Male-killing symbiosis across a predator-prey interaction: a genomic and experimental approach

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Most insects carry specialised bacteria that dwell permanently inside them. These bacteria are known as symbionts and may be beneficial or costly to their insect host. In this project, we will investigate a bacterial symbiont, Spiroplasma, that is able to manipulate host insect reproduction to its own advantage.Like many insect symbionts, Spiroplasma is predominantly transmitted from female insects to their offspring. Because males cannot transmit the bacteria, they are essentially an evolutionary 'dead end' from the perspective of the symbiont. Symbionts are therefore under selection to increase the proportion of female offspring, and the result is a diversity of symbiont-induced reproductive manipulation strategies. Spiroplasma employs one of the most straightforward: male offspring carrying the symbiont die before adulthood (usually in the egg stage). This is assumed to benefit the surviving sisters, although the advantages are not always clear.In addition to maternal transmission, symbionts can occasionally be transmitted between unrelated individuals, either within or between species. This 'horizontal' transmission is evolutionarily important because it is a route for heritable characteristics to be passed across species boundaries in animals. However, since such transfers are rare in nature, we know little about the process. In this project, we will study two closely-related groups of Spiroplasma, infecting ladybirds and aphids respectively, in order to ask what happens when symbionts move between distantly-related insects.First, we will sequence the genomes of 13 strains of Spiroplasma bacteria: three from different species of ladybirds, and 10 from the pea aphid. The pea aphid strains will include bacteria causing complete, partial and no death of male offspring. We will use the genomes to look for similarities and differences among the Spiroplasma strains in the putative genetic mechanism for male-killing. We also aim to identify the genetic variation that drives the phenotypic differences in male-killing seen among the aphid Spiroplasma. In the second part of the project, we will recreate a likely route of symbiont transmission. Ladybirds are well-known as predators of aphids, and it is highly plausible that this predator-prey relationship allowed transmission of Spiroplasma between the two groups in their evolutionary past. We will carry out microinjection of body fluid containing male-killing Spiroplasma from aphids to ladybirds, and vice versa. We will test whether a new heritable infection is established and if the new infections cause male-killing. Our study combines an ambitious plan to recreate cross-species symbiont transmission with a detailed understanding of mechanism through symbiont genome sequencing. Ladybirds and aphids present a great opportunity to understand horizontal acquisition of traits via horizontal transmission of symbionts, and also to investigate the barriers that may stand in the way of that transfer. By gaining a full picture of symbiont function and transmission in the context of one specific predator-prey interaction, we will open the way to answer further questions surrounding the acquisition of novel symbionts, and the evolution of symbiont-mediated effects. Insects are an extraordinary evolutionary success story. Hidden inside insects, bacterial symbionts play important roles in nutrition, defence and reproduction. Explaining how and why new symbiotic associations arise is therefore a vital element for understanding insect evolution, and is the overarching aim of the project we propose.