Mainstreaming<i>Caenorhabditis elegans</i>in experimental evolution

Gray, Jeremy C.; Cutter, Asher D.

doi:10.1098/rspb.2013.3055

Cited by 59 publications

(73 citation statements)

References 108 publications

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“…Microbial systems are very convenient due to their genetic tractability and short generation times but are limited in the space of behavioral traits they exhibit. At the other extreme, higher organisms exhibit rich neurobehavioral and genetic traits, but they are difficult to experimentally manipulate and generation times are very long.Recently, organisms such as the nematode worm Caenorhabditis elegans and the fruit fly Drosophila melanogaster have been increasingly used in evolutionary and behavioral studies (17)(18)(19)). These organisms demonstrate complex behavior and yet retain experimental tractability due to their extensive development as model systems in neurobiology and genetics.…”

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confidence: 99%

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Farming and public goods production in Caenorhabditis elegans populations

Thutupalli

Uppaluri

Constable

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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The ecological and evolutionary dynamics of populations are shaped by the strategies they use to produce and use resources. However, our understanding of the interplay between the genetic, behavioral, and environmental factors driving these strategies is limited. Here, we report on a Caenorhabditis elegansEscherichia coli (worm-bacteria) experimental system in which the worm-foraging behavior leads to a redistribution of the bacterial food source, resulting in a growth advantage for both organisms, similar to that achieved via farming. We show experimentally and theoretically that the increased resource growth represents a public good that can benefit all other consumers, regardless of whether or not they are producers. Mutant worms that cannot farm bacteria benefit from farming by other worms in direct proportion to the fraction of farmers in the worm population. The farming behavior can therefore be exploited if it is associated with either energetic or survival costs. However, when the individuals compete for resources with their own type, these costs can result in an increased population density. Altogether, our findings reveal a previously unrecognized mechanism of public good production resulting from the foraging behavior of C. elegans, which has important population-level consequences. This powerful system may provide broad insight into explorationexploitation tradeoffs, the resultant ecoevolutionary dynamics, and the underlying genetic and neurobehavioral driving forces of multispecies interactions.foraging behavior | public goods | predator-prey | population dynamics | farming T he fitness of an organism is affected by its strategies to produce, explore, and exploit resources (1, 2). These strategies are influenced, in large part, by interdependencies among organisms, such as competition, predation (3, 4), mutualism (5-7), or the production of public good resources (8-10). Despite the wide prevalence of such interactions in nature as well as numerous theoretical and empirical studies, we are still limited in our mechanistic understanding of the interplay between different survival strategies, the resultant evolutionary dynamics and the underlying genetic, neurobehavioral, and ecological driving forces. In this pursuit, model systems in the laboratory have served as a useful bridge between the complexity of nature and the simplifications inherent in theoretical investigations. Such model systems have predominantly been either microbial (11, 12) or higher organisms, such as primates and humans (13-16). Microbial systems are very convenient due to their genetic tractability and short generation times but are limited in the space of behavioral traits they exhibit. At the other extreme, higher organisms exhibit rich neurobehavioral and genetic traits, but they are difficult to experimentally manipulate and generation times are very long.Recently, organisms such as the nematode worm Caenorhabditis elegans and the fruit fly Drosophila melanogaster have been increasingly used in evolutionary and behavioral stu...

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confidence: 99%

“…Recently, organisms such as the nematode worm Caenorhabditis elegans and the fruit fly Drosophila melanogaster have been increasingly used in evolutionary and behavioral studies (17)(18)(19)). These organisms demonstrate complex behavior and yet retain experimental tractability due to their extensive development as model systems in neurobiology and genetics.…”

mentioning

confidence: 99%

Farming and public goods production in Caenorhabditis elegans populations

Thutupalli

Uppaluri

Constable

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…Many of the studies investigating the problem of male maintenance associated with the existence of outcrossing have used Caenorhabditis elegans, a common model species in evolutionary and genetic research (Gray and Cutter 2014). C. elegans is androdioecious, with hermaphrodites coexisting with males.…”

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Fitness effects of thermal stress differ between outcrossing and selfing populations inCaenorhabditis elegans

