High specificity of symbiont-conferred resistance in an aphid-parasitoid field community.

Host-parasite coevolution is mediated by genetic interactions between the antagonists and may lead to reciprocal adaptation. In the black bean aphid, Aphis fabae fabae, resistance to parasitoids can be conferred by the heritable bacterial endosymbiont Hamiltonella defensa. H. defensa has been shown to be variably protective against different parasitoid species, and different genotypes of the black bean aphid's main parasitoid Lysiphlebus fabarum. However, these results were obtained using haphazard combinations of laboratory-reared insect lines with different origins, making it unclear how representative they are of natural, locally (co)adapted communities. We therefore comprehensively sampled the parasitoids of a natural A. f. fabae population and measured the ability of the five most abundant species to parasitize aphids carrying the locally prevalent H. defensa haplotypes. H. defensa provided resistance only against the dominant parasitoid L. fabarum (70% of all parasitoids), but not against less abundant parasitoids, and resistance to L. fabarum acted in a genotype-specific manner (G × G interactions between H. defensa and L. fabarum). These results confirm that strong species- and genotype-specificity of symbiont-conferred resistance is indeed a hallmark of wild A. f. fabae populations, and they are consistent with symbiont-mediated adaptation of aphids to the parasitoids posing the highest risk.

Strong genotype-by-genotype interactions between aphid-defensive symbionts and parasitoids persist across different biotic environments.

The dynamics of coevolution between hosts and parasites are influenced by their genetic interactions. Highly specific interactions, where the outcome of an infection depends on the precise combination of host and parasite genotypes (G × G interactions), have the potential to maintain genetic variation by inducing negative frequency-dependent selection. The importance of this effect also rests on whether such interactions are consistent across different environments or modified by environmental variation (G × G × E interaction). In the black bean aphid, Aphis fabae, resistance to its parasitoid Lysiphlebus fabarum is largely determined by the possession of a heritable bacterial endosymbiont, Hamiltonella defensa, with strong G × G interactions between H. defensa and L. fabarum. A key environmental factor in this system is the host plant on which the aphid feeds. Here, we exposed genetically identical aphids harbouring three different strains of H. defensa to three asexual genotypes of L. fabarum and measured parasitism success on three common host plants of A. fabae, namely Vicia faba, Chenopodium album and Beta vulgaris. As expected, we observed the pervasive G × G interaction between H. defensa and L. fabarum, but despite strong main effects of the host plants on average rates of parasitism, this interaction was not altered significantly by the host plant environment (no G × G × E interaction). The symbiont-conferred specificity of resistance is thus likely to mediate the coevolution of A. fabae and L. fabarum, even when played out across diverse host plants of the aphid.

The ecologically relevant genetics of plant-plant interactions.

Interactions among plants have been long recognized as a major force driving plant community dynamics and crop yield. Surprisingly, our knowledge of the ecological genetics associated with variation of plant-plant interactions remains limited. In this opinion article by scientists from complementary disciplines, the international PLANTCOM network identified four timely questions to foster a better understanding of the mechanisms mediating plant assemblages. We propose that by identifying the key relationships among phenotypic traits involved in plant-plant interactions and the underlying adaptive genetic and molecular pathways, while considering environmental fluctuations at diverse spatial and time scales, we can improve predictions of genotype-by-genotype-by-environment interactions and modeling of productive and stable plant assemblages in wild habitats and crop fields.

Corrigendum: Investigating genetic diversity within the most abundant and prevalent non-pathogenic leaf-associated bacteria interacting with Arabidopsis thaliana in natural habitats.

[This corrects the article DOI: 10.3389/fmicb.2022.984832.].

Investigating genetic diversity within the most abundant and prevalent non-pathogenic leaf-associated bacteria interacting with Arabidopsis thaliana in natural habitats.

