Experimental replacement of an obligate insect symbiont

Moran, Nancy A.; Yao, Yun

doi:10.1073/pnas.1420037112

Cited by 118 publications

(103 citation statements)

References 28 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…A further prediction, and one that might be tested more readily, is that reproductive isolation in insects with symbionts will often be enforced by incompatibilities between host and symbiont loci or between different host loci that contribute to the regulation, support, and transmission of symbionts. Understanding the role of symbiosis in generating reproductive isolation can be approached through experimental investigations of symbiosis using hybridization or transfection to produce novel host-symbiont combinations (78).…”

Section: Consequences Of Symbiosis For Host Evolutionmentioning

confidence: 99%

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

Bennett

Moran

2015

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

432

515

View full text Add to dashboard Cite

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 sapfeeding 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 aphidBuchnera symbiosis and related systems illustrate that, whereas heritable symbiosis can expand ecological range and spur diversification, it also presents potential perils.Buchnera | aphid | Muller's ratchet | selection levels | coevolution

show abstract

Section: Consequences Of Symbiosis For Host Evolutionmentioning

confidence: 99%

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

Bennett

Moran

2015

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

432

515

View full text Add to dashboard Cite

show abstract

“…In aphids and other insects, defensive symbionts can sweep through populations and be horizontally transferred to new hosts (31,32). Even Buchnera, a vertically transferred obligate symbiont of aphids, still confers its benefits to new hosts after experimental infection (33). Taken together, this horizontal transfer suggests that little coevolution may be needed for the formation of novel symbiosis.…”

Section: Significancementioning

confidence: 99%

Burkholderia bacteria infectiously induce the proto-farming symbiosis of Dictyostelium amoebae and food bacteria

DiSalvo

Haselkorn

Bashir

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

104

239

View full text Add to dashboard Cite

Symbiotic associations can allow an organism to acquire novel traits by accessing the genetic repertoire of its partner. In the Dictyostelium discoideum farming symbiosis, certain amoebas (termed “farmers”) stably associate with bacterial partners. Farmers can suffer a reproductive cost but also gain beneficial capabilities, such as carriage of bacterial food (proto-farming) and defense against competitors. Farming status previously has been attributed to amoeba genotype, but the role of bacterial partners in its induction has not been examined. Here, we explore the role of bacterial associates in the initiation, maintenance, and phenotypic effects of the farming symbiosis. We demonstrate that two clades of farmer-associated Burkholderia isolates colonize D. discoideum nonfarmers and infectiously endow them with farmer-like characteristics, indicating that Burkholderia symbionts are a major driver of the farming phenomenon. Under food-rich conditions, Burkholderia-colonized amoebas produce fewer spores than uncolonized counterparts, with the severity of this reduction being dependent on the Burkholderia colonizer. However, the induction of food carriage by Burkholderia colonization may be considered a conditionally adaptive trait because it can confer an advantage to the amoeba host when grown in food-limiting conditions. We observed Burkholderia inside and outside colonized D. discoideum spores after fruiting body formation; this observation, together with the ability of Burkholderia to colonize new amoebas, suggests a mixed mode of symbiont transmission. These results change our understanding of the D. discoideum farming symbiosis by establishing that the bacterial partner, Burkholderia, is an important causative agent of the farming phenomenon.

show abstract

“…A model for symbiont studies, the aphid-Buchnera aphidicola symbiosis, can be disrupted through exposing the insects to both high (Wilcox et al, 2003;Dunbar et al, 2007) or low temperatures (Parish and Bale, 1991) as the symbiont populations decrease. Indeed, interclonal variation in the thermal sensitivity of aphids is associated with variation in Buchnera, with a singlenucleotide deletion in the heat shock promoter region of the heat shock gene ibpA being associated with reduced tolerance to thermal stress, but improved fitness at normal environmental temperatures (Dunbar et al, 2007;Moran and Yun, 2015). In field cages, aphid clones carrying the reduced heat tolerance strain of Buchnera outcompete clones carrying the tolerant strain at low temperatures, but these clones are outcompeted where heat shocks occur (Harmon et al, 2009).…”

Section: Obligate Heritable Microbes Commonly Represent a Thermal 'Wementioning

confidence: 99%

Heritable symbionts in a world of varying temperature

et al. 2016

View full text Add to dashboard Cite

Heritable microbes represent an important component of the biology, ecology and evolution of many plants, animals and fungi, acting as both parasites and partners. In this review, we examine how heritable symbiont-host interactions may alter host thermal tolerance, and how the dynamics of these interactions may more generally be altered by thermal environment. Obligate symbionts, those required by their host, are considered to represent a thermally sensitive weak point for their host, associated with accumulation of deleterious mutations. As such, these symbionts may represent an important determinant of host thermal envelope and spatial distribution. We then examine the varied relationship between thermal environment and the frequency of facultative symbionts that provide ecologically contingent benefits or act as parasites. We note that some facultative symbionts directly alter host thermotolerance. We outline how thermal environment will alter the benefits/costs of infection more widely, and additionally modulate vertical transmission efficiency. Multiple patterns are observed, with symbionts being cold sensitive in some species and heat sensitive in others, with varying and non-coincident thresholds at which phenotype and transmission are ablated. Nevertheless, it is clear that studies aiming to predict ecological and evolutionary dynamics of symbiont-host interactions need to examine the interaction across a range of thermal environments. Finally, we discuss the importance of thermal sensitivity in predicting the success/failure of symbionts to spread into novel species following natural/engineered introduction.

show abstract

Experimental replacement of an obligate insect symbiont

Cited by 118 publications

References 28 publications

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

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

Burkholderia bacteria infectiously induce the proto-farming symbiosis of Dictyostelium amoebae and food bacteria

Heritable symbionts in a world of varying temperature

Contact Info

Product

Resources

About