Housing microbial symbionts: evolutionary origins and diversification of symbiotic organs in animals

Abstract

In many animal hosts, microbial symbionts are housed within specialized structures known as symbiotic organs, but the evolutionary origins of these structures have rarely been investigated. Here, I adopt an evolutionary developmental (evo-devo) approach, specifically to apply knowledge of the development of symbiotic organs to gain insights into their evolutionary origins and diversification. In particular, host genetic changes associated with evolution of symbiotic organs can be inferred from studies to identify the host genes that orchestrate the development of symbiotic organs, recognizing that microbial products may also play a key role in triggering the developmental programme in some associations. These studies may also reveal whether higher animal taxonomic groups (order, class, phylum, etc.) possess a common genetic regulatory network for symbiosis that is latent in taxa lacking symbiotic organs, and activated at the origination of symbiosis in different host lineages. In this way, apparent instances of convergent evolution of symbiotic organs may be homologous in terms of a common genetic blueprint for symbiosis. Advances in genetic technologies, including reverse genetic tools and genome editing, will facilitate the application of evo-devo approaches to investigate the evolution of symbiotic organs in animals. This article is part of the theme issue 'The role of the microbiome in host evolution'.

Keywords: bacteriome; light organ; symbiosis; symbiotic organ; trophosome.

Figure 1.

The squid light organ. (a) Localization of light organ in mantle cavity of the squid Euprymna scolopes. (b) Structure of E. scolopes light organ. (c) Phylogenetic distribution of bacterial light organs in cephalopod molluscs (indicated by asterisks (*)). Redrawn from figure 1 of Pankey et al. [3].

Figure 2.

Microbial symbioses in insects of the order Hemiptera. (a) Phylogenetic distribution of symbioses. Bacteriomes bearing intracellular bacteria are the likely ancestral condition of suborders Sternorrhyncha, Auchenorrhyncha and Coleorrhyncha (*) but not Heteroptera. Within the Heteroptera, a symbiotic organ comprising ceca in the distal midgut (M4 region) is ancestral to four superfamilies of the Pentatomomorpha, and harbours either β-proteobacteria of the Burkholderia group (Lygaeoidea, Coroidea and Pyrrhococoidea) or γ-proteobacteria (Pentatomoidea). This association has been replaced by a M3 gut symbiosis in some Pyrrhocoroidea and by bacteriomes in some Lygoidea. (b) Functional anatomy of the gut of Riptortus pedestris, showing the M4 symbiotic organ and the divergent fate of ingested food and Burkholderia.