The evolution of host-symbiont dependence

Abstract

Organisms across the tree of life form symbiotic partnerships with microbes for metabolism, protection and resources. While some hosts evolve extreme dependence on their symbionts, others maintain facultative associations. Explaining this variation is fundamental to understanding when symbiosis can lead to new higher-level individuals, such as during the evolution of the eukaryotic cell. Here we perform phylogenetic comparative analyses on 106 unique host-bacterial symbioses to test for correlations between symbiont function, transmission mode, genome size and host dependence. We find that both transmission mode and symbiont function are correlated with host dependence, with reductions in host fitness being greatest when nutrient-provisioning, vertically transmitted symbionts are removed. We also find a negative correlation between host dependence and symbiont genome size in vertically, but not horizontally, transmitted symbionts. These results suggest that both function and population structure are important in driving irreversible dependence between hosts and symbionts.

Figure 1. Variation in host dependence on symbionts and their predominant mode of transmission.

The degree to which hosts are dependent on bacterial symbionts for survival and reproduction varies hugely across taxa. Some hosts and symbionts have facultative relationships, where neither partner is dependent on each other. This may be because hosts only need symbionts in certain conditions, for example, legumes and Rhizobia, or because symbionts are only present in some of the host population, for example, aphids and Hamiltonella. In contrast, some hosts are entirely dependent on symbionts for nutrition either because they live in extreme environments, for example, deep-sea tube worms and Endoriftia, or because they have restricted diets, for example, leafhoppers and Baumannia. Image of Graphocephala coccinea sourced from phylopic.org, courtesy of Melissa Broussard available under a Creative Commons license.

Figure 2. Bacterial symbiosis across the tree of life.

A phylogeny of bacterial symbionts in our database built using an ∼1,500 bp region of the 16S rRNA gene, with images of their host groups. Vertically transmitted symbionts are shown with red circles and horizontally transmitted symbionts are shown with black circles. Multiple species names at the tips are distinct lineages found in different host groups. Images of hosts are not intended to be exact representations of the host species, but more of the general host group (for example, wasp, worm and plant). Where there is no image, this is because a suitable representation of the host species was not available. Host images sourced from Phylopic (phylopic.org): Graphocephala coccinea courtesy of Melissa Broussard; Hippoboscoidea fly courtesy of Gareth Monger; Sepioidea squid courtesy of David Sim and T. Michael Keesey; Uropodina tick courtesy of Birgit Lang; and Brugia nematode courtesy of Gareth Monger; all available under a Creative Commons license.

Figure 3. Transmission mode and symbiont function correlate with host dependence.

Each data point represents the mean % reduction in host fitness when its symbiont is removed from each unique symbiosis. The horizontal lines represent the mean % host fitness reduction. (a) Hosts tend to be more dependent on vertically transmitted symbionts. Plotted N_symbioses=38; (b) Hosts tend to be more dependent on nutritional compared to defensive symbionts. Plotted nutritional, N_symbioses=28, and defensive, N_symbioses=7.

Figure 4. Correlated evolution of host dependence and symbiont genome size.

Each data point represents the mean % host fitness reduction for a unique host-symbiont combination with 95% confidence intervals. (a) Vertical transmission: BPMM; posterior mode for slope=−0.14; CI=−30.54 to 6.65; N_symbioses=12. (b) Horizontal transmission: BPMM; posterior mode for slope=1.03; CI=−31.51 to 24.50; N_symbioses=10.

Figure 5. Vertically transmitted symbionts have smaller genomes.

Each data point represents the genome size for the symbiont in a unique host–symbiont combination. The horizontal bars represent mean genome sizes for each transmission mode. Horizontal: N_symbioses=13 and N_datapoints=125; vertical: N_symbioses=55 and N_datapoints=253.