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Generalized linear mixed effect model estimates from Table 1 showing best fit patterns (solid line) of population-level endophyte frequencies (a, b) and individual-level vertical transmission rates (c, d) across annual mean maximum temperature (°C) or mean annual drought (SPEI) for E. virginicus and E. canadensis hosts. The null model (intercept) is indicated by dotted lines (b–d). Hatched circles in (b) and (d) indicate endophyte vertical transmission rates from site number 2 (flagstaff: Supplementary Table 1) that were not included in the final model estimates (Table 1)
Source publication
Heritable microbes are abundant in nature and influential to their hosts and the communities in which they reside. However, drivers of variability in the prevalence of heritable symbionts and their rates of transmission are poorly resolved, particularly across host populations experiencing variable biotic and abiotic environments. To fill these gap...
Citations
... Vertical transmission provides the key link between host and symbiont fitness, provided that greater plant biomass increases the population size of associated symbionts [58]. While vertical transmission is quite widespread for mutualistic fungal endophytes [59,60], obligate vertical transmission is believed to be rare in plant-associated bacteria [61]. Plants predominantly acquire bacteria via horizontal transmission [61], so associations with hosts are fluid and transient in evolutionary time, making short-term interactions with other microbes more significant. ...
Predicting the conditions under which rhizobacteria benefit plant growth remains challenging. Here we tested the hypothesis that benefits from inoculation with phosphate-solubilizing rhizobacteria will depend upon two environmental conditions: phosphate availability and competition between bacteria. We used maize-associated rhizobacteria with varying phosphate solubilization ability in experiments in soil, sterilized soil and gnotobiotic microcosms under conditions of varying orthophosphate availability, while we manipulated the intensity of competition by varying the number of isolates in plant inocula. Growth promotion by microbes did not depend on phosphate availability but was affected by interactions between inoculants: the beneficial effects of one Serratia isolate were only detectable when plants were inoculated with a single strain and the beneficial effects of a competition-sensitive Rhizobium was only detectable in sterilized soil or in microcosms inoculated with single strains. Moreover, microcosm experiments suggested that facilitation of a parasitic isolate, not competitive interactions between bacteria, prevented plants from gaining benefits from a potential mutualist. Competition and facilitation affected colonization of plants in microcosms but growth promotion by Serratia was more affected by inoculation treatment than culturable densities on roots. Experimental manipulation of seed inocula can reveal whether plant growth stimulation is robust with respect to competition, as well as the ecological strategies of different rhizobacteria. From an applied perspective, phosphate solubilization may not provide the mechanism for bacterial growth promotion but may indicate mutualistic potential due to phylogenetic associations. Importantly, benefits to plants are vulnerable to interactions between rhizobacteria and may not persist in mixed inoculations.
... Interaction outcomes can also be conditional based on the specific genotypes of the interacting grass and endophyte [41][42][43]. For example, genetic mismatches between red fescue and its endophyte Epichloë festucae lead to reduced endophyte prevalence [36], and variation in endophyte genotype [44] is linked with endophyte transmission rate variation in Epichloë canadensis. ...
... Based on earlier studies, CWR appears to have significant interpopulation variation based on SSR markers [49] and vegetative growth [50]. Genetic variation has also been documented in E. canadensis based on markers linked to alkaloid production, genes presumably under selection [44]. ...
Symbiotic mutualisms are thought to be stabilized by correlations between the interacting genotypes which may be strengthened via vertical transmission and/or reduced genetic variability within each species. Vertical transmission, however, may weaken interactions over time as the endosymbionts would acquire mutations that could not be purged. Additionally, temporal variation in a conditional mutualism could create genetic variation and increased variation in the interaction outcome. In this study, we assessed genetic variation in both members of a symbiosis, the endosymbiotic fungal endophyte Epichloë canadensis and its grass host Canada wildrye (Elymus canadensis). Both species exhibited comparable levels of diversity, mostly within populations rather than between. There were significant differences between populations, although not in the same pattern for the two species, and the differences were not correlated with geographic distance for either species. Interindividual genetic distance matrices for the two species were significantly correlated, although all combinations of discriminant analysis of principle components (DAPC) defined multilocus genotype groups were found suggesting that strict genotype matching is not necessary. Variation in interaction outcome is common in grass/endophyte interactions, and our results suggest that the accumulation of mutations overtime combined with temporal variation in selection pressures increasing genetic variation in the symbiosis may be the cause.
