Multicellularity in animals: The potential for within-organism conflict

Howe, Jack; Rink, Jochen C.; Wang, Bo; Griffin, Ashleigh S.

doi:10.1073/pnas.2120457119

Cited by 18 publications

(27 citation statements)

References 115 publications

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“…Our focus is on ‘selfish elements’, which we use as a catch‐all term to cover both selfish genetic elements and selfish cell lineages. Throughout we will use intentional words like ‘selfish’, ‘goals’, and ‘strategy’, as is common in evolutionary biology (Dawkins, 1995; Ågren & Patten, 2022; Ågren 2021; Howe et al ., 2022).…”

Section: A Classification Of Selfish Elementsmentioning

confidence: 99%

“…4A). Cells of the same body are in principle fully related to each other (Queller, 2000; Howe et al ., 2022). Consequently, all gene copies residing within somatic cells have an equal chance of being represented in the germline, and so all benefit from furthering the fitness of the organism rather than trying to undermine it (Haig, 2021).…”

Section: Organismality In the Face Of Internal Conflictsmentioning

confidence: 99%

“…Different parts of an organism's genome and body, however, may not always have the organism's interests at heart. From a theoretical perspective, this threatens the unity of purpose required for evolutionary agency to reside solely with organisms from within (Hurst, 1996; Clarke, 2016; Okasha, 2018; Howe et al ., 2022), although empirically organismal integrity appears to be maintained as these threats are kept in check (see also Section III). Nonetheless, agents like cancer cells and selfish genetic elements have the ability to promote their own propagation at the expense of other cells and genes (Burt & Trivers, 2006; Ågren & Clark, 2018).…”

Section: Introductionmentioning

confidence: 99%

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Adaptation in the face of internal conflict: the paradox of the organism revisited

2023

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The paradox of the organism refers to the observation that organisms appear to function as coherent purposeful entities, despite the potential for within‐organismal components like selfish genetic elements and cancer cells to erode them from within. While it is commonly accepted that organisms may pursue fitness maximisation and can be thought to hold particular agendas, there is a growing recognition that genes and cells do so as well. This can lead to evolutionary conflicts between an organism and the parts that reside within it. Here, we revisit the paradox of the organism. We first outline its conception and relationship to debates about adaptation in evolutionary biology. Second, we review the ways selfish elements may exploit organisms, and the extent to which this threatens organismal integrity. To this end, we introduce a novel classification scheme that distinguishes between selfish elements that seek to distort transmission versus those that seek to distort phenotypic traits. Our classification scheme also highlights how some selfish elements elude a multi‐level selection decomposition using the Price equation. Third, we discuss how the organism can retain its status as the primary fitness‐maximising agent in the face of selfish elements. The success of selfish elements is often constrained by their strategy and further limited by a combination of fitness alignment and enforcement mechanisms controlled by the organism. Finally, we argue for the need for quantitative measures of both internal conflicts and organismality.

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Section: A Classification Of Selfish Elementsmentioning

confidence: 99%

Section: Organismality In the Face Of Internal Conflictsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Adaptation in the face of internal conflict: the paradox of the organism revisited

2023

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“…That is, if natural selection is conceived as a would-be designer of sorts (e.g., Lewens, 2004;Dennett, 2009), then its designs (adaptations) are for the benefit of the individual organism (Gardner, 2009). The existence of selfish genetic elements and selfish cell lineages, however, threatens both of these views (Ågren, 2016;Gardner & Úbeda, 2017;Okasha, 2018;Scott & West, 2019;Howe et al, 2022Howe et al, , 2024. Such internal conflict can prevent organisms from maximizing their inclusive fitness, and it leaves open the possibility that adaptive phenotypes can be found at sub-organismal levels of selection.…”

