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Holobiont Evolution: Mathematical Model with Vertical vs. Horizontal Microbiome Transmission

Roughgarden, Joan (2020) Holobiont Evolution: Mathematical Model with Vertical vs. Horizontal Microbiome Transmission. Philosophy, Theory, and Practice in Biology, 12 (002). ISSN 2475-3025

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Abstract

A holobiont is a composite organism consisting of a host together with its microbiome, such as a coral with its zooxanthellae. To explain the often intimate integration between hosts and their microbiomes, some investigators contend that selection operates on holobionts as a unit and view the microbiome’s genes as extending the host’s nuclear genome to jointly comprise a hologenome. Because vertical transmission of microbiomes is uncommon, other investigators contend that holobiont selection cannot be effective because a holobiont’s microbiome is an acquired condition rather than an inherited trait. This disagreement invites a simple mathematical model to see how holobiont selection might operate and to assess its plausibility as an evolutionary force. This paper presents two variants of such a model. In one variant, juvenile hosts obtain microbiomes from their parents (vertical transmission). In the other variant, microbiomes of juvenile hosts are assembled from source pools containing the combined microbiomes of all parents (horizontal transmission). According to both variants, holobiont selection indeed causes evolutionary change in holobiont traits. Therefore, holobiont selection is plausibly an effective evolutionary force with either mode of microbiome transmission. The modeling employs two distinct concepts of inheritance, depending on the mode of microbiome transmission: collective inheritance whereby juveniles inherit a sample of the collected genomes from all parents, as contrasted with lineal inheritance whereby juveniles inherit the genomes from only their own parents. A distinction between collective and lineal inheritance also features in theories of multilevel selection.


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Item Type: Published Article or Volume
Creators:
CreatorsEmailORCID
Roughgarden, Joanjoan.roughgarden@stanford.edu
Additional Information: ISSN: 1949-0739 (print)
Keywords: Collective inheritance; Holobiont; Holobiont selection; Hologenome; Lineal inheritance; Microbiome; Multilevel selection
Subjects: Specific Sciences > Biology
Specific Sciences > Biology > Evolutionary Theory
Specific Sciences > Biology > Systematics
General Issues > History of Science Case Studies
General Issues > Models and Idealization
Depositing User: Jordan Miller
Date Deposited: 24 Jul 2020 15:52
Last Modified: 18 Jun 2021 13:55
Item ID: 17655
Journal or Publication Title: Philosophy, Theory, and Practice in Biology
Official URL: https://quod.lib.umich.edu/p/ptpbio/16039257.0012....
DOI or Unique Handle: 10.3998/ptpbio.16039257.0012.002
Subjects: Specific Sciences > Biology
Specific Sciences > Biology > Evolutionary Theory
Specific Sciences > Biology > Systematics
General Issues > History of Science Case Studies
General Issues > Models and Idealization
Date: 2020
Volume: 12
Number: 002
ISSN: 2475-3025
URI: https://philsci-archive.pitt.edu/id/eprint/17655

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