... Despite the central role of transmission dynamics in models of hostsymbiont interactions (Lipsitch et al., 1995;Genkai-Kato and Yamamura, 1999;Gundel et al., 2008), relatively few empirical studies have investigated ecological controls on the rate and mode of transmission (Douglas, 2010;Gundel et al., 2011;Sneck et al., 2019). However, observations suggest that abiotic environmental context, such as climatic variability and type of soil, could underlie variable transmission (Gundel et al., 2009;Gibert and Hazard, 2013;Sneck et al., 2017). Ecological interactions with other species could also influence transmission dynamics, but have received little study. ...
... In addition to herbivory, other environmental and genetic factors probably regulate the prevalence of endophyte symbiosis in plant populations (Rudgers et al., 2009;Gundel et al., 2011;Semmartin et al., 2015;Sneck et al., 2017Sneck et al., , 2019 through their effects on symbiont transmission. In comparison with other studies (e.g. ...
Background
Invasive plants may displace native species. This is the case of Poa annua, the only non-native plant species successfully established in Maritime Antarctica. Nonetheless, it is uncertain which factors drive the competitive success of P. annua in the harsh environmental conditions of the region. The ability of this plant species to establish novel mutualistic interactions with resident soil fungi may be crucial for its invasiveness. Such ability may be linked to the vertical transmission of the fungal endophytes via seeds.
Aims
We undertook a study to assess the role of seed fungal endophytes as promoters of the establishment and invasion of Poa annua in Maritime Antarctica.
Methods
We explored the composition and diversity of fungal communities associated with different P. annua tissues (seeds, leaves and roots) and the soil. We also measured parameters including germination rate, above-ground biomass, reproductive structures, and the survival of invasive P. annua as well as of the native Colobanthus quitensis and Deschampsia antarctica grown from seeds with and without endophytes. Furthermore, we conducted inter- and intraspecific competition experiments among native and invasive plants, where chemically-mediated plant-to-plant interference (allelopathy) and plant growth rate were measured to calculate a relative competition index.
Results
We found that fungal endophyte taxa associated with P. annua tissues were very different from those in the soil. Fungal endophytes in P. annua differed among seed, root and shoot tissues, which suggests low transmission among different organs. The removal of endophytes from P. annua seeds was associated with reduced seed germination, plant growth and survivorship, while the competitive ability of P. annua (assessed by accumulated biomass) relative to native species, as well as levels of allelochemicals in soils, were higher in the presence of seed fungal endophytes.
Conclusion
Our results suggest that fungal endophytes, maternally inherited through seeds, improve host fitness and may contribute to the invasive success of P. annua in Antarctica.
... 利用内生真菌进行作物育种, 主要利用了其对宿 主植物的诸多增益作用、内生真菌在植物中的分布特 点及其随种子传播等优良特性 [22] , 主要包括: 内生真菌 侵染所诱导的抗逆性状可稳定遗传 [22,23] ; 内生真菌缺 乏有性繁殖, 不在植物体外部产生子实体, 这决定了内 生真菌与宿主植物的共生特性不会造成种间、个体间 的泛滥传播, 对环境具备安全性 [24] ; 内生真菌传播具有 高效性, 其侵染不受根围和叶围等外界微生物的竞争, 侵染内生真菌的植株可通过种子进行垂直传播, 子代 种子带菌率接近100% [1] . 综上所述, 人工接种的方式获 利用愈伤组织法将内生真菌接种至直立雀麦(Bromus erectus), 发现同一植株接种两种内生真菌仅有8% 的侵染成功率 [25] , 人工接种两种内生真菌往往只能成 功侵染一种内生真菌 [26] . ...
