Symbiote transmission and maintenance of extra-genomic associations

Abstract

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. © 2014 Fitzpatrick.