Evolution with a seed bank: The population genetic consequences of microbial dormancy

Shoemaker, William R.; Lennon, Jay T.

doi:10.1111/eva.12557

Cited by 101 publications

(137 citation statements)

References 177 publications

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“…Furthermore, it has been shown that the distribution of activity among a population of starving microorganisms may be highly negatively skewed (i.e., a small number of cells utilizing a large proportion of total energy) (Shoemaker & Lennon, 2017). It is likely, therefore, that simulated POC degradation rates exceed the actual POC degradation rates over this interval, and thus, by extension, simulated microbial maintenance activity is too high.…”

Section: Model Resultsmentioning

confidence: 99%

Survival of the fewest: Microbial dormancy and maintenance in marine sediments through deep time

2018

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Microorganisms buried in marine sediments are known to endure starvation over geologic timescales. However, the mechanisms of how these microorganisms cope with prolonged energy limitation is unknown and therefore yet to be captured in a quantitative framework. Here, we present a novel mathematical model that considers (a) the physiological transitions between the active and dormant states of microorganisms, (b) the varying requirement for maintenance power between these phases, and (c) flexibility in the provenance (i.e., source) of energy from exogenous and endogenous catabolism. The model is applied to sediments underlying the oligotrophic South Pacific Gyre where microorganisms endure ultra‐low fluxes of energy for tens of millions of years. Good fits between model simulations and measurements of cellular carbon and organic carbon concentrations are obtained and are interpreted as follows: (a) the unfavourable microbial habitat in South Pacific Gyre sediments triggers rapid mortality and a transition to dormancy; (b) there is minimal biomass growth, and organic carbon consumption is dominated by catabolism to support maintenance activities rather than new biomass synthesis; (c) the amount of organic carbon that microorganisms consume for maintenance activities is equivalent to approximately 2% of their carbon biomass per year; and (d) microorganisms must rely solely on exogenous rather than endogenous catabolism to persist in South Pacific Gyre sediments over long timescales. This leads us to the conclusion that under oligotrophic conditions, the fitness of an organism is determined by its ability to simply stay alive, rather than to grow. This modelling framework is designed to be flexible for application to other sites and habitats, and thus serves as a new quantitative tool for determining the habitability of and an ultimate limit for life in any environment.

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Section: Model Resultsmentioning

confidence: 99%

Survival of the fewest: Microbial dormancy and maintenance in marine sediments through deep time

2018

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“…Seed banks also store genetic diversity that provides a source of gene flow from the 310 past (Hairston and Kearns 2002;Vitalis et al 2004;Lundemo et al 2009;Rubio de Casas et al 2015). Maladaptive gene flow from the seed bank can inhibit monopolization by slowing the 312 response to directional selection (Templeton and Levin 1979;Hairston and De Stasio 1988;Shoemaker and Lennon 2018;Tellier 2019), a process we call the 'dormancy load'. 314…”

Section: Evolving Metacommunities With Dormancymentioning

confidence: 99%

Dormancy in metacommunities

Wisnoski¹,

Leibold²,

Lennon³

2018

Preprint

Self Cite

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Although metacommunity ecology has improved our understanding of how dispersal 16 affects community structure and dynamics across spatial scales, it has yet to adequately account for dormancy. Dormancy is a reversible state of reduced metabolic activity that enables temporal 18 dispersal within the metacommunity. Dormancy is also a metacommunity-level process because it can covary with spatial dispersal and affect diversity across spatial scales. We develop a 20 framework to integrate dispersal and dormancy, focusing on the covariation they exhibit, to predict how dormancy modifies the importance of species interactions, dispersal, and historical 22 contingencies in metacommunities. We examine case studies of microcrustaceans in ephemeral ponds, where dormancy is integral to metacommunity dynamics. We analyze traits of bromeliad-24 dwelling invertebrates and identify constraints on dispersal and dormancy strategies. Using simulations, we demonstrate that dormancy can alter classic metacommunity patterns of diversity 26 in ways that depend on dispersal-dormancy covariation and spatiotemporal environmental variability. We propose that dormancy may also facilitate evolution-mediated priority effects if 28 locally adapted seed banks prevent colonization by more dispersal-limited species. We present theoretically and empirically testable predictions for other possible ecological and evolutionary 30 implications of dormancy in metacommunities, some of which may fundamentally alter our understanding of metacommunity ecology.

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“…The above predictions also apply to micro‐organisms (bacteria or fungi) with persistent dormant stages found in soil or in plant microbiomes, albeit with even stronger signatures (e.g. Shoemaker & Lennon, ). The set of current predictions could promote the inter‐disciplinary study of persistent seed banking as a key eco‐evolutionary factor using population genomics, ecology, plant physiology and molecular biology.…”

Section: Resultsmentioning

confidence: 88%

Persistent seed banking as eco‐evolutionary determinant of plant nucleotide diversity: novel population genetics insights

Tellier

2018

New Phytologist

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Contents Summary725I.Introduction725II.Seed banks decrease the population extinction rate726III.Seed banks define the effective population size727IV.Seed banks affect the mutation rate728V.Seed banks affect the effective recombination rate728VI.Seed banks influence the rate and signatures of natural selection729VII.Conclusion729Acknowledgements729References729 Summary Long‐term persistent seed banking is a common temporal bet‐hedging strategy in plants to adapt to unpredictable environments. The population genomics perspective developed in this article suggests that seed banking determines plant nucleotide diversity by decreasing the rate of genetic drift and the effect of linked selection while increasing mutational input. As a result, persistent seed banks are important factors determining the magnitude of the discrepancy between the census size of the above‐ground plant population and its genetic diversity, an effect known as the Lewontin paradox. The theoretical population genetics predictions presented here can be tested by combining genome‐wide polymorphism data with ecological studies of dormancy.

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Evolution with a seed bank: The population genetic consequences of microbial dormancy

Cited by 101 publications

References 177 publications

Survival of the fewest: Microbial dormancy and maintenance in marine sediments through deep time

Survival of the fewest: Microbial dormancy and maintenance in marine sediments through deep time

Dormancy in metacommunities

Persistent seed banking as eco‐evolutionary determinant of plant nucleotide diversity: novel population genetics insights

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