Section: Introductionmentioning

confidence: 99%

Quantifying internal conflicts and their threats to organismal form and fitness

Schenkel,

Patten,

Ågren

2024

Preprint

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Evolutionary biologists often treat organisms as both fitness-maximizing agents and as the primary level at which adaptation manifests. Yet, genes and cells may also seek to optimize their fitness by distorting the Mendelian rules of transmission or by influencing organismal traits for their own benefit. Organismal form and fitness are therefore threatened from within by selfish genes and cells. However, to what extent such internal conflicts actually harm individual organisms and threaten our concept of the organism as the sole bearer of adaptation remains unclear. We introduce a mathematical framework to capture the threat posed by internal conflicts and develop two metrics to measure their various forms of harm. We name these metrics fitness unity and trait unity, and use them to refer to the threats posed by internal conflicts to an organism's role as the optimizing agent and the strategy wielded to achieve that optimization, respectively. We apply our framework to two examples of internal conflicts, genomic imprinting and sex ratio distortion, to illustrate how such harms from internal conflict may be quantified. We conclude by discussing the conditions under which internal conflict becomes sufficiently disruptive to organisms that it no longer makes sense to think of them as unified fitness-maximizing agents, but instead as adaptive compromises of multiple competing sub-agents.

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“…However, planarian reproductive strategies are highly diverse at the taxon level and range from sexual reproduction to various forms of parthenogenesis and asexual propagation by fission and regeneration 26 . The formation of germ cells from somatic neoblasts and the “inheritance” of many parental neoblasts by a fission fragment raises profound questions regarding genome evolution, including the maintenance of “genetic self” within the pluripotent stem cell population of an individual 27 . Given these profound questions regarding genome evolution and the rapid growth of the planarian research community in general, high-quality genomic resources are highly desirable.…”

Section: Introductionmentioning

confidence: 99%

A comparative analysis of planarian genomes reveals regulatory conservation in the face of rapid structural divergence

Ivankovic,

Brand,

Pandolfini

et al. 2023

Preprint

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The planarianSchmidtea mediterraneacan regenerate its entire body from small tissue fragments and is studied as regeneration model species. The assembly and functional analysis of planarian genomes has proven challenging due its high A/T content (70% A/T), repetitive nature, and limited transferability of routine laboratory protocols due to their divergent biochemistry. Only few and often fragmented genome assemblies are currently available, and open challenges include the provision of well-annotated chromosome-scale reference assemblies of the model species and other planarians for a comparative genome evolution perspective. Here we report a haplotype-phased, chromosome-scale genome assembly and high-quality gene annotations of the sexual S2 strain ofS. mediterraneaand provide putative regulatory region annotations via optimized ATAC-seq and ChIP-seq protocols. To additionally leverage sequence conservation for regulatory element annotations, we generated chromosome-scale genome assemblies and chromatin accessibility data for the three closest relatives ofS. mediterranea:S. polychroa,S. nova, andS. lugubris. We find substantial divergence in protein-coding sequences and regulatory regions, yet reveal remarkable conservation in ChIP-mark bearing open chromatin regions identified as promoters and enhancers inS. mediterranea. The resulting high-confidence set of evolutionary conserved enhancers and promoters provides a valuable resource for the analysis of gene regulatory circuits and their evolution within the taxon. In addition, our four chromosome-scale genome assemblies provide a first comparative perspective on planarian genome evolution. Our analyses reveal frequent retrotransposon-associated chromosomal inversions and inter-chromosomal translocations that lead to a degradation of synteny across the genus. Interestingly, we further find independent and near-complete losses of the ancestral metazoan synteny acrossSchmidteaand two other flatworm groups, indicating that platyhelminth genomes largely evolve without syntenic constraints. Our work provides valuable genome resources for the planarian research community and sets a foundation for the comparative genomics of planarians. We reveal a contrast between the fast structural evolution of planarian genomes and the conservation of their regulatory elements, suggesting a unique genome evolution in flatworms where gene positioning may not be essential.

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Multicellularity in animals: The potential for within-organism conflict

Cited by 18 publications

References 115 publications

Adaptation in the face of internal conflict: the paradox of the organism revisited

Adaptation in the face of internal conflict: the paradox of the organism revisited

Quantifying internal conflicts and their threats to organismal form and fitness

A comparative analysis of planarian genomes reveals regulatory conservation in the face of rapid structural divergence

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