Variation in the Obligate Symbionts of Aphids

Abstract

Intimate, mutualistic, association with microbes is a common mechanism for organisms to utilize certain niches. Insects are a particularly well-studied group in this respect, frequently forming long-term, obligate associations with symbiotic microbes. These symbioses are often nutritional in nature, with the symbiont providing the host with nutrients that are otherwise unavailable. Aphids are notable for their well-defined relationship with the symbiotic Bacteria Buchnera aphidicola. By synthesizing the amino acids the aphid is unable to produce itself, Buchnera permits its host to feed on plant phloem, which lacks sufficient quantities of these essential nutrients. Buchnera, as with many obligate intracellular symbionts, has a reduced effective population size (Nₑ) due to asexual reproduction and severe population bottlenecks experienced during transmission between generations. The reduction in Nₑ has facilitated the degradation of the symbiont genome through fixation of deleterious mutations via drift. The consequences of accelerated evolutionary rates has been examined primarily through genome sequencing and comparative studies of symbionts from different host species. The work detailed in this dissertation examines the role of deleterious mutations and drift at multiple taxonomic levels. Analysis of aphid amino acid requirements utilizing an artificial diet assay revealed variation in clones of the pea aphid, Acyrthosiphon pisum. In one clone, a mutation in the arginine biosynthesis pathway appears to underlie a host dietary requirement for arginine. Examination of the number of Buchnera within an A. pisum clone also revealed variation in symbiont titer between clones. When compared across F₁ offspring of cross between a low- and a high-titer clone, extensive variation was observed in titer that exceeded variation observed in field-collected clones. No maternal effects were observed, suggesting that Buchnera is not in control of its replication. At a broader taxonomic scale, the replacement of Buchnera in the aphid Cerataphis brasiliensis was examined by sequencing the genome of its fungal symbiont (YLS). The genome of the YLS revealed a much greater metabolic capacity than Buchnera, possibly due to its extracellular habitat. The YLS exhibited signatures of elevated evolutionary rates and intron gain consistent with a reduction in Nₑ due to its symbiotic niche.