Plant-endophyte associations play important roles in grassland agricultural ecology. Many studies indicate that endophytic fungi can promote host growth and reduce the biotic and abiotic stresses of host plants. Epichloë endophytes of the family Clavicitaceae are fungal symbionts of Pooideae grasses. These endophytes usually do not express any obvious host symptoms. Many Epichloë endophytes can endow hosts with increased abiotic stress tolerance as a result of enhanced growth, tillering, reproduction and nutrient acquisition, particularly under conditions of drought, cold, salt and nutrient deficiencies and thus, have important roles in pastoral agricultural systems. Animal-safe grass-endophyte associations that confer bio-protective properties for increased pasture persistence and productivity have been developed and commercialized. Artificial inoculation with symbiotic Epichloë microbes is an important technique for the creation of novel germplasm. Selected Epichloë strains can add value to some grass-based forage systems by providing both biotic and abiotic stress resistance. In addition, they can improve and strengthen grass physiological functions and plant vigor. The Epichloë bromicola WBE1 endophyte of Hordeum brevisubulatum played an important role in maintaining the growth of host grass by promoting nutrient absorption and maintaining the ionic balance under salt stress. E. bromicola WBE1 can produce peramine, an alkaloid produced by Epichloë species, that protects host grasses from herbivorous insects. However, this strain was unable to synthesize the alkaloids that are toxic to livestock, such as ergine, ergonovine, ergovaline or lolitrem B. Barley (Hordeum vulgare) is one of the most important cereal crops. The importance of barley to human and animal nutrition, and indeed to the foundation and maintenance of human civilization, is well documented. Traditional barley breeding for improved environmental stress tolerance has resulted in good varieties. However, conventional breeding techniques neglect the microorganisms in plants. In this study, animal-safe endophytic E. bromicola WBE1 isolated from wild barley (H. brevisubulatum) was artificially inoculated into cultivated hulled barley (H. vulgare cv. Yangsimai No. 1) and hull-less barley (H. vulgare var. nudum cv. Chaiqing No. 1), creating novel barley germplasm. Plants that were inoculated with endophytes and those that were free of endophytes were evaluated for growth in the field. The plant height, tiller numbers, biomass and the grain weight per plant of endophyte-inoculated hulled barley plants (Yangsimai No. 1) were 5%, 20%, 46% and 22% higher than those of the control hulled barley plants, respectively, and they matured about 5 days earlier. The tiller numbers, biomass and grain weight per plant of endophyte-inoculated hull-less barley plants (Chaiqing No. 1) were 29%, 37% and 28% higher, respectively, than those of the control hull-less barley plants in the field. However, there was no significant difference between inoculated hull-less barley plants and control hullless barley plants in the plant height and growth period. A novel germplasm of barley containing the endophyte was successfully created. E. bromicola improves plant characteristics and the growth of host. The results presented here provide evidence that the inoculation of barley with E. bromicola may be used to improve its germplasm. E. bromicola can be successfully inoculated into other phylogenetically close host species, and this technique has the potential to improve the growth of Hordeae cereal crops and serve as a broad application to produce agriculturally useful synthetic novel symbioses in germplasm.
... Agrostis hyemalis, plant demography, dynamic stability, Epichloë amarillans, hierarchical Bayesian model, long-term outcomes, mutualism, plant-microbe et al., 2015;Sneck et al., 2017) and animals (Chen & Purcell, 1997;Darby & Douglas, 2003;Fukatsu et al., 2001;Hilgenboecker et al., 2008;Jaenike et al., 2010) have documented variability in population prevalence of heritable microbes, typically with little or no knowledge of individual fitness effects. A different body of work has contrasted the fitness of symbiotic and non-symbiotic hosts (Oliver et al., 2007;Sakurai et al., 2005), often with limited insight into population-scale outcomes. ...
