Towards a Dynamic Interaction Network of Life to Unify and Expand the Evolutionary Theory Eric Bapteste, Philippe Huneman
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Towards a Dynamic Interaction Network of Life to unify and expand the evolutionary theory Eric Bapteste, Philippe Huneman To cite this version: Eric Bapteste, Philippe Huneman. Towards a Dynamic Interaction Network of Life to unify and expand the evolutionary theory. BMC Biology, BioMed Central, 2018, 16 (1), 10.1186/s12915-018- 0531-6. hal-01968453 HAL Id: hal-01968453 https://hal.archives-ouvertes.fr/hal-01968453 Submitted on 2 Jan 2019 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Bapteste and Huneman BMC Biology _#####################_ https://doi.org/10.1186/s12915-018-0531-6 1 OPINION Open Access 2 Towards a Dynamic Interaction Network of 3 Life to unify and expand the evolutionary 4 theory 1,2* 3 Q1 6785 Eric Bapteste and Philippe Huneman ’ 9 Abstract Mendel s idea of particular inheritance, giving rise to 39 population and quantitative genetics, a theoretical frame 40 10 The classic Darwinian theory and the Synthetic ’ that corroborated Darwin s hypothesis of the paramount 41 11 evolutionary theory and their linear models, while power of selection for driving adaptive evolution [2]. 42 12 invaluable to study the origins and evolution of species, This framework progressively aggregated multiple disci- 43 13 are not primarily designed to model the evolution of plines: behavioural ecology, microbiology, paleobiology, 44 14 organisations, typically that of ecosystems, nor that of etc. Overall, this classic framework considers that the 45 15 processes. How could evolutionary theory better principal agency of evolution is natural selection of 46 16 explain the evolution of biological complexity and favourable variations, and that those variations are con- 47 17 diversity? Inclusive network-based analyses of dynamic stituted by random mutations and recombination in a 48 18 systems could retrace interactions between (related or Mendelian population. The processes of microevolution, 49 19 unrelated) components. This theoretical shift from a modelled by population and quantitative genetics, are 50 20 Tree of Life to a Dynamic Interaction Network of Life, likely to be extrapolated to macroevolution [3]. To this 51 21 which is supported by diverse molecular, cellular, extent, models that focus on one or two loci are able to 52 22 microbiological, organismal, ecological and evolutionary capture much of the evolutionary dynamics of an organ- 53 23 studies, would further unify evolutionary biology. ism, even though in reality many interdependencies be- 54 24 Keywords: Evolutionary biology, Interactions, tween thousands of loci (epistasis, dominance, etc.) 55 Theoretical biology, Tree of Life, Web of Life occur as the basis of the production and functioning of a 56 25 phenotypic trait. Among forces acting on populations 57 and modelled by population geneticists, natural selection 58 26 Deciphering diversity through evolution is the one that shapes traits as adaptations and the de- 59 27 The living world is nested and multilevel, involves mul- sign of organisms; adaptive radiation then explains much 60 28 tiple agents and changes at different timescales. Evolu- of the diversity; and common descent from adapted 61 29 tionary biology tries to characterize the dynamics organisms explains most of the commonalities across 62 30 responsible for such complexity to decipher the pro- living forms (labelled homologies), and allows for classi- 63 31 cesses accounting for the past and extant diversity ob- fying living beings into phylogenetic trees. Evolution is 64 32 served in molecules (namely, genes, RNA, proteins), gradual because the effects of mutations are generally 65 33 cellular machineries, unicellular and multi-cellular or- small, large ones being most likely to be deleterious as 66 ’ 34 ganisms, species, communities and ecosystems. In the theorized by Fisher s geometric model [4]. 