Defensive nymphs in the water-repellent gall of the social aphid Colophina monstrifica (Hemiptera: Aphididae: Eriosomatinae)

The aphid Colophina monstrifica forms woolly colonies with sterile soldiers on the secondary host Clematis uncinata in Taiwan. However, the gall or primary-host generation of C. monstrifica has not been found to date. We successfully induced galls of the species on trees of Zelkova serrata through attaching its eggs onto the trees, and also found a few naturally formed galls on another Z. serrata tree. The identity of the aphids was confirmed by examining their morphology and mitochondrial DNA sequences. First- and second-instar nymphs in the galls exhibited attacking behavior toward artificially introduced moth larvae. Observations with a scanning electron microscope revealed that the gall inner surface was densely covered with minute trichomes. This indicates the water repellency of the inner surface, and strongly suggests that young nymphs of C. monstrifica dispose of honeydew globules outside the gall, as known in the congener C. clematis.

Evolution and maintenance of microbe-mediated protection under occasional pathogen infection

Every host is colonized by a variety of microbes, some of which can protect their hosts from pathogen infection. However, pathogen presence naturally varies over time in nature, such as in the case of seasonal epidemics. We experimentally coevolved populations of Caenorhabditis elegans worm hosts with bacteria possessing protective traits (Enterococcus faecalis), in treatments varying the infection frequency with pathogenic Staphylococcus aureus every host generation, alternating host generations, every fifth host generation or never. We additionally investigated the effect of initial pathogen presence at the formation of the defensive symbiosis. Our results show that enhanced microbe-mediated protection evolved during host-protective microbe coevolution when faced with rare infections by a pathogen. Initial pathogen presence had no effect on the evolutionary outcome of microbe-mediated protection. We also found that protection was only effective at preventing mortality during the time of pathogen infection. Overall, our results suggest that resident microbes can be a form of transgenerational immunity against rare pathogen infection.

The role of multilevel selection in host microbiome evolution

Animals are associated with a microbiome that can affect their reproductive success. It is, therefore, important to understand how a host and its microbiome coevolve. According to the hologenome concept, hosts and their microbiome form an integrated evolutionary entity, a holobiont, on which selection can potentially act directly. However, this view is controversial, and there is an active debate on whether the association between hosts and their microbiomes is strong enough to allow for selection at the holobiont level. Much of this debate is based on verbal arguments, but a quantitative framework is needed to investigate the conditions under which selection can act at the holobiont level. Here, we use multilevel selection theory to develop such a framework. We found that selection at the holobiont level can in principle favor a trait that is costly to the microbes but that provides a benefit to the host. However, such scenarios require rather stringent conditions. The degree to which microbiome composition is heritable decays with time, and selection can only act at the holobiont level when this decay is slow enough, which occurs when vertical transmission is stronger than horizontal transmission. Moreover, the host generation time has to be short enough compared with the timescale of the evolutionary dynamics at the microbe level. Our framework thus allows us to quantitatively predict for what kind of systems selection could act at the holobiont level.

The role of multilevel selection in host microbiome evolution

Animals are associated with a microbiome that can affect their reproductive success. It is therefore important to understand how a host and its microbiome coevolve. According to the hologenome concept, hosts and their microbiome form an integrated evolutionary entity, a holobiont, on which selection can potentially act directly. However, this view is controversial and there is an active debate on whether the association between hosts and their microbiomes is strong enough to allow for selection at the holobiont level. Much of this debate is based on verbal arguments, but a quantitative framework is needed to investigate the conditions under which selection can act at the holobiont level. Here we use multilevel selection theory to develop such a framework. We found that selection at the holobiont level can in principle favor a trait that is costly to the microbes but that provides a benefit to the host. However, such scenarios require rather stringent conditions. The degree to which microbiome composition is heritable decays with time, and selection can only act at the holobiont level when this decay is slow enough, which occurs when vertical transmission is stronger than horizontal transmission. Moreover, the host generation time has to be short enough compared to the timescale of the evolutionary dynamics at the microbe level. Our framework thus allows us to quantitatively predict for what kind of systems selection could act at the holobiont level.

