Holobionts as Units of Selection and a Model of Their Population Dynamics and Evolution

Roughgarden, Joan; Gilbert, Scott F.; Rosenberg, Eugene; Zilber‐Rosenberg, Ilana; Lloyd, Elisabeth A.

doi:10.1007/s13752-017-0287-1

Cited by 158 publications

(172 citation statements)

References 202 publications

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“…This can be achieved in several ways, such as the selection of existing individuals from heat-exposed habitats and relocating breeding populations into degraded habitats (Morikawa & Palumbi, 2019). Other approaches include conventional cross-breeding of strains or species to create hybrids likely to be vigorous under future environmental conditions (van Oppen et al, 2015), and the optimization of symbiotic relationships to select for resistant holobionts (see review by Roughgarden, Gilbert, Rosenberg, Zilber-Rosenberg, & Lloyd, 2018). In the most extreme examples, these approaches extend to modifying the genomes of the target species and/or its symbiont(s) to create novel genotypes and holobionts (see reviews by Phelps, Seeb, & Seeb, 2018;Rode, Estoup, Bourguet, Courtier-Orgogozo, & Débarre, 2019).…”

Section: Prop Os Ed Ecosys Tem Interventions From the Org Anis Mal mentioning

confidence: 99%

How do we overcome abrupt degradation of marine ecosystems and meet the challenge of heat waves and climate extremes?

Ainsworth

Hurd

Gates

et al. 2019

Global Change Biology

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Extreme heat wave events are now causing ecosystem degradation across marine ecosystems. The consequences of this heat‐induced damage range from the rapid loss of habitat‐forming organisms, through to a reduction in the services that ecosystems support, and ultimately to impacts on human health and society. How we tackle the sudden emergence of ecosystem‐wide degradation has not yet been addressed in the context of marine heat waves. An examination of recent marine heat waves from around Australia points to the potential important role that respite or refuge from environmental extremes can play in enabling organismal survival. However, most ecological interventions are being devised with a target of mid to late‐century implementation, at which time many of the ecosystems, that the interventions are targeted towards, will have already undergone repeated and widespread heat wave induced degradation. Here, our assessment of the merits of proposed ecological interventions, across a spectrum of approaches, to counter marine environmental extremes, reveals a lack preparedness to counter the effects of extreme conditions on marine ecosystems. The ecological influence of these extremes are projected to continue to impact marine ecosystems in the coming years, long before these interventions can be developed. Our assessment reveals that approaches which are technologically ready and likely to be socially acceptable are locally deployable only, whereas those which are scalable—for example to features as large as major reef systems—are not close to being testable, and are unlikely to obtain social licence for deployment. Knowledge of the environmental timescales for survival of extremes, via respite or refuge, inferred from field observations will help test such intervention tools. The growing frequency of extreme events such as marine heat waves increases the urgency to consider mitigation and intervention tools that support organismal and ecosystem survival in the immediate future, while global climate mitigation and/or intervention are formulated.

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Section: Prop Os Ed Ecosys Tem Interventions From the Org Anis Mal mentioning

confidence: 99%

How do we overcome abrupt degradation of marine ecosystems and meet the challenge of heat waves and climate extremes?

Ainsworth

Hurd

Gates

et al. 2019

Global Change Biology

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“…Alleles of symbiotic microbes are a source of selectable variation that can be stably inherited for millions of generations (Gilbert & Epel, 2015;Gilbert et al, 2010;Moran & Yun, 2015), and the phenotype that natural selection selects is the holobiont. It has been argued that holobionts are a critically important level of biological organization and evolutionary selection (Osmanovic, Kessler, Rabin, & Soen, 2018;Roughgarden, 2019;Roughgarden, Gilbert, Rosenberg, Zilber-Rosenberg, & Lloyd, 2017;Zilber-Rosenberg & Rosenberg, 2008).…”

