large biobanks

Katja R. Kasimatis, Abin Abraham, Peter L. Ralph, Andrew D. Kern, John A. Capra, Patrick C. Phillips

Summary: Sex and sexual differentiation are common in various species, leading to different selection pressures between sexes. However, studies on autosomal loci in humans did not find clear evidence of sexually antagonistic viability selection, possibly due to cross-hybridization with sex chromosome regions at these loci.

GENETICS (2021)

No Data Available