67 35 1930s and 1940s, a unified framework to handle this task Many theoretical divergences surround this core view: 68 36 was built under the name of Modern Synthesis [1]. It not everyone agrees that evolution is change in allele fre- 69 ’ 37 encompassed Darwin s idea of evolution by natural selec- quencies, or that population genetics captures the whole 70 38 tion as an explanation for diversity and adaptation and of the evolutionary process, or that the genotypic view- 71 — ‘ ’ point tracking the dynamics of genes as replicators [5] 72 or the strategy ‘choices’ of organisms as fitness maximiz- * Correspondence: [email protected] 73 1 — Q7 Sorbonne Universités, UPMC Université Paris 06, Institut de Biologie ing agents [6] should be favoured to understand evolu- 74 Paris-Seine (IBPS), F-75005 Paris, France tion. Nevertheless, it has been a powerful enough 2 75 CNRS, UMR7138, Institut de Biologie Paris-Seine, F-75005 Paris, France framework to drive successful research programs on Full list of author information is available at the end of the article 76 © Bapteste et al. 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Bapteste and Huneman BMC Biology _#####################_ Page 2 of 16 77 speciation, adaptation, phylogenies, evolution of sex, we argue that evolutionary biology could become a sci- 131 78 cooperation altruism, mutualism, etc., and incorporate ap- ence of evolving networks, which would allow biologists 132 79 parent challenges such as neutral evolution [7], acknow- to explain organisational complexity, while providing a 133 80 ledgement of constraints on variation [8], or the recent novel way to reframe and to unify evolutionary biology. 134 81 theoretical turn from genetics to genomics following the 82 achievement of the Human Genome Program [9]. Caus- Biology is regulated by networks 135 83 ation is here overall conceived of as a linear causal relation Networks at the molecular level 136 84 of a twofold nature: from the genotype to the phenotype Although numerous studies have focused on the functions 137 85 (assuming of course environmental parameters), and from of individual genes, proteins and other molecules, it is in- 138 86 the environment to the shaping of organisms via natural creasingly clear that each of these functions belongs to 139 87 selection. For instance, in the classic case of evolution of complex networks of interactions. Starting at the molecu- 140 88 peppered moths in urban forests at the time of the indus- lar scale, the importance of a diversity of molecular agents, 141 89 trial revolution, trees became darkened with soot, and such as (DNA-based) genes and their regulatory se- 142 90 then natural selection favored darker morphs as ‘fitter’ quences, RNAs and proteins, is well recognized. Import- 143 91 ones, due to their being less easily detected by predator antly, in terms of their origins and modes of evolution, 144 92 birds, resulting in a relative increase in frequency of the these agents are diverse. Genes are replicated across gen- 145 93 darker morphs in the population [10]. erations, via the recruitment of bases along a DNA tem- 146 94 Yet in the last 15 years biologists and philosophers of plate, thereby forming continuous lineages, affected by 147 95 biology have regularly questioned the genuinely unifying Darwinian evolution. By contrast, proteins are recon- 148 96 character of this Synthesis, as well as its explanatory ac- structed by recruitment of amino acids at the ribosomal 149 97 curacy [11]. Those criticisms questioned notably the set machinery. There is no physical continuity between gener- 150 98 of objects privileged by the Modern Synthesis, arguably ations of proteins, and thus no possibility for these agents 151 99 too gene-centered [12], and its key explanatory to directly accumulate beneficial mutations [25]. 152 100 processes, since niche construction [13], lateral gene Moreover, all these molecular entities are compositionally 153 101 transfer [14, 15], phenotypic plasticity [16, 17], and mass complex, in the sense that they are made of inherited or 154 102 extinction [18] could, for example, be added [11]. reassembled parts. E pluribus unum: genes and proteins 155 103 Usually these critiques emphasize aspects rooted in a are (often) conglomerates of exons, (eventually) introns 156 104 particular biological discipline: lateral gene transfer from [26–28], and domains [29–31]. Similar claims can be 157 105 microbiology, plasticity from developmental biology, made about composite molecular systems, such as 158 106 mass extinction from paleobiology, ecosystem engineer- CRISPR and Casposons [32, 33], etc. This modular organ- 159 107 ing from functional ecology,