Section: Foregrounding John Bonner's Questionsmentioning

confidence: 99%

Evolutionary transitions revisited: Holobiont evo‐devo

Gilbert

2019

J Exp Zool Pt B

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John T. Bonner lists four essential transformations in the evolution of life: the emergence of the eukaryotic cell, meiosis, multicellularity, and the nervous system. This paper analyses the mechanisms for those transitions in light of three of Dr. Bonner's earlier hypotheses: (a) that the organism is its life cycle, (b) that evolution consists of alterations of the life cycle, and (c) that development extends beyond the body and into interactions with other organisms. Using the notion of the holobiont life cycle, this paper attempts to show that these evolutionary transitions can be accomplished through various means of symbiosis. Perceiving the organism both as an interspecies consortium and as a life cycle supports a twofold redefinition of the organism as a holobiont constructed by integrating together the life cycles of several species. These findings highlight the importance of symbiosis and the holobiont development in analyses of evolution.

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“…The holobiont is an anatomical, physiological, developmental, and immunological unit (Gilbert et al, 2012;McFall-Ngai et al, 2013, Rosenberg & Zilber-Rosenberg, 2016Roughgarden, Gilbert, Rosenberg, Zilber-Rosenberg, & Lloyd, 2017;Zilber-Rosenberg & Rosenberg, 2008). The holobiont nature of animal anatomy and physiology is highlighted in several species where the microbes play critical roles in defining the organism.…”

Section: Introductionmentioning

confidence: 99%

“…The "hologenome concept of evolution" considers the holobiont with its hologenome (the collective genomes of the microbes as well as the zygote-derived cells) as a level of selection in evolution (Osmanovic, Kessler, Rabin, & Soen, 2018;Roughgarden, 2019;Roughgarden et al, 2017;Zilber-Rosenberg & Rosenberg, 2008). The "hologenome concept of evolution" considers the holobiont with its hologenome (the collective genomes of the microbes as well as the zygote-derived cells) as a level of selection in evolution (Osmanovic, Kessler, Rabin, & Soen, 2018;Roughgarden, 2019;Roughgarden et al, 2017;Zilber-Rosenberg & Rosenberg, 2008).…”

Section: Introductionmentioning

confidence: 99%

“…These properties of holobionts have important evolutionary implications. The "hologenome concept of evolution" considers the holobiont with its hologenome (the collective genomes of the microbes as well as the zygote-derived cells) as a level of selection in evolution (Osmanovic, Kessler, Rabin, & Soen, 2018;Roughgarden, 2019;Roughgarden et al, 2017;Zilber-Rosenberg & Rosenberg, 2008). Holobionts meet the criteria for being considered evolutionary agents, as they are interactors, replicators/reproducers, and manifestors of adaptation (Roughgarden et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

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Developmental symbiosis facilitates the multiple origins of herbivory

Gilbert

2019

Evolution and Development

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Developmental bias toward particular evolutionary trajectories can be facilitated through symbiosis. Organisms are holobionts, consisting of zygotederived cells and a consortia of microbes, and the development, physiology, and immunity of animals are properties of complex interactions between the zygotederived cells and microbial symbionts. Such symbionts can be agents of developmental plasticity, allowing an organism to develop in particular directions. This plasticity can lead to genetic assimilation either through the incorporation of microbial genes into host genomes or through the direct maternal transmission of the microbes. Such plasticity can lead to niche construction, enabling the microbes to remodel host anatomy and/or physiology. In this article, I will focus on the ability of symbionts to bias development toward the evolution of herbivory. I will posit that the behavioral and morphological manifestations of herbivorous phenotypes must be preceded by the successful establishment of a community of symbiotic microbes that can digest cell walls and detoxify plant poisons. The ability of holobionts to digest plant materials can range from being a plastic trait, dependent on the transient incorporation of environmental microbes, to becoming a heritable trait of the holobiont organism, transmitted through the maternal propagation of symbionts or their genes. K E Y W O R D S

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Holobionts as Units of Selection and a Model of Their Population Dynamics and Evolution

Cited by 158 publications

References 202 publications

How do we overcome abrupt degradation of marine ecosystems and meet the challenge of heat waves and climate extremes?

How do we overcome abrupt degradation of marine ecosystems and meet the challenge of heat waves and climate extremes?

Evolutionary transitions revisited: Holobiont evo‐devo

Developmental symbiosis facilitates the multiple origins of herbivory

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