Nancy A. Moran^a,¹ and Yueli Yun^a,^b

EVOLUTION

Significance

In many invertebrates, development depends on obligate bacterial symbionts that are confined to specialized host cells and are transmitted directly from mother to progeny. A primary model for this kind of symbiosis is the Buchnera/pea aphid association, which has been maintained for more than 100 million years through strict maternal transmission. The intimacy of this symbiosis has thwarted experiments aimed at dissecting how symbiont and host genotypes contribute to overall phenotype and ecological tolerances. Using a selectable Buchnera phenotype combined with microinjection, we successfully replaced Buchnera within a matriline, thus generating matrilines with identical aphid genotypes but distinct Buchnera genotypes. Buchnera replacement dramatically increased heat tolerance of the aphid matriline, demonstrating directly that symbiont genotype can affect host ecology.

Abstract

Symbiosis, the close association of unrelated organisms, has been pivotal in biological diversification. In the obligate symbioses found in many insect hosts, organisms that were once independent are permanently and intimately associated, resulting in expanded ecological capabilities. The primary model for this kind of symbiosis is the association between the bacterium Buchnera and the pea aphid (Acyrthosiphon pisum). A longstanding obstacle to efforts to illuminate genetic changes underlying obligate symbioses has been the inability to experimentally disrupt and reconstitute symbiont–host partnerships. Our experiments show that Buchnera can be experimentally transferred between aphid matrilines and, furthermore, that Buchnera replacement has a massive effect on host fitness. Using a recipient pea aphid matriline containing Buchnera that are heat sensitive because of an allele eliminating the heat shock response of a small chaperone, we reduced native Buchnera through heat exposure and introduced a genetically distinct Buchnera from another matriline, achieving complete replacement and stable inheritance. This transfer disrupted 100 million years (∼1 billion generations) of continuous maternal transmission of Buchnera in its host aphids. Furthermore, aphids with the Buchnera replacement enjoyed a dramatic increase in heat tolerance, directly demonstrating a strong effect of symbiont genotype on host ecology.

See: http://www.pnas.org/content/112/7/2093.abstract.html?etoc

PNAS February 17 2015; vol.112; no.7 2093-2096

Fig. 1.

Experimental approach for replacement of the native Buchnera symbionts within an A. pisum matriline. The recipient line (LSR1) contains a heat-sensitive Buchnera genotype, and the donor (5AY) contains a heat-tolerant Buchnera genotype. Native Buchnera are depleted by heat in the recipient line, and microinjection is used to flood the hemocoel with donor Buchnera. Most embryos are successfully colonized by the donor symbionts. In some cases, complete replacement occurs in the progeny of injected females. In other cases, progeny have a mixed Buchnera population, which can be shifted completely to the donor type through further heat exposure.