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Original Research ARTICLE

Front. Microbiol., 24 February 2014 | http://dx.doi.org/10.3389/fmicb.2014.00046

Symbiote transmission and maintenance of extra-genomic associations

  • Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, TN, USA

Symbiotes can be transmitted from parents to offspring or horizontally from unrelated hosts or the environment. A key question is whether symbiote transmission is similar enough to Mendelian gene transmission to generate and maintain coevolutionary associations between host and symbiote genes. Recent papers come to opposite conclusions, with some suggesting that any horizontal transmission eliminates genetic association. These studies are hard to compare owing to arbitrary differences in modeling approach, parameter values, and assumptions about selection. I show that associations between host and symbiote genes (extra-genomic associations) can be described by the same dynamic model as conventional linkage disequilibria between genes in the same genome. Thus, covariance between host and symbiote genomes depends on population history, geographic structure, selection, and co-transmission rate, just as covariance between genes within a genome. The conclusion that horizontal transmission rapidly erodes extra-genomic associations is equivalent to the conclusion that recombination rapidly erodes associations between genes within a genome. The conclusion is correct in the absence of population structure or selection. However, population structure can maintain spatial associations between host and symbiote traits, and non-additive selection (interspecific epistasis) can generate covariances between host and symbiote genotypes. These results can also be applied to cultural or other non-genetic traits. This work contributes to a growing consensus that genomic, symbiotic, and gene-culture evolution can be analyzed under a common theoretical framework. In terms of coevolutionary potential, symbiotes can be viewed as lying on a continuum between the intimacy of genes and the indifference of casually co-occurring species.

Keywords: vertical transmission, horizontal transmission, symbiosis, gene-culture, coevolution, dual-inheritance theory, interspecific disequilibrium, metagenome

Citation: Fitzpatrick BM (2014) Symbiote transmission and maintenance of extra-genomic associations. Front. Microbiol. 5:46. doi: 10.3389/fmicb.2014.00046

Received: 18 December 2013; Paper pending published: 20 January 2014;
Accepted: 21 January 2014; Published online: 24 February 2014.

Edited by:

Monica Medina, Pennsylvania State University, USA

Reviewed by:

Carl J. Yeoman, Montana State University, USA
Martin Zimmer, Universität Salzburg, Austria

Copyright © 2014 Fitzpatrick. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Benjamin M. Fitzpatrick, Department of Ecology and Evolutionary Biology, University of Tennessee, 569 Dabney, Knoxville, TN 37996, USA e-mail: benfitz@utk.edu