Deep data mining reveals variable abundance and distribution of microbial reproductive manipulators within and among diverse host species

Abstract

Bacterial symbionts that manipulate the reproduction of their hosts are important factors in invertebrate ecology and evolution, and are being leveraged for host biological control. Infection prevalence restricts which biological control strategies are possible and is thought to be strongly influenced by the density of symbiont infection within hosts, termed titer. Current methods to estimate infection prevalence and symbiont titers are low-throughput, biased towards sampling infected species, and rarely measure titer. Here we develop a data mining approach to estimate symbiont infection frequencies within host species and titers within host tissues. We applied this approach to screen ~32,000 publicly available sequence samples from the most common symbiont host taxa, discovering 2,083 arthropod and 119 nematode infected samples. From these data, we estimated that Wolbachia infects approximately 44% of all arthropod and 34% of all nematode species, while other reproductive manipulators only infect 1-8% of arthropod and nematode species. Although relative titers within hosts were highly variable within and between arthropod species, a combination of arthropod host species and Wolbachia strain explained approximately 36% of variation in Wolbachia titer across the dataset. To explore potential mechanisms for host control of symbiont titer, we leveraged population genomic data from the model system Drosophila melanogaster. In this host, we found a number of SNPs associated with titer in candidate genes potentially relevant to host interactions with Wolbachia. Our study demonstrates that data mining is a powerful tool to detect bacterial infections and quantify infection intensities, thus opening an array of previously inaccessible data for further analysis in host-symbiont evolution.