... survival, growth, reproduction and recruitment; Bibian et al., 2016;Chung et al., 2015;Gibert et al., 2015;Palmer et al., 2010;Rudgers et al., 2012;Yule et al., 2013). Contextdependent variation in vertical transmission has received less attention, yet some studies have shown different transmission patterns dependent on abiotic (Sneck et al., 2017) Miller, unpubl. data, Rudgers et al., 2009). ...
Heritable symbionts are often observed at intermediate prevalence within host populations, despite expectations that positive fitness feedbacks should drive beneficial symbionts to fixation. Intermediate prevalence may reflect neutral dynamics of symbionts with weak fitness effects, transient dynamics of symbionts trending towards fixation (or elimination), or a stable intermediate outcome determined by the balance of fitness effects and failed symbiont transmission. Theory suggests that these outcomes should depend on symbiont‐conferred demographic effects and vertical transmission efficiency, which may both depend on environmental context.
We established experimental populations of winter bent grass Agrostis hyemalis across a range of prevalence of the heritable fungal endophyte Epichloë amarillans. Using irrigation, we elevated the precipitation for half of the populations, which we hypothesized would weaken the benefits of symbiosis. Across two annual transitions, we assayed 5,485 individuals to determine prevalence and censused 954 individuals for demographic (survival, flowering, reproduction and recruitment) and vertical transmission data. We used hierarchical Bayesian models to infer long‐run equilibria from short‐term changes in symbiont prevalence and estimated demographic vital rates to link individual‐level effects to population‐level outcomes.
We found evidence for all three proposed mechanisms for intermediate symbiont prevalence, but the outcome differed qualitatively across years and precipitation treatments. In the first year, symbionts trended towards fixation under drought conditions but drifted neutrally under elevated precipitation. Fixation likely arose from symbiont‐conferred recruitment benefits outweighing reproductive costs under the drought conditions, while elevated precipitation tempered these effects. In the second transition year, we inferred stable intermediate prevalence across both precipitation treatments, which indicated a balance between symbiont conferred recruitment benefits that allowed low‐prevalence populations to increase and imperfect transmission that caused high‐prevalence populations to decrease.
Synthesis. We find support for neutral, transient and stable mechanisms underlying symbiont prevalence, indicating that symbiont prevalence is often pushed and pulled in different directions by the composite outcome of symbiont effects on demographic rates and transmission efficiency, and the way in which these processes respond to environmental context.
... Despite the central role of transmission dynamics in models of hostsymbiont interactions (Lipsitch et al., 1995;Genkai-Kato and Yamamura, 1999;Gundel et al., 2008), relatively few empirical studies have investigated ecological controls on the rate and mode of transmission (Douglas, 2010;Gundel et al., 2011;Sneck et al., 2019). However, observations suggest that abiotic environmental context, such as climatic variability and type of soil, could underlie variable transmission (Gundel et al., 2009;Gibert and Hazard, 2013;Sneck et al., 2017). Ecological interactions with other species could also influence transmission dynamics, but have received little study. ...
... In addition to herbivory, other environmental and genetic factors probably regulate the prevalence of endophyte symbiosis in plant populations (Rudgers et al., 2009;Gundel et al., 2011;Semmartin et al., 2015;Sneck et al., 2017Sneck et al., , 2019 through their effects on symbiont transmission. In comparison with other studies (e.g. ...