Plesnar‐Bielak

Labocha

Kosztyła

et al. 2016

Preprint

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The maintenance of males and outcrossing is widespread, despite considerable costs of males. By enabling recombination between distinct genotypes, outcrossing may be advantageous during adaptation to a novel environments and if so, it should be selected for under environmental challenge. However, a given environmental change may influence fitness of male, female, and hermaphrodite or asexual individuals differently, and hence the relationship between reproductive system and dynamics of adaptation to novel conditions may not be driven solely by the level of outcrossing and recombination. This has important implications for studies investigating the evolution of reproductive modes in the context of environmental changes, and for the extent to which their findings can be generalized. Here, we use Caenorhabditis elegans – a free-living nematode species in which hermaphrodites (capable of selfing but not cross-fertilizing each other) coexist with males (capable of fertilizing hermaphrodites) – to investigate the response of wild type as well as obligatorily outcrossing and obligatorily selfing lines to stressfully increased ambient temperature. We found that thermal stress affects fitness of outcrossers much more drastically than that of selfers. This shows that apart from the potential for recombination, the selective pressures imposed by the same environmental change can differ between populations expressing different reproductive systems and affect their adaptive potential.

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“…The microscopic Caenorhabditis elegans nematode is an excellent eukaryotic model for studying molecular-genetic and phenotypic evolution (Gray and Cutter 2014). There are several aspects of C. elegans'…”

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confidence: 99%

“…It is also relatively easy to cross C. elegans-using males and hermaphrodites-to generate isogenic strains with different mutations that confer experimentally useful phenotypes (Hope 1999). Additionally, C. elegans nematodes are highly tractable in laboratory environments and a diverse array of experiments can be performed on them (Hope 1999;Riddle et al 1997;Hope 1999;Gray and Cutter 2014).…”

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confidence: 99%

Adaptive Evolution under Favorable and Unfavorable Population Genetic Conditions in Mitochondrial-deficient Caenorhabditis Elegans Nematodes

Christy¹

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Mutation is a fundamental process that drives evolutionary change; however, most new mutations are deleterious for organismal fitness and can readily propagate within populations under a broad range of conditions. Mutational processes able to counteract deleterious mutation accumulation include: 1) reversion mutation back to wildtype, 2) acquisition of generally beneficial mutations, and 3) compensatory mutations that specifically mitigate the effects of previously-acquired deleterious mutations through epistasis. The potential for any of these mutation types alters our expectations for the impact of deleterious mutation in populations, but since the fitness effects of individual mutations are rarely characterized, the relative importance of beneficial and compensatory epistatic mutations is unknown. In this thesis, I characterized the nuclear mutations that arose in a previous mutation accumulation (MA) experiment using Caenorhabditis elegans nematodes, in which mutations were allowed to accumulate under extreme drift conditions in replicate, independently evolving lines initiated from a low-fitness mitochondrial electron transport chain (ETC) mutant, gas-1. In contrast to the results of typical MA experiments, gas-1 MA lines improved fitness slightly compared to their ancestor. Here, I find that the gas-1 MA lines demonstrate little increase in amongline variance and that the gas-1 MA nuclear mutations are more narrowly functionally defined than wildtype MA nuclear mutations. When combined with evidence for zygotic or post zygotic selection these data suggest that selection-both purifying and positivecan be an extremely powerful force even in conditions of extreme genetic drift.Furthermore, functional characterization of a four-mutation set isolated from one of the ii gas-1 MA lines on gas-1 and wildtype backgrounds shows fitness improvements on both backgrounds. This beneficial four-mutation set is associated with a decrease in steady-

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MainstreamingCaenorhabditis elegansin experimental evolution

Cited by 59 publications

References 108 publications

Farming and public goods production in Caenorhabditis elegans populations

Farming and public goods production in Caenorhabditis elegans populations

Fitness effects of thermal stress differ between outcrossing and selfing populations inCaenorhabditis elegans

Adaptive Evolution under Favorable and Unfavorable Population Genetic Conditions in Mitochondrial-deficient Caenorhabditis Elegans Nematodes

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