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Heritable Symbiosis: the Advantages and Perils of an Evolutionary Rabbit

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Heritable Symbiosis: the Advantages and Perils of an Evolutionary Rabbit PAPER Heritable symbiosis: The advantages and perils of an COLLOQUIUM evolutionary rabbit hole Gordon M. Bennett and Nancy A. Moran1 Department of Integrative Biology, University of Texas at Austin, Austin, TX 78712 Edited by W. Ford Doolittle, Dalhousie University, Halifax, NS, Canada, and approved January 26, 2015 (received for review December 19, 2014) Many eukaryotes have obligate associations with microorganisms leading to symbiont selfishness, and adaptive compensation on that are transmitted directly between generations. A model for thepartofhosts(Fig.1).Theinteraction of these forces results heritable symbiosis is the association of aphids, a clade of sap- in rapid and ongoing evolutionary change in both symbiotic feeding insects, and Buchnera aphidicola, a gammaproteobacte- partners, with profound evolutionary consequences. Symbiont de- rium that colonized an aphid ancestor 150 million years ago and generation coupled with host compensation is a defining charac- persists in almost all 5,000 aphid species. Symbiont acquisition teristic of heritable symbiosis. A salient feature of this relationship is enables evolutionary and ecological expansion; aphids are one that the host must maintain a viable symbiosis with a partner that of many insect groups that would not exist without heritable sym- has a rapidly evolving genome due to the nonadaptive fixation of biosis. Receiving less attention are potential negative ramifications mutations through drift. In sum, the host must keep pace with of symbiotic alliances. In the short run, symbionts impose meta- itssymbiontasmultipleforcesdrawiteverfurtherdownthe bolic costs. Over evolutionary time, hosts evolve dependence be- rabbit hole. yond the original benefits of the symbiosis. Symbiotic partners In this perspective, we focus on insect–bacterial symbioses, enter into an evolutionary spiral that leads to irreversible code- especially the symbiosis of pea aphid (Hemiptera: Acyrthosiphon pendence and associated risks. Host adaptations to symbiosis (e.g., pisum)andBuchnera aphidicola (Gammaproteobacteria), for which immune-system modification) may impose vulnerabilities. Symbi- recent experimental studies have yielded new insights into the ont genomes also continuously accumulate deleterious mutations, integration of symbiotic partners. These ideas are potentially ap- limiting their beneficial contributions and environmental toler- plicable to a broad range of heritable symbioses in which the sym- EVOLUTION ance. Finally, the fitness interests of obligate heritable symbionts biont is strictly clonal and restricted to living in hosts. are distinct from those of their hosts, leading to selfish tendencies. Thus, genes underlying the host–symbiont interface are predicted Evolutionary Opportunities from Symbiosis: Ecological to follow a coevolutionary arms race, as observed for genes gov- Benefit and Lineage Expansion erning host–pathogen interactions. On the macroevolutionary On macroevolutionary time scales, symbiont acquisition has often scale, the rapid evolution of interacting symbiont and host genes enabled evolutionary diversification and ecological expansion. is predicted to accelerate host speciation rates by generating genetic By acquiring maternally transmitted bacterial symbionts, many incompatibilities. However, degeneration of symbiont genomes insect lineages have succeeded in unlocking new ecological niches, may ultimately limit the ecological range of host species, poten- particularly ones that present nutritionally unbalanced diets. tially increasing extinction risk. Recent results for the aphid– Aphids and other sap-feeding insects rely on phloem sap or xylem Buchnera symbiosis and related systems illustrate that, whereas sap as their only food, and these diets are extremely limited in heritable symbiosis can expand ecological range and spur diversi- essential amino acids and some vitamins (6). Use of these un- fication, it also presents potential perils. balanced diets is possible because symbionts supply missing nutrients (7–10). Buchnera | aphid | Muller’s ratchet | selection levels | coevolution The macroevolutionary and ecological consequences of ac- quiring symbionts can be immense. Continuing with the same bligate symbiotic relationships shape the evolution of example, symbiont-dependent sap-feeding insects were among Opartner lineages. In symbioses that are mutually beneficial, the first herbivores to exploit vascular plants (11, 12) and include partners evolve traits that enable and stabilize the symbiosis: this highly successful clades such as aphids (5,000 described species), cooperative coevolution is emphasized in most studies of