Heritable microbial symbionts have profound impacts upon the biology of their arthropod hosts. Whilst our current understanding of the dynamics of these symbionts is typically cast within a framework of vertical transmission only, horizontal transmission has been observed in a number of cases. For instance, several symbionts can transmit horizontally when their parasitoid hosts share oviposition patches with uninfected conspecifics, a phenomenon called superparasitism. Despite this, horizontal transmission, and the host contact structures that facilitates it, have not been considered in heritable symbiont epidemiology. Here, we tested for the importance of host contact, and resulting horizontal transmission, for the epidemiology of a male-killing heritable symbiont (Arsenophonus nasoniae) in parasitoid wasp hosts. We observed that host contact through superparasitism is necessary for this symbiont’s spread in populations of its primary host Nasonia vitripennis, such that when superparasitism rates are high, A. nasoniae almost reaches fixation, causes highly female biased population sex ratios and consequently causes local host extinction. We further tested if natural interspecific variation in superparasitism behaviours predicted symbiont dynamics among parasitoid species. We found that A. nasoniae was maintained in laboratory populations of a closely related set of Nasonia species, but declined in other, more distantly related pteromalid hosts. The natural proclivity of a species to superparasitise was the primary factor determining symbiont persistence. Our results thus indicate that host contact behaviour is a key factor for heritable microbe dynamics when horizontal transmission is possible, and that ‘reproductive parasite’ phenotypes, such as male-killing, may be of secondary importance in the dynamics of such symbiont infections.

READMEReadmMe containing details of associated data filesData_S1infection prevalence and sex ratio through eight generations. Used to produce Figure_1, Figure_2 and Table_1S1_Dataset.xlsxData_S2Population viability through time. Used for Figure_3S2_Dataset.xlsxData_S3Infection prevalence at generation 4 for populations of N.vitripennis kept at variable opportunities to super parasitise. Used for Figure_4.S3_Dataset.xlsxData_S4Multiple host species infection dynamics: Used in Figure 5S4_Dataset.xlsxData_S5Vertical transmission efficiency of Arsenophonus nasoniae in five species of parasitoid wasps. Data collected after two generations of passage following Arsenophonus introduction. Used for Figure 6S5_Dataset.xlsxData_S6Cost of Arsenophonus nasoniae infection in multiple species: Data collected from 4 of 5 species after two generations of passage following Arsenophonus introduction. Used for Figure 7S6_Dataset.xlsxData S7Male killing efficiency of Arsenophonus strain CAN1 in host wasp Nasonia vitripennisData S8Male killing efficiency of Arsenophonus nasonaie strain UK1 in multiple host wasp species.Data S9Superparasitism intensity of Nasonia vitripennis at varying wasp and host densities.