Microbiota modulates plant health and appears as a promising lever to develop innovative, sustainable and eco-friendly agro-ecosystems. Key patterns of microbiota assemblages in plants have been revealed by an extensive number of studies based on taxonomic profiling by metabarcoding. However, understanding the functionality of microbiota is still in its infancy and relies on reductionist approaches primarily based on the establishment of representative microbial collections. In Arabidopsis thaliana, most of these microbial collections include one strain per OTU isolated from a limited number of habitats, thereby neglecting the ecological potential of genetic diversity within microbial species. With this study, we aimed at estimating the extent of genetic variation between strains within the most abundant and prevalent leaf-associated non-pathogenic bacterial species in A. thaliana located south-west of France. By combining a culture-based collection approach consisting of the isolation of more than 7,000 bacterial colonies with an informative-driven approach, we isolated 35 pure strains from eight non-pathogenic bacterial species. We detected significant intra-specific genetic variation at the genomic level and for growth rate in synthetic media. In addition, significant host genetic variation was detected in response to most bacterial strains in in vitro conditions, albeit dependent on the developmental stage at which plants were inoculated, with the presence of both negative and positive responses on plant growth. Our study provides new genetic and genomic resources for a better understanding of the plant-microbe ecological interactions at the microbiota level. We also highlight the need of considering genetic variation in both non-pathogenic bacterial species and A. thaliana to decipher the genetic and molecular mechanisms involved in the ecologically relevant dialog between hosts and leaf microbiota.

A diverse parasite pool can improve effectiveness of biological control constrained by genotype-by-genotype interactions.

The outcomes of biological control programs can be highly variable, with natural enemies often failing to establish or spread in pest populations. This variability has posed a major obstacle in use of the bacterial parasite Pasteuria penetrans for biological control of Meloidogyne species, economically devastating plant-parasitic nematodes for which there are limited management options. A leading hypothesis for this variability in control is that infection is successful only for specific combinations of bacterial and nematode genotypes. Under this hypothesis, failure of biological control results from the use of P. penetrans genotypes that cannot infect local Meloidogyne genotypes. We tested this hypothesis using isofemale lines of M. arenaria derived from a single field population and multiple sources of P. penetrans from the same and nearby fields. In strong support of the hypothesis, susceptibility to infection depended on the specific combination of host line and parasite source, with lines of M. arenaria varying substantially in which P. penetrans source could infect them. In light of this result, we tested whether using a diverse pool of P. penetrans could increase infection and thereby control. We found that increasing the diversity of the P. penetrans inoculum from one to eight sources more than doubled the fraction of M. arenaria individuals susceptible to infection and reduced variation in susceptibility across host lines. Together, our results highlight genotype-by-genotype specificity as an important cause of variation in biological control and call for the maintenance of genetic diversity in natural enemy populations.

Toward Unifying Evolutionary Ecology and Genomics to Understand Positive Plant-Plant Interactions Within Wild Species.

In a local environment, plant networks include interactions among individuals of different species and among genotypes of the same species. While interspecific interactions are recognized as main drivers of plant community patterns, intraspecific interactions have recently gained attention in explaining plant community dynamics. However, an overview of intraspecific genotype-by-genotype interaction patterns within wild plant species is still missing. From the literature, we identified 91 experiments that were mainly designed to investigate the presence of positive interactions based on two contrasting hypotheses. Kin selection theory predicts partisan help given to a genealogical relative. The rationale behind this hypothesis relies on kin/non-kin recognition, with the positive outcome of kin cooperation substantiating it. On the other hand, the elbow-room hypothesis supports intraspecific niche partitioning leading to positive outcome when genetically distant genotypes interact. Positive diversity-productivity relationship rationalizes this hypothesis, notably with the outcome of overyielding. We found that both these hypotheses have been highly supported in experimental studies despite their opposite predictions between the extent of genetic relatedness among neighbors and the level of positive interactions. Interestingly, we identified a highly significant effect of breeding system, with a high proportion of selfing species associated with the presence of kin cooperation. Nonetheless, we identified several shortcomings regardless of the species considered, such as the lack of a reliable estimate of genetic relatedness among genotypes and ecological characterization of the natural habitats from which genotypes were collected, thereby impeding the identification of selective drivers of positive interactions. We therefore propose a framework combining evolutionary ecology and genomics to establish the eco-genomic landscape of positive GxG interactions in wild plant species.

Host Genotype and Tissue Type Determine DWV Infection Intensity.

Varroa mite-vectored viruses such as Deformed wing virus (DWV) are of great concern for honey bee health as they can cause disease in individuals and increase colony mortality. Two genotypes of DWV (A and B) are prevalent in the United States and may have differential virulence and pathogenicity. Honey bee genetic stocks bred to resist Varroa mites also exhibit differential infection responses to the Varroa mite-vectored viruses. The goal of this project was to determine if interactions between host genotype could influence the overall infection levels and dissemination of DWV within honey bees. To do this, we injected DWV isolated from symptomatic adult bees into mite-free, newly emerged adult bees from five genetic stocks with varying levels of resistance to Varroa mites. We measured DWV-A and DWV-B dissemination among tissues chosen based on relevance to general health outcomes for 10 days. Injury from sham injections did not increase DWV-A levels but did increase DWV-B infections. DWV injection increased both DWV-A and DWV-B levels over time with significant host stock interactions. While we did not observe any differences in viral dissemination among host stocks, we found differences in virus genotype dissemination to different body parts. DWV-A exhibited the highest initial levels in heads and legs while the highest initial levels of DWV-B were found in heads and abdomens. These interactions underscore the need to evaluate viral genotype and tissue specificity in conjunction with host genotype, particularly when the host has been selected for traits relative to virus-vector and virus resistance.

