Parasitoids as vectors of facultative bacterial endosymbionts in aphids

Abstract

Heritable bacterial endosymbionts play an important role in aphid ecology. Sequence-based evidence suggests that facultative symbionts such as Hamiltonella defensa or Regiella insecticola also undergo horizontal transmission. Other than through male-to-female transfer during the sexual generation in autumn, the routes by which this occurs remain largely unknown. Here, we tested if parasitoids or ectoparasitic mites can act as vectors for horizontal transfer of facultative symbionts. Using symbiont-specific primers for diagnostic PCR, we demonstrate for the first time, to our knowledge, that parasitoids can indeed transfer H. defensa and R. insecticola by sequentially stabbing infected and uninfected individuals of their host, Aphis fabae, establishing new, heritable infections. Thus, a natural route of horizontal symbiont transmission is also available during the many clonal generations of the aphid life cycle. No transmissions by ectoparasitic mites were observed, nor did parasitoids that emerged from symbiont-infected aphids transfer any symbionts in our experiments.

Experimental replacement of an obligate insect symbiont

“…Many facultative symbionts are readily transferred between hosts in the laboratory, and such transfers have been a critical tool in the experimental identification of symbiont-based traits while controlling for host genetic background (8,(15)(16)(17)(18)(19). This ease of transferring facultative symbionts might be expected, as they undergo horizontal transfer in natural populations via several mechanisms (20)(21)(22), and their genomes encode machinery such as type III secretion systems, known to enable invasion of eukaryotic cells (9,10). In contrast, exclusively maternally transmitted, obligate symbionts, such as Buchnera, are never faced with the challenge of invading new matrilines.…”

Phenotypic Effect of “Candidatus Rickettsiella viridis,” a Facultative Symbiont of the Pea Aphid (Acyrthosiphon pisum), and Its Interaction with a Coexisting Symbiont

“…If we assume an initial population with only single Rickettsiella or Hamiltonella infections, horizontal transfer of either of these symbionts would be essential to generate multiple infections. Recent experimental studies have shown that Hamiltonella undergoes horizontal transmission during sexual reproduction (13) or by parasitoid vectors (14). Therefore, the high prevalence of coinfection may reflect the high horizontal transfer rate of Hamiltonella.…”

“…Moreover, A. pisum often harbors one or several additional, facultatively symbiotic bacteria, including Serratia symbiotica, Hamiltonella defensa, Regiella insecticola, a Rickettsia sp., a Spiroplasma sp., and others (8)(9)(10)(11)(12). These facultative symbionts are not essential for host growth and reproduction and are subjected mostly to vertical transmission, although they are occasionally transmitted horizontally (4,13,14). Notably, some of these facultative symbionts have conditionally beneficial fitness consequences for the host, including resistance to parasitoid wasps or pathogenic fungi (Hamiltonella, Serratia, or Regiella) (15)(16)(17), tolerance to heat stress (Serratia) (18,19), or broadening of the food plant range (Regiella) (20,21).…”

Novel Endosymbioses as a Catalyst of Fast Speciation

“…However, since in many cases, there is no concordance between the phylogeny of bacteria and their hosts, and there is indication of horizontal transmission (Vavre et al 1999;Thao et al 2000;Russell et al 2003;Ahmed et al 2013). It is conceivable that in an environment inhabited by organisms infected and non-infected with bacteria, given enough time, high densities and reiterated contacts, the probability of horizontal transmission of symbionts is not negligible (Gehrer and Vorburger 2012;Le Clec'h et al 2013). Moreover, several studies have demonstrated that some microbial symbionts retain a generalized ability to infect multiple hosts (Schilthuizen and Stouthamer 1997;Heath et al 1999;Huigens et al 2004;Duron et al 2010).…”