Holobiont Evolution: Population Genetic Theory for the Hologenome

Abstract

AbstractThis paper develops a mathematical theory for holobiont evolution that parallels the population-genetic theory of classical evolutionary biology. It presents theory for hologenomes having two haploid microbial strains and two diploid host alleles. The theory reveals how selection on holobionts causes the joint evolution of microbial and host components of the hologenome. The paper shows how holobiont selection differs from coevolutionary selection, how holobiont selection is effective with both vertical and horizontal microbiome transmission, how inheritance can be a collective process rather than solely a lineal process, how random microbial colonization of the microbiome is the counterpart to random union of gametes for nuclear genes, how the evolutionary success of a microbial strain depends on within-host K-selection and between-host r-selection leading to an expression for the multilevel fitness per holobiont, how the hologenome is analogous to a two-loci genetic system, how holobiont selection maximizes equality of marginal fitnesses and not overall mean fitness, how the concept of an evolutionarily stable strategy (ESS) can be extended to hologenomes (HSS) leading to the evolution of cooperative microbe-host coadaptation, how the HSS can be invaded by an altruistic microbe resulting in a microbial polymorphism that expresses a balance of within-holobiont selfishness and between-holobiont altruism, how holobiont selection with horizontal transmission comprises a new third type of multilevel selection, and overall, how the concept of the hologenome with holobiont selection can be made conceptually and mathematically rigorous.