Background and aims:
Processes that maintain variation in the prevalence of symbioses within host populations are not well understood. While fitness benefits of symbiosis can clearly drive changes in symbiont prevalence, the rate of transmission has been less studied. Many grasses host symbiotic fungi (Epichloë spp.), which can transmit vertically to seeds or horizontally via spores. These symbionts may protect plants against herbivores by producing alkaloids or by increasing tolerance to damage. Therefore, herbivory could be a key ecological factor that alters symbiont prevalence within host populations by affecting either symbiont benefits to host fitness or the symbiont transmission rate. Here, we addressed the following questions: does symbiont presence modulate plant tolerance to herbivory? Does folivory increase symbiont vertical transmission to seeds or hyphal density in seedlings? Do plants with symbiont horizontal transmission have lower rates of vertical transmission than plants lacking horizontal transmission?
Methods:
We studied the grass Poa autumnalis and symbiotic fungi in genus Epichloë. We measured plant fitness (survival, growth, reproduction) and symbiont transmission to seeds following simulated folivory in a 3-year common garden experiment and surveyed natural populations that varied in mode of symbiont transmission.
Key results:
Poa autumnalis hosted two Epichloë taxa, an undescribed vertically transmitted Epichloë sp. PauTG-1 and E. typhina subsp. poae with both vertical and horizontal transmission. Simulated folivory reduced plant survival, but endophyte presence increased tolerance to damage and boosted fitness. Folivory increased vertical transmission and hyphal density within seedlings, suggesting induced protection for progeny of damaged plants. Across natural populations, the prevalence of vertical transmission did not correlate with symbiont prevalence or differ with mode of transmission.
Conclusions:
Herbivory not only mediated the reproductive fitness benefits of symbiosis, but also promoted symbiosis persistence by increasing vertical transmission to the next generation. Our results reveal a new mechanism by which herbivores could influence the prevalence of microbial symbionts in host populations.
... It is possible that alates also use these signals to recognize the gut protist composition of potential mates and preferentially choose a negative assortative mate partner in order to complete the gut protist community in their offspring. Gundel, Rudgers, & Ghersa, 2011;Sneck, Rudgers, Young, & Miller, 2017). In Reticulitermes termites, several nonexclusive hypotheses could explain why some protists are not perfectly transmitted by the alates. ...
Although mutualistic associations between animals and microbial symbionts are widespread in nature, the mechanisms that have promoted their evolutionary persistence remain poorly understood. A vertical mode of symbiont transmission (from parents to offspring) is thought to ensure partner fidelity and stabilisation, although the efficiency of vertical transmission has rarely been investigated, especially in cases where hosts harbour a diverse microbial community. Here we evaluated vertical transmission rates of cellulolytic gut oxymonad and parabasalid protists in the wood‐feeding termite Reticulitermes grassei. We sequenced amplicons of the 18S rRNA gene of protists from 24 colonies of R. grassei collected in two populations. For each colony, the protist community was characterised from the gut of 14 swarming reproductives and from a pool of 10 worker guts. A total of 98 OTUs belonging to 13 species‐level taxa were found. The vertical transmission rate was estimated for each protist present in a colony by its frequency among the reproductives. Results revealed that transmission rates were high, with an average of 0.897 (±0.164) per protist species. Overall, the protist community did not differ between reproductive sexes, suggesting that both the queen and king could contribute to the gut microbiota of the offspring. A positive relationship between the transmission rate of protists and their prevalence within populations was also detected. However, transmission rates alone did not explain protist prevalence. In conclusion, these findings reveal key forces behind a conserved, multi‐species mutualism, raising further questions on the roles of horizontal transfer and negative selection in shaping symbiont prevalence.
... Future research will have to investigate the maternal and environmental drivers of the rate of vertical transmission of microorganisms (e.g. Cavazos et al., 2018;Sneck et al., 2017;Leff et al., 2017), and assess the role of these microorganisms on seed survival and germination, seedling growth and health (e.g. Vivas et al., 2017;Leroy et al., 2019), and ultimately tree fitness. ...
