PSA2016: The 25th Biennial Meeting of the Philosophy of Science Association

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Holobionts and biofilms are not as a rule “units of selection”, but the metabolic interaction networks they support, replicating by recruitment, arguably are.

Animals and plants together with all the microbes in and on them are now often called “holobionts” and the ensemble of their genomes “hologenomes”. There is active debate about whether such multi-lineage entities can rightly be conceived as units of selection (Moran and Sloan 2015; Theis et al 2016). A similar controversy concerns multi-species microbial biofilms (structured microbial communities embedded in an extracellular matrix and not necessarily associated with an animal or plant [Clarke 2016]). A central issue in both debates is whether the several organismal or genomic lineages involved in these microbe-macrobe or microbe-microbe communities comprise “collective reproducers” (Godfrey-Smith 2015). But both holobionts and biofilms are so disparate as classes that no general resolution can be reasonably expected, and the fact that the taxa that comprise them typically vary rules out collective reproduction. Without this, it seems implausible that multilineage entities can be units of selection, and yet the notion that holobionts and biofilms call for something beyond traditional co-evolutionary models retains considerable appeal. One way to preserve such appeal is to consider the collective interactions (metabolic pathways or physiological/developmental activities) of multi-lineage assemblages as that which responds to selection. Such patterns of interaction replicate (like DNA) by recruitment (of taxa rather than nucleotides), and potentially vary in “fitness”, this understood as effects on hosts, ecological spread, or persistence. Another and largely complementary way to retain the interest in the evolutionary role of multilineage entities would see collective interactions as constructed niches, comprising opportunities and challenges that largely drive microbial evolution at the level of individual organisms and their genes. Interestingly, once communities of microbes and/or hosts capable of carrying out the various components of a collective interaction pattern (multi-step biosynthesis of an essential metabolite or a complex developmental process for instance) have been established, that pattern can be temporarily disrupted but will be recreated by the community: recurrence mimics replication. Although most interaction patterns may be only “marginal” units of selection, the existence of metabolic pathways, cycles and community-wide interactions fuels, on a global scale, the evolution of thousands or millions of genes and taxa that carry out their steps and processes, underwriting that existence and stabilizing the biosphere.

Clarke, Ellen. 2016. Levels of selection in biofilms: multispecies biofilms are not evolutionary individuals. Biology and Philosophy 31(2): 191-212.

Godfrey-Smith, Peter. 2015. Reproduction, symbiosis and the eukaryotic cell. Proceedings of the National Academy of Sciences 112: 10120-10125.

Moran, Nancy A, and Sloan, David B. 2015. The hologenome concept: helpful or hollow? PLoS Biology 13(12) e1002311.

Theis, Kevin, et al. 2016. Getting the hologenome concept right: an eco-evolutionary framework for hosts and their microbiomes. mSystems 1(2):e00028-16.

Author Information:

W. Ford Doolittle    
Biochemistry and Molecular Biology
Dalhousie University

Austin Booth    
Biochemistry and Molecular Biology AND Philosophy
Dalhousie University

 

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