Evidence of within-species specialization by soil microbes and the implications for plant community diversity

Eck, Jenalle L.; Stump, Simon Maccracken; Delavaux, Camille S.; Mangan, Scott A.; Comita, Liza S.

doi:10.1073/pnas.1810767116

Cited by 64 publications

(99 citation statements)

References 48 publications

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“…This might be due to within-species pathogen specialization, which would have a greater effect near the mother tree relative to any conspecific adult (Eck et al, 2019, Gallery et al, 2007. Comparing these kernels may thus also indicate the relative strength of distance-dependent mortality relative to a potential parent vs. any large conspecific individual.…”

Section: Discussionmentioning

confidence: 99%

Seed‐to‐seedling transitions exhibit distance‐dependent mortality but no strong spacing effects in a Neotropical forest

Marchand

Comita

Wright

et al. 2019

Ecology

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Patterns of seed dispersal and seed mortality influence the spatial structure of plant communities and the local coexistence of competing species. Most seeds are dispersed in proximity to the parent tree, where mortality is also expected to be the highest, because of competition with siblings or the attraction of natural enemies. Whereas distance‐dependent mortality in the seed‐to‐seedling transition was often observed in tropical forests, few studies have attempted to estimate the shape of the survival‐distance curves, which determines whether the peak of seedling establishment occurs away from the parent tree (Janzen–Connell pattern) or if the peak attenuates but remains at the parent location (Hubbell pattern). In this study, we inferred the probability density of seed dispersal and two stages of seedling establishment (new recruits, and seedlings 20 cm or taller) with distance for 24 tree species present in the 50‐ha Forest Dynamics Plot of Barro Colorado Island, Panama. Using data from seed traps, seedling survey quadrats, and tree‐census records spanning the 1988–2014 period, we fit hierarchical Bayesian models including parameters for tree fecundity, the shape of the dispersal kernel, and overdispersion of seed or seedling counts. We combined predictions from multiple dispersal kernels to obtain more robust inferences. We find that Hubbell patterns are the most common and Janzen–Connell patterns are very rare among those species; that distance‐dependent mortality may be stronger in the seed stage, in the early recruit stage, or comparable in both; and that species with larger seeds experience less overall mortality and less distance‐dependent mortality. Finally, we describe how this modeling approach could be extended at a community scale to include less abundant species.

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Section: Discussionmentioning

confidence: 99%

Seed‐to‐seedling transitions exhibit distance‐dependent mortality but no strong spacing effects in a Neotropical forest

Marchand

Comita

Wright

et al. 2019

Ecology

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“…When focusing on the results when natural aboveground insect herbivory was excluded, i.e., the sole effect of soil biota, no differences in intraspecific PSFs for populations of P. lanceolata were observed. Although only scarcely treated in the literature, there are examples of studies that found intraspecific variation in PSFs (Wagg et al, 2015;Luo et al, 2016;Eck et al, 2019). For example, Smith et al (2012) found seedling survival of Populus angustifolia to be 2.5 times higher in soil biota from the rhizosphere of their mother tree, but neutral PSFs as well have been found (Bukowski and Petermann, 2014;Allen et al, 2018).…”

Section: Psfs Without Aboveground Herbivoresmentioning

confidence: 99%

Plant-Soil Feedbacks of Plantago lanceolata in the Field Depend on Plant Origin and Herbivory

et al. 2019

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Soil biota involved in plant-soil feedbacks (PSFs) have an impact on the growth of plant individuals. So far, studies investigating the role of soil-biota mediated PSFs in plant performance were mostly performed in greenhouses and focused predominantly on species differences, whereas the contribution of PSFs to plant performance under field conditions and intraspecific variation in PSFs among plant populations remain poorly investigated. Here, we performed a PSF pot experiment under field conditions to study intraspecific variation in plant responses to soil biota. We used seeds from multiple seed families of Plantago lanceolata L. together with Plantago-conditioned soils from contrasting habitats (three non-fertilized pastures vs. three fertilized mown pastures) to test whether plants show a positive or negative response to their parental soil biota. We furthermore tested whether these PSFs depend on abiotic habitat factors and insect herbivory. To this end, we reciprocally transplanted plants and their soil biota between the two habitat types and excluded aboveground herbivores from half of the plants, respectively. When grown without herbivores, plants from both habitat types showed similar and neutral PSFs independently of the transplant site. In contrast, in the presence of herbivores, PSFs for plants from non-fertilized pastures were negative in both habitats (i.e., plants performed better when they grew with foreign soil biota), whereas PSFs for plants from fertilized mown-pastures remained neutral. Our results suggest that soil biota alone might only play a minor role for performance of P. lanceolata and that the outcome of soil-biota mediated PSFs is modulated by effects of herbivores in different habitats.