Characterization of Phytophthora nicotianae Resistance Conferred by the Introgressed Nicotiana rustica Region, Wz, in Flue-Cured Tobacco

Black shank, caused by Phytophthora nicotianae, is one of the most important diseases affecting tobacco worldwide and is primarily managed through use of host resistance. An additional source of resistance to P. nicotianae, designated as Wz, has been introgressed into Nicotiana tabacum from N. rustica. The Wz gene region confers high levels of resistance to all races, but has not been characterized. Our study found Wz-mediated resistance is most highly expressed in the roots, with only a slight reduction in stem-lesion size in Wz genotypes compared with susceptible controls. No substantial relationships were observed between initial inoculum levels and disease development on Wz genotypes, which is generally consistent with qualitative or complete resistance. Isolates of P. nicotianae adapted for five host generations on plants with the Wz gene caused higher disease severity than isolates adapted on Wz plants for only one host generation. Wz-adapted isolates did not exhibit increased aggressiveness on genotypes with other sources of partial resistance, suggesting pathogen adaptation was specific to the Wz gene. To reduce potential for pathogen population shifts with virulence on Wz genotypes, Wz should be combined with other resistance sources and rotation of varying black shank resistance mechanisms is also recommended.

Widespread Negative Frequency-Dependent Selection Maintains Diversity in the Legume-Rhizobia Symbiosis: Balancing nodulation may explain the paradox of rhizobium diversity

The evolutionary origin and ecological maintenance of biodiversity is a central problem in biology. For diversity to be stable through time, each genotype or species must have an advantage when rare. This negative frequency-dependence prevents deterministic extinction and mitigates the stochastic loss of diversity (1–4). However, models of mutualism typically generate positive frequency-dependence that reduces diversity (5–8). Here, we report empirical evidence for negative frequency-dependence in the legume-rhizobium mutualism within a single host generation, a phenomenon that we term balancing nodulation. Balancing nodulation increases rare rhizobia across all 13 legume genera investigated to date, at high and low inoculum densities, and with minimal genetic differentiation between rhizobia strains. While the mechanism generating this phenomenon is currently unknown, balancing nodulation could actively maintain variation in the rhizobia-legume symbiosis.

Defying Muller’s Ratchet: Ancient Heritable Endobacteria Escape Extinction through Retention of Recombination and Genome Plasticity

ABSTRACT Heritable endobacteria, which are transmitted from one host generation to the next, are subjected to evolutionary forces that are different from those experienced by free-living bacteria. In particular, they suffer consequences of Muller’s ratchet, a mechanism that leads to extinction of small asexual populations due to fixation of slightly deleterious mutations combined with the random loss of the most-fit genotypes, which cannot be recreated without recombination. Mycoplasma-related endobacteria (MRE) are heritable symbionts of fungi from two ancient lineages, Glomeromycota (arbuscular mycorrhizal fungi) and Mucoromycotina . Previous studies revealed that MRE maintain unusually diverse populations inside their hosts and may have been associated with fungi already in the early Paleozoic. Here we show that MRE are vulnerable to genomic degeneration and propose that they defy Muller’s ratchet thanks to retention of recombination and genome plasticity. We suggest that other endobacteria may be capable of raising similar defenses against Muller’s ratchet.

Plasticity, not genetic variation, drives infection success of a fungal parasite

SUMMARYHosts strongly influence parasite fitness. However, it is challenging to disentangle host effects on genetic vs plasticity-driven traits of parasites, since parasites can evolve quickly. It remains especially difficult to determine the causes and magnitude of parasite plasticity. In successive generations, parasites may respond plastically to better infect their current type of host, or hosts may produce generally ‘good’ or ‘bad’ quality parasites. Here, we characterized parasite plasticity by taking advantage of a system in which the parasite (the yeast Metschnikowia bicuspidata, which infects Daphnia) has no detectable heritable variation, preventing rapid evolution. In experimental infection assays, we found an effect of rearing host genotype on parasite infectivity, where host genotypes produced overall high or low quality parasite spores. Additionally, these plastically induced differences were gained or lost in just a single host generation. Together, these results demonstrate phenotypic plasticity in infectivity driven by the within-host rearing environment. Such plasticity is rarely investigated in parasites, but could shape epidemiologically important traits.