Making sense of lineage integration and discordance in host-microbe symbioses

In this paper, I will discuss the complications involved in making sense of lineage integration and discordance in host-microbiota symbioses, now commonly referred to as a single unit: the holobiont. Following this terminology, the genome of the host together with the genomes of all host-associated microbiota is often referred to as the hologenome. Some authors have equated the microbes in a hologenome with genes in the host’s genome. Equating microbes with genes, coupled with horizontal transmission of microbial symbionts, would mean that there is a high degree of (gene or microbe) discordance within any particular holobiont. I will argue that this is a mistaken interpretation, microbes are not the equivalents of genes.

Reciprocal selection pressures emerging from gene-gene interactions between species are commonly recognized as the framework by which to understand co-evolution. I will look to the field of community genetics as a better way to understand host-microbe gene interactions. One promising concept for understanding the interaction of gene lineages between species is Θ. Initially introduced for studying epistasis within genomes, Θ has recently been applied to gene interactions across genomes in the context of community genetics—a type of intergenomic epistasis. It is a measure of the degree of co-inheritance of gene combinations, and it represents the simultaneous co-variance in identity-by-descent of host and symbiont genes when two infected hosts are compared. Theoretically, Θ is increased by vertical transmission and reduced by horizontal transmission and an increased Θ facilitates selection to act on gene combinations across genomes. A high average overall Θ between the host genome and microbial genes might indicate the action of selection at the level of the holobiont and the integration of formerly separate lineages into a single lineage. I will explore the consequences of this framework for combing ecological and evolutionary perspectives—one of the recognized aims of community genetics--in the context of the holobiont.

I conclude by turning to a debate about holobionts in the context of biological individuality. Much of this debate has focused on whether holobionts are integrated individuals, co-evolving communities, or something more akin to transient ecosystems. I will argue that the community genetics framework sheds light on this debate and helps to clarify what factors are important for determining where a particular holobiont sits along the continuum between individual and community. I contend that most holobionts share features of both organisms and communities. Neither reducing the holobiont to a set of pairwise interactions between symbiont partners nor treating the entire community as a single biological individual is a universally appropriate approach.