Coevolution and consequences of symbioses between aphids and maternally transmitted bacteria

Abstract

Symbiosis is a prevalent phenomenon among organisms throughout the tree of life, including the insects which often harbor maternally transmitted bacteria. Aphids engage in symbiotic interactions with several maternally transmitted bacteria, and many are known to associate with microbes known as secondary symbionts. These bacteria are typically not essential from the aphid's perspective, and until recently little was known about their roles in aphid biology or the coevolutionary histories of these symbioses. I have addressed these mysteries in this dissertation, through use of molecular and experimental analyses. My findings reveal that secondary symbionts are diverse and infect members of numerous aphid and insect taxa. Though they are maternally transmitted, their distributions can be attributed to occasional horizontal transmission among species. Consequences of symbiosis were observed at genomic levels, with "T-" and "U-type" symbionts exhibiting accelerated evolution in their 16S rRNA sequences. The "R-type" symbiont, in contrast, has not experienced accelerated substitution rates, though it does show a recent trend toward increased AT content, as observed for other symbiotic bacteria. Molecular and phylogenetic evidence presented in this dissertation suggest that secondary symbionts are generalists, capable of infecting numerous aphid hosts. Here, I also present experimental evidence in support of this hypothesis, demonstrating that two of three horizontally transferred symbionts are passed on maternally, at high efficiency, in a novel host, Acyrthosiphon pisum. However, not all efficiently transmitted symbionts would be expected to persist in populations of A. pisum, as some reduce aphid fitness. Finally, evidence obtained from my research and previous experimental and theoretical studies suggests that secondary symbionts should improve aphid fitness, though benefits may not accrue in all environments. Here, I examine the effects of temperature on the fitness effects induced by R-, T-, and U-type symibionts, finding that the R- and T-types confer benefits in aphids exposed to high temperatures, compared to slight and even non-existent effects on A. pisum reared under permissive temperatures. The U-type reduced fitness of aphids reared under high temperatures, revealing a potential cost to symbiont infection that could help to explain intermediate infection frequencies.