Les interactions entre micro-organismes sous-tendent de nombreux services écosystémiques, y compris la régulation des maladies des plantes cultivées. Un acteur de cette régulation est le pathobiome, défini comme le sous-ensemble des micro-organismes associés à une plante hôte en interaction avec un agent pathogène. L'un des défis actuels consiste à reconstruire les pathobiomes à partir de données de metabarcoding, pour identifier des agents potentiels de biocontrôle et pour surveiller en temps réel leurs réponses aux changements environnementaux. Plusieurs verrous méthodologiques doivent cependant être levés pour atteindre ces objectifs. Tout d’abord, il n’existe pas de consensus concernant l’approche bioinformatique la plus fiable pour déterminer l’identité et l’abondance des micro-organismes présents dans les échantillons végétaux. De plus, les réseaux microbiens construits avec les méthodes actuellement disponibles sont des réseaux d’associations statistiques entre des comptages de séquences, non directement superposables aux réseaux d’interactions (ex : compétition, parasitisme) entre micro-organismes. L’objectif de la thèse était donc de déterminer les approches bioinformatiques et statistiques les plus pertinentes pour reconstruire des réseaux d’interactions microbiennes à partir de données de metabarcoding. Le modèle d’étude était la vigne (Vitis vinifera L. cv. Merlot noir) et l’oïdium de la vigne, Erysiphe necator. Nous avons tout d’abord déterminé l’approche bioinformatique la plus adaptée pour identifier la communauté fongique associée à ce pathogène, en comparant la capacité de 360 pipelines à retrouver la composition d’une communauté artificielle de 189 souches fongiques. DADA2 est apparu comme l’outil le plus performant. Nous avons ensuite évalué l’influence de la pratique culturale (viticulture conventionnelle vs. biologique) sur les communautés fongiques des feuilles et évalué le niveau de réplicabilité des réseaux microbiens construits avec une méthode d’inférence classique, SparCC. La réplicabilité était très faible, jetant ainsi un doute sur l’utilité de ces réseaux pour le biocontrôle et la biosurveillance. Nous avons donc utilisé une nouvelle approche statistique, le modèle PLN, qui permet de prendre en compte la variabilité environnementale, pour explorer finement le pathobiome d’Erysiphe necator. Les interactions microbiennes prédites par le modèle sont en cours de comparaison avec des expériences de confrontations de levures en co-cultures. Une approche alternative, HMSC, a également été testée sur un autre modèle biologique et certaines prédictions ont été confrontées avec succès aux données de la littérature. Les réseaux microbiens, sous réserve d’amélioration des méthodes de reconstruction, pourraient donc être utilisés pour capturer les signaux des interactions biotiques dans le pathobiome.
... Correlation with environmental factors can point to possible factors that may determine the distribution and relative frequency of the endophyte species. However, the assumption that higher relative frequencies of an endophyte species reflect greater benefits may be misleading because other factors such as differences in rate of endophyte transmission (Afkhami & Rudgers, 2008;Sneck, Rudgers, Young, & Miller, 2017), timing of species origin or host-endophyte associations, meta-population or meta-community dynamics, or differences in dispersal may affect frequencies (Faeth & Sullivan, 2003;Saikkonen, Faeth, Helander, & Sullivan, 1998;Saikkonen, Lehtonen, Helander, Koricheva, & Faeth, 2006;Saikkonen, Wali, Helander, & Faeth, 2004 (Jia, Oberhofer, Shymanovich, & Faeth, 2016;Jia et al., 2015;Oberhofer et al., 2014;Vandegrift et al., 2015). ...
Aim
The endophyte Epichloë alsodes, with known insecticidal properties, is found in a majority of Poa alsodes populations across a latitudinal gradient from North Carolina to New York. A second endophyte, E. schardlii var. pennsylvanica, with known insect‐deterring effects, is limited to a few populations in Pennsylvania. We explored whether such disparate differences in distributions could be explained by selection from biotic and abiotic environmental factors.
Location
Along the Appalachian Mountains from North Carolina to New York, USA.