sym- whiteflies (1,600 species), psyllids (3,000 species), scale insects bioses. Genomic work has also revealed that obligate symbiosis (8,000 species), leafhoppers (>20,000 species), cicadas (2,500 produces unusual genome modifications, including extreme re- species), spittlebugs (3,000 species), and planthoppers (13,000 duction, rapid protein evolution, and codon reassignments, all of species) (11). All possess needle-like mouthparts, or stylets, used which are evident in ancient obligate symbionts of insects (1, 2). to access plant fluid and sap diets. These groups exhibit diverse Recent studies suggest that host genomes also have acquired plant–parasitic lifestyles and are critical players in terrestrial unusual modifications that are linked to symbiosis, including ecosystems as vectors of plant disease, food to diverse predators acquisition of genes from bacterial donors that seem to play a and parasites, and mutualists to other insects including ants. In role in controlling or supporting symbionts (3–5). Below, we each of these sap-feeding insect groups, phylogenetic analyses explore why lineages entering into obligate heritable symbiosis undergo strange patterns of genome evolution and display features that are difficult to interpret simply as adaptations for improving This paper results from the Arthur M. Sackler Colloquium of the National Academy of symbiotic function. We refer to the commitment to obligate, Sciences, “Symbioses Becoming Permanent: The Origins and Evolutionary Trajectories of “ ” Organelles,” held October 15–17, 2014, at the Arnold and Mabel Beckman Center of the inherited symbiosis as the evolutionary rabbit hole of obligate National Academies of Sciences and Engineering in Irvine, CA. The complete program and symbiosis, implying a generally irreversible journey into a very video recordings of most presentations are available on the NAS website at www.nasonline. odd world where the usual rules do not apply. org/Symbioses. Broadly, the symbiosis rabbit hole refers to the confluence of Author contributions: G.M.B. and N.A.M. designed research, performed research, ana- selection and neutral evolution in generating the extreme pat- lyzed data, and wrote the paper. terns of genomic evolution observed in symbiotic partners. As we The authors declare no conflict of interest. argue, these extremes are driven by three main forces: deleteri- This article is a PNAS Direct Submission. ous symbiont evolution due to genetic drift, within-host selection 1To whom correspondence should be addressed. Email: [email protected]. www.pnas.org/cgi/doi/10.1073/pnas.1421388112 PNAS | August 18, 2015 | vol. 112 | no. 33 | 10169–10176 Downloaded by guest on September 29, 2021 Symbiotic Coevolution as a Source of Genetic Incompatibility Fig. 1. Causes and consequences of symbiotic co- evolution. Mutations that negatively impact the Host & Symbiont Mutation Symbiosis Rabbit Hole Increased Genetic Incompatability symbiosis can be fixed through genetic drift due to Selfish Mutation Symbiont clonality and small population size (shown in blue) Acquisition or through within-host selection for selfish sym- bionts that favor their own fitness over that of the host (red). In response, the host is selected to buffer Deleterious Mutation these mutations (green), leading to a spiral down the symbiosis rabbit hole. This symbiont–host co- evolution may drive the rapid accumulation of ge- Insect Ancestor netic incompatibilities between host lineages and Host Compensatory between hosts and symbiont strains. Lineage-spe- Mutation cific symbiont–host coevolution may lead to accel- erated reproductive isolation and speciation, which could further reduce the effective size of geneti- cally compatible host populations. show that obligate symbionts have been vertically transmitted for aphids, cells that are specified to become bacteriocytes show millions of years, in many cases from the late Permian [>250 distinctive gene expression in early developmental stages, and Mya (million years ago)] (8, 10). The diversity and abundance of their cellular fate is determined before Buchnera colonization insects feeding on xylem or phloem sap reflect the dominance of (31, 32). Bacteriocyte expression of genes underlying amino acid vascular plants in terrestrial ecosystems: symbionts provided the metabolism complements Buchnera pathways for amino acid entry to a vast and expanding new niche that spread across the biosynthesis, reflecting extensive host–symbiont collaboration in globe. As a counterexample, the Coleorrhyncha, which resem- this central nutritional function (33–35). Certain aphid genes bles other sap-feeding groups in originating around the same seem to function solely in controlling or supporting Buchnera. time (the Permian) and having an obligate symbiont, contains For example, some highly expressed peptides are confined to only
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