Are island plants really poorly defended? No support for the loss of defense hypothesis in domatia-bearing plants

The loss of defense hypothesis posits that island colonizers experience a release from predation on the mainland and subsequently lose their defensive adaptations. While support for the hypothesis is abundant, it has never been tested in domatia-bearing plants. Leaf domatia are cave-like structures produced on the underside of leaves that facilitate a defensive mutualism with predatory and fungivorous mites. I tested the loss of defense hypothesis in six domatia-bearing taxa inhabiting New Zealand and its offshore islands. No support for the loss of defense hypothesis was found. Changes in domatia investment were instead associated with changes in leaf size; a trait that has been repeatedly observed to undergo rapid evolution on islands. Overall results demonstrate that not all types of defense are lost on islands, suggesting a higher-resolution approach is needed when studying the evolution of defense on islands.

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.

Fungal endophytes of Festuca rubra increase in frequency following long-term exclusion of rabbits

Plant – fungal endophyte interactions are common in nature and they can shape the ecology of plants. Vertically transmitted endophytes are hypothesized to serve as mutualists, protecting plants from herbivores. If this hypothesis is true, then we expect endophytes to be most abundant in the presence of herbivores and least abundant in their absence, assuming endophytes incur a cost to their host. We tested this prediction by studying the effects of intense rabbit (Oryctolagus cuniculus Linnaeus) grazing on grass–endophyte interactions at Silwood Park, UK. We examined seeds of red fescue (Festuca rubra L.) collected from 15 natural populations that were protected from rabbits for 0.3–21 years. Contrary to our prediction, the mean proportion of seeds with endophytes increased 1.84×, from 0.45 to 0.83, following 21 years of rabbit exclusion. To better understand the mechanisms driving this increase in frequency, we conducted a fully factorial greenhouse experiment where we manipulated the presence or absence of endophyte infection, intraspecific competition, and simulated grazing on F. rubra plants. In both damaged and undamaged treatments, infected plants produced approximately twice as much biomass as uninfected plants, and endophytes did not influence tolerance to herbivory. These results suggest that endophytes directly change plant growth but not compensatory responses to damage. In the absence of competitors, infected plants produced 2.17× more biomass than uninfected plants, whereas in the presence of competitors, infected plants produced only 1.55× more biomass than uninfected plants. This difference suggests that intraspecific competition might lessen the benefits of endophyte infection. Our results do not support the defensive mutualism hypothesis, but instead suggest that endophyte-induced plant growth is important in shaping the costs and benefits of endophytes in our system.