Repeated Genetic and Adaptive Phenotypic Divergence across Tidal Elevation in a Foundation Plant Species

Zerebecki, Robyn A.; Sotka, Erik E.; Hanley, Torrance C.; Bell, Katherine L.; Gehring, Catherine A.; Nice, Chris C.; Richards, Christina L.; Hughes, A. Randall

doi:10.1086/716512

Cited by 15 publications

(24 citation statements)

References 131 publications

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“…The Aulac salt marsh restoration is now just starting the fourth phase (years 10+), distinguished by the development of the S. alterniflora short phenotype, spread of S. patens, and likely interaction between S. alterniflora and S. patens (Virgin et al, 2020). During earlier phases, mature S. alterniflora plants throughout the restoration sites were the tall phenotype (similar in canopy height to those growing in creeks of reference sites), indicating that they were healthy and not stressed by intraspecific competition, nutrient limitation, or abiotic conditions (Anderson and Treshow, 1980;Zerebecki et al, 2021). However, at the beginning of the fourth phase, S. alterniflora growing close to the seaward edge of the restoration sites began to resemble the shortform plants of the reference marshes.…”

Section: Processes Underlying the Later Phases Of Salt Marsh Restorat...mentioning

confidence: 99%

“…It is well-adapted to frequent flooding by saltwater, being tolerant of high salinities including 0.6 M NaCl (35 ppt; Vasquez et al, 2006) and above (Webb, 1983). Furthermore, it displays tall and short phenotypes, with the short phenotype likely reflecting less favorable environmental conditions (Anderson and Treshow, 1980;Zerebecki et al, 2021). Spartina alterniflora's asexual spread rates when colonizing intertidal soft sediments can be vigorous (134 ± 28 m y −1 ; Callaway and Josselyn, 1992), and its seeds can disperse up to hundreds of km via tidal currents (Morgan and Sytsma, 2013).…”

Section: Introductionmentioning

confidence: 99%

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Patch-level processes of vegetation underlying site-level restoration patterns in a megatidal salt marsh

et al. 2022

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Vegetation patterns during salt marsh restoration reflect underlying processes related to colonization, reproduction, and interactions of halotolerant plants. Examining both pattern and process during recovery is valuable for understanding and managing salt marsh restoration projects. We present a decade of vegetation dynamics during salt marsh restoration (2011–2020) at a study site in the Bay of Fundy with megatidal amplitudes, strong currents, cold winter temperatures, and ice. We mainly investigated reproduction (asexual and sexual) and associated spread rates of Spartina grasses, and their health-related states (stem density, canopy height, and percent flowering) which help inform the probability of processes occurring. We also estimated modes of colonization and began quantifying the effects of interspecific interactions and environmental conditions on plant state. Spartina pectinata was the only pastureland plant to survive dike-breaching and saltwater intrusion in 2010; however, it was stunted compared to reference plants. Spartina pectinata patches remained consistent initially, before decreasing in size, and disappearing by the fifth year (2015). This early dynamic may provide initial protection to a developing salt marsh before Spartina alterniflora becomes established. Spartina alterniflora first colonized the sites in year 2 (2012), likely via deposition of rhizomal material, and then spread asexually before seedlings (sexual reproduction) appeared in year 4 (2014). Vegetation cover subsequently increased greatly until near-complete in year 9 (2019). The early successional dynamics of S. pectinata and S. alterniflora occurred spatially independently of each other, and likely contributed to sediment retention, creating an improved environment for S. patens, the dominant high marsh species in our region. Spartina patens have been slowly spreading into restoration sites from high elevation areas since year 6 (2016). We expect that competition between S. alterniflora and S. patens will result in the typical distinct zonation between high and low marsh zones. A next study will use the quantified processes for spatial-explicit modeling to simulate patterns of vegetation recovery, and to evaluate different salt marsh restoration strategies for the Bay of Fundy and elsewhere. Thus, proper identification and quantification of pattern-building processes in salt marsh vegetation recovery, the focus of our present study, was an essential step.

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Section: Processes Underlying the Later Phases Of Salt Marsh Restorat...mentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Patch-level processes of vegetation underlying site-level restoration patterns in a megatidal salt marsh

et al. 2022

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“…This finding of more differences in the beach habitat is similar to our previous study where we found differences in succulence and root to shoot biomass ratio only under salt addition, but not under pure water conditions (Richards et al, 2008; see similar results in Borrichia frutescens Richards et al, 2010). Similarly, a recent reciprocal transplant study in the salt marsh cordgrass Spartina alterniflora identified more extreme differences in the “Tall Spartina zone” habitat for survival, maximum height, root to shoot biomass ratio and total biomass (Zerebecki et al, 2021). In these examples, the conditions that were more challenging for the plants also elicited more differences between plants.…”