An interaction between host and microbe genotypes determines colonization success of a key bumble bee gut microbiota member.

There has been a proliferation of studies demonstrating an organism's health is influenced by its microbiota. However, factors influencing beneficial microbe colonization and the evolution of these relationships remain understudied relative to host-pathogen interactions. Vertically transmitted beneficial microbes are predicted to show high levels of specificity in colonization, including genotype matching, which may transpire through coevolution. We investigate how host and bacterial genotypes influence colonization of a core coevolved microbiota member in bumble bees. The hindgut colonizing Snodgrassella alvi confers direct benefits, but, as an early colonizer, also facilitates the further development of a healthy microbiota. Due to predominantly vertical transmission promoting tight evolution between colonization factors of bacteria and host lineages, we predict that genotype-by-genotype interactions will determine successful colonization. Germ-free adult bees from seven bumble bee colonies (host genotypic units) were inoculated with one of six genetically distinct strains of S. alvi. Subsequent colonization within host and microbe genotypes combinations ranged from 0 to 100%, and an interaction between host and microbe genotypes determined colonization success. This novel finding of a genotype-by-genotype interaction determining colonization in an animal host-beneficial microbe system has implications for the ecological and evolutionary dynamics of host and microbe, including associated host-fitness benefits.

The impact of spatial scale and habitat configuration on patterns of trait variation and local adaptation in a wild plant parasite.

Theory indicates that spatial scale and habitat configuration are fundamental for coevolutionary dynamics and how diversity is maintained in host-pathogen interactions. Yet, we lack empirical data to translate the theory to natural host-parasite systems. In this study, we conduct a multiscale cross-inoculation study using the specialist wild plant pathogen Podosphaera plantaginis on its host plant Plantago lanceolata. We apply the same sampling scheme to a region with highly fragmented (Åland) and continuous (Saaremaa) host populations. Although theory predicts higher parasite virulence in continuous regions, we did not detect differences in traits conferring virulence among the regions. Patterns of adaptation were highly scale dependent. We detected parasite maladaptation among regions, and among populations separated by intermediate distances (6.0-40.0 km) within the fragmented region. In contrast, parasite performance did not vary significantly according to host origin in the continuous landscape. For both regions, differentiation among populations was much larger for genetic variation than for phenotypic variation, indicating balancing selection maintaining phenotypic variation within populations. Our findings illustrate the critical role of spatial scale and habitat configuration in driving host-parasite coevolution. The absence of more aggressive strains in the continuous landscape, in contrast to theoretical predictions, has major implications for long-term decision making in conservation, agriculture, and public health.

Mapping the genetic basis of symbiotic variation in legume-rhizobium interactions in Medicago truncatula.

Mutualisms are known to be genetically variable, where the genotypes differ in the fitness benefits they gain from the interaction. To date, little is known about the loci that underlie such genetic variation in fitness or whether the loci influencing fitness are partner specific, and depend on the genotype of the interaction partner. In the legume-rhizobium mutualism, one set of potential candidate genes that may influence the fitness benefits of the symbiosis are the plant genes involved in the initiation of the signaling pathway between the two partners. Here we performed quantitative trait loci (QTL) mapping in Medicago truncatula in two different rhizobium strain treatments to locate regions of the genome influencing plant traits, assess whether such regions are dependent on the genotype of the rhizobial mutualist (QTL × rhizobium strain), and evaluate the contribution of sequence variation at known symbiosis signaling genes. Two of the symbiotic signaling genes, NFP and DMI3, colocalized with two QTL affecting average fruit weight and leaf number, suggesting that natural variation in nodulation genes may potentially influence plant fitness. In both rhizobium strain treatments, there were QTL that influenced multiple traits, indicative of either tight linkage between loci or pleiotropy, including one QTL with opposing effects on growth and reproduction. There was no evidence for QTL × rhizobium strain or genotype × genotype interactions, suggesting either that such interactions are due to small-effect loci or that more genotype-genotype combinations need to be tested in future mapping studies.