Taxon
Fungi.
Methods
Studied correlations of infection frequencies with abiotic and biotic environmental factors. Checked endophyte vertical transmission rates and effects on overwintering survival. With artificial inoculations for two host populations with two isolates per endophyte species, tested endophyte–host compatibility. Studied effects of isolates on host performances in greenhouse experiment with four water‐nutrients treatments.
Results
Correlation analysis revealed positive associations of E. alsodes frequency with July Max temperatures, July precipitation, and soil nitrogen and phosphorous and negative associations with insect damage and soil magnesium and potassium. Plants infected with E. alsodes had increased overwintering survival compared to plants infected with E. schardlii or uninfected (E−) plants. Artificial inoculations indicated that E. alsodes had better compatibility with a variety of host genotypes than did E. schardlii. The experiment with reciprocally inoculated plants grown under different treatments revealed a complexity of interactions among hosts, endophyte species, isolate within species, host plant origin, and environmental factors. Neither of the endophyte species increased plant biomass, but some of the isolates within each species had other effects on plant growth such as increased root:shoot ratio, number of tillers, and changes in plant height that might affect host fitness.
Main conclusion
In the absence of clear and consistent effects of the endophytes on host growth, the differences in endophyte‐mediated protection against herbivores may be the key factor determining distribution differences of the two endophyte species.
... Exploring the ways in which host outcrossing may disrupt symbiont transmission is important because imperfect vertical transmission is widely documented across plant and animal hosts, even for symbioses that are thought to be strongly beneficial (Afkhami and Rudgers 2008, Bright and Bulgheresi 2010, Gundel et al. 2011, Sneck et al. 2017), but the causes of this variation are poorly understood. Additional work is needed on several fronts. ...
... Elymus virginicus and E. canadensis are perennial, cool season grasses that harbor intermediate to high frequencies of fungal endophytes (Epichloё spp.), which can grow asymptomatically in above-ground host tissues (Sneck et al. 2017). Epichloё endophytes are known to provide mutualistic benefits to cool-season grass hosts, including our focal host species E. virginicus (Rudgers and Swafford 2009), though host fitness benefits are often context-dependent. ...
... In total, 107 E+ plants from 89 maternal families were reared over two years (2014 and 2015) to act as the P 1 generation for the greenhouse crossing experiment. Our previous work (Sneck et al. 2017) determined the genotypes of Epichloё sp. occupying the maternal families used in the present experiment by amplifying 18 fungal genetic markers. ...
Vertically transmitted microbes are common in macro‐organisms and can enhance host defense against environmental stress. Because vertical transmission couples host and symbiont lineages, symbionts may become specialized to host species or genotypes. Specialization and contrasting reproductive modes of symbiotic partners could create incompatibilities between inherited symbionts and novel host genotypes when hosts outcross or hybridize. Such incompatibilities could manifest as failed colonization or poor symbiont growth in host offspring that are genetically dissimilar from their maternal host. Moreover, outcrossing between host species could influence both host and symbiont reproductive performance. We tested these hypotheses by manipulating outcrossing between populations and species of two grasses, Elymus virginicus and E. Canadensis, that host vertically transmitted fungal endophytes (genus Epichloё). In both greenhouse and field settings, we found that host‐symbiont compatibility was robust to variation in host genetic background, spanning within‐population, between‐population, and between‐species crosses. Symbiont transmission into the F1 generation was generally high and weakly affected by host outcrossing. Furthermore, endophytes grew equally well in planta regardless of host genetic background and transmitted at high frequencies into the F2 generation. However, outcrossing, especially inter‐specific hybridization, reduced reproductive fitness of the host, and thereby the symbiont. Our results challenge the hypothesis that host genetic recombination, which typically exceeds that of symbionts, is a disruptive force in heritable symbioses. Instead, symbionts may be sufficiently generalized to tolerate ecologically realistic variation in host outcrossing.
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