Section: Discussionmentioning

confidence: 98%

“…In this study, we investigated how one of the world’s most invasive plants may be adapting to three different habitats on Long Island, NY. Many studies have demonstrated that significant differences in habitat characteristics can result in adaptive differentiation within species, even under high levels of gene flow between habitats (Antonovics and Bradshaw, 1970; Linhart and Grant, 1996; Sambatti and Rice, 2006; Papadopulos et al, 2021; Zerebecki et al, 2021 but see Leimu and Fischer, 2008). Introduced species in particular have been highlighted because they can evolve rapidly in response to novel conditions (Lee, 2002; Leger and Rice, 2007; Dlugosch and Parker, 2008).…”

Section: Discussionmentioning

confidence: 99%

Rapid phenotypic differentiation and local adaptation in Japanese knotweed s.l. (Reynoutria japonicaandR. ×bohemica, Polygonaceae) invading novel habitats

Yuan

Pigliucci

Richards

2022

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PREMISE: Many plant invaders like the Japanese knotweeds are thought to colonize new habitats with low genetic diversity. Such species provide an opportunity to study rapid adaptation to complex environmental conditions. METHODS: Using replicate reciprocal transplants of clones across three habitats, we described patterns of phenotypic response and assessed degree of local adaptation. KEY RESULTS: We found plants from beach habitats had decreased height, number of leaves, leaf area, and biomass allocation to roots and shoots compared to plants from marsh and roadside habitats when grown in their home habitat. In the marsh habitat, marsh plants were generally larger than beach plants, but not different from roadside plants. There were no differences among plants from different habitats grown in the roadside habitat. Despite this evidence of differentiation in beach and marsh habitats, we found mixed evidence for local adaptation. In their "home site" plants from the marsh habitat had greater biomass than plants from the beaches but not compared to plants from roadsides. Biomass comparisons in other habitats were either maladaptive or not significant. However, plants from the roadside had greater survival in their "home site" compared to foreign plants. There were no differences in survival in the other habitats. CONCLUSIONS: We found phenotypic differentiation associated with habitats despite the low reported genetic diversity for these populations. Our results partially support the hypothesis of local adaptation in marsh and roadside habitats. Identifying whether these patterns of differentiation result from genetic or heritable non-genetic mechanisms will require further work.

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“…(Stalter and Batson, 1969;Shea et al, 1975;Valiela et al, 1978;Gallagher et al, 1988). However, a recent reciprocal transplant study demonstrated that plants from the high and low marsh habitats were differentiated genetically and in several plant traits, which translated into fitness differences, supporting the hypothesis of local adaptation (Zerebecki et al, 2021).…”

Section: Introductionmentioning

confidence: 90%

Genetic and Epigenetic Differentiation Across Intertidal Gradients in the Foundation Plant Spartina alterniflora

et al. 2022

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Ecological genomics approaches have informed us about the structure of genetic diversity in natural populations that might underlie patterns in trait variation. However, we still know surprisingly little about the mechanisms that permit organisms to adapt to variable environmental conditions. The salt marsh foundation plant Spartina alterniflora exhibits a dramatic range in phenotype that is associated with a pronounced intertidal environmental gradient across a narrow spatial scale. Both genetic and non-genetic molecular mechanisms might underlie this phenotypic variation. To investigate both, we used epigenotyping-by-sequencing (epiGBS) to evaluate the make-up of natural populations across the intertidal environmental gradient. Based on recent findings, we expected that both DNA sequence and DNA methylation diversity would be explained by source population and habitat within populations. However, we predicted that epigenetic variation might be more strongly associated with habitat since similar epigenetic modifications could be rapidly elicited across different genetic backgrounds by similar environmental conditions. Overall, with PERMANOVA we found that population of origin explained a significant amount of the genetic (8.6%) and epigenetic (3.2%) variance. In addition, we found that a small but significant amount of genetic and epigenetic variance (<1%) was explained by habitat within populations. The interaction of population and habitat explained an additional 2.9% of the genetic variance and 1.4% of the epigenetic variance. By examining genetic and epigenetic variation within the same fragments (variation in close-cis), we found that population explained epigenetic variation in 9.2% of 8,960 tested loci, even after accounting for differences in the DNA sequence of the fragment. Habitat alone explained very little (<0.1%) of the variation in these close-cis comparisons, but the interaction of population and habitat explained 2.1% of the epigenetic variation in these loci. Using multiple matrix regression with randomization (MMRR) we found that phenotypic differences in natural populations were correlated with epigenetic and environmental differences even when accounting for genetic differences. Our results support the contention that sequence variation explains most of the variation in DNA methylation, but we have provided evidence that DNA methylation distinctly contributes to plant responses in natural populations.

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Repeated Genetic and Adaptive Phenotypic Divergence across Tidal Elevation in a Foundation Plant Species

Cited by 15 publications

References 131 publications

Patch-level processes of vegetation underlying site-level restoration patterns in a megatidal salt marsh

Patch-level processes of vegetation underlying site-level restoration patterns in a megatidal salt marsh

Rapid phenotypic differentiation and local adaptation in Japanese knotweed s.l. (Reynoutria japonicaandR. ×bohemica, Polygonaceae) invading novel habitats

Genetic and Epigenetic Differentiation Across Intertidal Gradients in the Foundation Plant Spartina alterniflora

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