Superparasitism Drives Heritable Symbiont Epidemiology and Host Sex Ratio in a Wasp

Abstract

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.

Mutual fitness benefits arise during coevolution in a nematode-defensive microbe model

“…However, it is increasingly known that many inherited bacteria can also transmit horizontally across host lineages (Parratt et al. ), and mechanisms of coadaptation have been well‐characterized in horizontally transmitted microbe‐host mutualisms, such as between squid and Vibrio fischeri (McFall‐Ngai and Ruby ; Nyholm and McFall‐Ngai ; Nyholm and Nishiguchi ; Collins et al. ).…”

Transitions in symbiosis: evidence for environmental acquisition & social transmission within a clade of heritable symbionts

“…Despite this dependence, many of these symbionts can also transmit horizontally (inter and intraspecifically) over evolutionary timescales [9][10][11]. However it is generally accepted that VT predominantly drives population dynamics [12], but see [13]. In contrast, exclusively horizontally acquired symbionts must be transmitted to new hosts via infected con-/heterospecifics or environmental reservoirs [14,15].…”

Reproduction of Trichospilus diatraeae (Hymenoptera: Eulophidae) with Different Densities and Parasitism Periods in Anticarsia gemmatalis (Lepidoptera: Noctuidae) Pupae

“…In the present work the densities and time provided more than 85% of females in all treatments. Densities above those recommended may cause superparasitism, and consequently host contact through superparasitism is necessary for the symbiont's spread in populations of its primary host N. vitripennis, such that when superparasitism rates are high, the symbiont causes highly female biased population sex ratios and consequently causes local host extinction (PARRATT et al 2016).…”