Aphid Heritable Symbiont Exploits Defensive Mutualism

Abstract

Insects and other animals commonly form symbioses with heritable bacteria, which can exert large influences on host biology and ecology. The pea aphid, Acyrthosiphon pisum, is a model for studying effects of infection with heritable facultative symbionts (HFS), and each of its seven common HFS species has been reported to provide resistance to biotic or abiotic stresses. However, one common HFS, called X-type, rarely occurs as a single infection in field populations and instead typically superinfects individual aphids with Hamiltonella defensa, another HFS that protects aphids against attack by parasitic wasps. Using experimental aphid lines comprised of all possible infection combinations in a uniform aphid genotype, we investigated whether the most common strain of X-type provides any of the established benefits associated with aphid HFS as a single infection or superinfection with H. defensa. We found that X-type does not confer protection to any tested threats, including parasitoid wasps, fungal pathogens, or thermal stress. Instead, component fitness assays identified large costs associated with X-type infection, costs which were ameliorated in superinfected aphids. Together these findings suggest that X-type exploits the aphid/H. defensa mutualism and is maintained primarily as a superinfection by "hitchhiking" via the mutualistic benefits provided by another HFS. Exploitative symbionts potentially restrict the functions and distributions of mutualistic symbioses with effects that extend to other community members.IMPORTANCE Maternally transmitted bacterial symbionts are widespread and can have major impacts on the biology of arthropods, including insects of medical and agricultural importance. Given that host fitness and symbiont fitness are tightly linked, inherited symbionts can spread within host populations by providing beneficial services. Many insects, however, are frequently infected with multiple heritable symbiont species, providing potential alternative routes of symbiont maintenance. Here we show that a common pea aphid symbiont called X-type likely employs an exploitative strategy of hitchhiking off the benefits of a protective symbiont, Hamiltonella. Infection with X-type provides none of the benefits conferred by other aphid symbionts and instead results in large fitness costs, costs lessened by superinfection with Hamiltonella. These findings are corroborated by natural infections in field populations, where X-type is mostly found superinfecting aphids with Hamiltonella. Exploitative symbionts may be common in hosts with communities of heritable symbionts and serve to hasten the breakdown of mutualisms.KEYWORDS Hamiltonella defensa, PAXS, entomopathogenic fungi, heat stress, heritable symbionts, parasitoids, pea aphid resistance H eritable bacterial symbionts are ubiquitous in arthropod species, especially insects occupying terrestrial ecosystems (1). These heritable symbionts are usually maternally transmitted and cannot survive outside host tissues and consequently have limited s...

Nonrandom associations of maternally transmitted symbionts in insects: The roles of drift versus biased cotransmission and selection

“…Field observations are also informative when they do not match the expectations from laboratory work. For example, laboratory experiments suggested that X‐Type does not provide any detectable benefit to the pea aphid, but it is quite frequent and positively associated to H. defensa , suggesting it might have benefited from hitchhiking during the spread of H. defensa (Doremus & Oliver, ). Also, Wulff, Buckman, Wu, Heimpel, and White () did not find that the symbiont Arsenophonus was protecting its Aphis glycines host against its main parasites, but it was present at high frequency.…”

Breakdown of a defensive symbiosis, but not endogenous defences, at elevated temperatures

“…We also examined one strain of the HFS X‐type and three H. defensa strains carrying different APSE phage types with varying effects on the protective phenotype at 20°C. Specifically, in prior work, strains carrying APSE2 (82B) and APSE8 (5D) confer moderate resistance (Doremus & Oliver, ; Oliver et al., ), while those associating with APSE3 (A1A) confer high levels of protection (Oliver et al., ). Experimental lines were created using microinjection or selective antibiotic curing, establishing genetically identical aphid stocks varying only with respect to their harboured HFS (Douglas, Francois, & Minto, ).…”

“…However, neither of these studies disentangled effects of host genotype, which was later shown to contribute to resistance to parasitoids (Martinez, Ritter et al., ). A recent study using North American pea aphids found that a common X‐type strain does not confer protection against another braconid parasitoid, Praon pequodourm (or heat shock) either as a single or co‐infection with H. defensa (Doremus & Oliver, ), but this study did not examine interactions with the dominant parasitoid A. ervi or incorporate parasitism assays at higher temperatures. Hence, the impacts of temperature on H. defensa ‐mediated defence, and the abilities of co‐infecting symbionts to rescue heat‐induced detriments, remain uncertain.…”

“…Much of this variation depends on infection with different strains of the HFS Hamiltonella defensa and its associated bacteriophages called APSEs (Oliver, Degnan, Hunter, & Moran, ; Oliver, Moran, & Hunter, ). Three major APSE variants (APSE2, 3 & 8) have been reported in North American pea aphid populations (Degnan & Moran, ; Doremus & Oliver, ; Martinez, Weldon, & Oliver, ; Moran, Degnan, Santos, Dunbar, & Ochman, ), and in laboratory studies, aphids carrying strains of H. defensa with APSE3 receive high to complete protection. In contrast, those with APSE2 and APSE8 bearing H. defensa receive moderate protection, while those with phage‐free H. defensa are highly susceptible (Doremus & Oliver, ; Oliver & Moran, ; Oliver et al., ).…”

“…Three major APSE variants (APSE2, 3 & 8) have been reported in North American pea aphid populations (Degnan & Moran, ; Doremus & Oliver, ; Martinez, Weldon, & Oliver, ; Moran, Degnan, Santos, Dunbar, & Ochman, ), and in laboratory studies, aphids carrying strains of H. defensa with APSE3 receive high to complete protection. In contrast, those with APSE2 and APSE8 bearing H. defensa receive moderate protection, while those with phage‐free H. defensa are highly susceptible (Doremus & Oliver, ; Oliver & Moran, ; Oliver et al., ). Additionally, some aphid clones lacking HFS possess endogenous resistance to A. ervi (Martinez, Ritter et al., ).…”