Heritable symbiosis: The advantages and perils of an evolutionary rabbit hole

Abstract

Many eukaryotes have obligate associations with microorganisms that are transmitted directly between generations. A model for heritable symbiosis is the association of aphids, a clade of sap-feeding insects, and Buchnera aphidicola, a gammaproteobacterium that colonized an aphid ancestor 150 million years ago and persists in almost all 5,000 aphid species. Symbiont acquisition enables evolutionary and ecological expansion; aphids are one of many insect groups that would not exist without heritable symbiosis. Receiving less attention are potential negative ramifications of symbiotic alliances. In the short run, symbionts impose metabolic costs. Over evolutionary time, hosts evolve dependence beyond the original benefits of the symbiosis. Symbiotic partners enter into an evolutionary spiral that leads to irreversible codependence and associated risks. Host adaptations to symbiosis (e.g., immune-system modification) may impose vulnerabilities. Symbiont genomes also continuously accumulate deleterious mutations, limiting their beneficial contributions and environmental tolerance. Finally, the fitness interests of obligate heritable symbionts are distinct from those of their hosts, leading to selfish tendencies. Thus, genes underlying the host-symbiont interface are predicted to follow a coevolutionary arms race, as observed for genes governing host-pathogen interactions. On the macroevolutionary scale, the rapid evolution of interacting symbiont and host genes is predicted to accelerate host speciation rates by generating genetic incompatibilities. However, degeneration of symbiont genomes may ultimately limit the ecological range of host species, potentially increasing extinction risk. Recent results for the aphid-Buchnera symbiosis and related systems illustrate that, whereas heritable symbiosis can expand ecological range and spur diversification, it also presents potential perils.

Keywords: Buchnera; Muller's ratchet; aphid; coevolution; selection levels.

Fig. 1.

Causes and consequences of symbiotic coevolution. Mutations that negatively impact the symbiosis can be fixed through genetic drift due to clonality and small population size (shown in blue) or through within-host selection for selfish symbionts that favor their own fitness over that of the host (red). In response, the host is selected to buffer these mutations (green), leading to a spiral down the symbiosis rabbit hole. This symbiont–host coevolution may drive the rapid accumulation of genetic incompatibilities between host lineages and between hosts and symbiont strains. Lineage-specific symbiont–host coevolution may lead to accelerated reproductive isolation and speciation, which could further reduce the effective size of genetically compatible host populations.

Fig. 2.

Ecological range restriction by symbiont gene loss. In a specific environment, some symbiont genes may not be needed, resulting in relaxed selection for their maintenance and inactivation. In sap-feeding insects with obligate symbionts, using a food plant with abundant levels of a particular nutrient can lead to irreversible loss of symbiont genes for making that nutrient. A consequence is permanent restriction of the host’s ecological range: for example, confinement to a smaller set of food plant species. As available resources change over time (e.g., due to climate change), a possible consequence of a narrower ecological niche is smaller population size or eventual extinction.

Fig. 3.

Summary of the gains and losses of heritable symbionts across sap-feeding insects in the order Hemiptera. The phylogenies show evolutionary relationships of host insect groups (gray) and heritable symbionts. For color-coded lines, see Inset legend. Host phylogeny represents the most recent understanding, but placement of certain lineages (e.g., the Coleorrhyncha and Heteroptera) is uncertain (12, 89). Ancestral symbiont names are in boxes along their lineage; in some cases, the same symbiont lineage has different names in different insect clades. Names of acquired symbionts are shown where the symbiont is acquired on the host phylogeny. Dashed lines represent hypothetical relationships and possible origins of symbiosis deep in the evolution of the Hemiptera. The white-dashed lineage represents an ancestral symbiont that permitted the initial diversification of the Hemiptera; its identity is not yet known. Lineages that terminate at a question mark remain uncertain; host–symbiont relationships in these clades are diverse and their origins unclear. See text for citations regarding specific symbionts presented on the tree.