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“…This has driven decades of empirical work to understand whether enemies are specialized enough in nature to cause this pattern and allow coexistence by this mechanism, and a recent metaanalysis supports the prediction that seed or seedling survival is greater away from conspecific adults (3). In PNAS, Eck et al (4) show that natural enemies can be even more specialized, specializing on individual genotypes within a wild population. Through simulation models exploring the theoretical implications of this field result, Eck et al (4) show that this greater specialization may weaken the stabilizing effects of natural enemies on species coexistence but also may select for greater dispersal over evolutionary time.…”

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confidence: 99%

“…In PNAS, Eck et al (4) show that natural enemies can be even more specialized, specializing on individual genotypes within a wild population. Through simulation models exploring the theoretical implications of this field result, Eck et al (4) show that this greater specialization may weaken the stabilizing effects of natural enemies on species coexistence but also may select for greater dispersal over evolutionary time.…”

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Maternal microbes complicate coexistence for tropical trees

Rogers

Fricke

2019

Proc. Natl. Acad. Sci. U.S.A.

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How can hundreds of tree species coexist in a single hectare of tropical forest when the environmental conditions, as well as the species' basic requirements, appear so similar? A leading explanation, particularly in tropical forests, is called the Janzen-Connell hypothesis after the two ecologists who proposed it in the early 1970s (1, 2). In this mechanism, specialized predators and pathogens concentrated near adult plants differentially reduce survival and growth of conspecific offspring relative to seedlings of other species. These natural enemies limit regeneration of common species and confer a relative advantage to rare species because they have more enemy-free regeneration sites. This has driven decades of empirical work to understand whether enemies are specialized enough in nature to cause this pattern and allow coexistence by this mechanism, and a recent metaanalysis supports the prediction that seed or seedling survival is greater away from conspecific adults (3). In PNAS, Eck et al. (4) show that natural enemies can be even more specialized, specializing on individual genotypes within a wild population. Through simulation models exploring the theoretical implications of this field result, Eck et al. (4) show that this greater specialization may weaken the stabilizing effects of natural enemies on species coexistence but also may select for greater dispersal over evolutionary time.The body of theory developed since the original formulation of the Janzen-Connell hypothesis has primarily asked (i) How specialized must the natural enemies be? and (ii) At what scale must these patterns operate? With regard to natural enemies, a longstanding conclusion is that species specificity of natural enemies allows coexistence. If a rare plant species shares a generalist enemy with an abundant plant species, then this abundant generalist enemy could extirpate the rare species from the community. With regard to patterns, the spatial scale matters-both in terms of enemy attack and of seed dispersal away from the maternal plant. A plant would experience a rare-species advantage if the abundance of its specialist enemy declines as the plant becomes rare, or if many seeds disperse away from areas of high specialist enemy abundance near conspecific plants. Although this body of theory emphasizes specialization, these models have only considered specialization down to the species level.While coexistence theory that is focused on naturalenemy specialization stops at the species level, empirical work supports a role for specialization within species. In agricultural systems, there is increasing recognition that microbes can specialize on particular genotypes (5,6). Several studies on plants in the wild have hinted at an advantage associated with escaping one's mother plant, with rare genotypes showing an advantage over common genotypes (7), greater survival away from close relatives (8), and the general finding that seedlings underneath a tree typically are not the Fig. 1. For rare species, the benefit of escape from pathoge...

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Evidence of within-species specialization by soil microbes and the implications for plant community diversity

Cited by 64 publications

References 48 publications

Seed‐to‐seedling transitions exhibit distance‐dependent mortality but no strong spacing effects in a Neotropical forest

Seed‐to‐seedling transitions exhibit distance‐dependent mortality but no strong spacing effects in a Neotropical forest

Plant-Soil Feedbacks of Plantago lanceolata in the Field Depend on Plant Origin and Herbivory

Maternal microbes complicate coexistence for tropical trees

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