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  1. Abstract

    Infectious disease can shape community structure, particularly when pathogens affect foundation species. Seagrasses are foundation species that form meadows along coasts worldwide, controlling sediment deposition and biogeochemical cycling while supporting a diverse community of fish and invertebrates. These plants are hosts to wasting diseases that cause necrotic tissue lesions, which could alter seagrass value as food, habitat and mediators of ecosystem processes. However, such biotic interactions and influences on disease dynamics are still not well understood. We investigated whether a common herbivore affected the development of wasting disease on eelgrass.

    We measured the severity and prevalence of eelgrass wasting disease in a meadow across two summers through repeated field surveys. We assessed the role of the eelgrass herbivore on disease spread and growth using microcosm and mesocosm experiments. We further explored herbivore feeding preferences in a choice trial, which was paired with chemical analysis of plant tissue and analysed using a structural equation model.

    While the herbivore facilitates the growth of new disease lesions among isolated leaves, on balance they reduce lesion severity by more than 50% in comparison with no‐herbivore controls in field‐realistic settings. This was likely because the herbivore strongly prefers to eat diseased rather than healthy tissue, consuming nearly twice as much lesion area in choice trials. This preference arises from pathogen‐driven changes in the host plant; lesioned tissue requires less force to penetrate than non‐lesioned tissue. Additionally, as lesions increase in size, their polyphenolic concentrations drop, which further increases the magnitude of preference for lesioned tissue.

    Synthesis: These results suggest that these herbivores could help maintain disease in this system at a high prevalence (by facilitating disease development) but low severity (through preferential consumption), which is consistent with our field observations of nearly 100% prevalence and low severity in a natural bed where herbivore density is high. Describing such multi‐species interactions in marine systems will advance our predictions of future disease states, as current understandings focus primarily on how environmental change contributes to pathogen outbreaks.

     
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  2. Abstract

    Fish biodiversity is an important indicator of ecosystem health and a priority for the National Park Service in Drakes Estero, a shallow estuary within Point Reyes National Seashore, Marin County, California. However, fish diversity has yet to be described following the removal of oyster aquaculture infrastructure within Drakes Estero from 2016 to 2017. We used environmental DNA (eDNA) to characterize fish biodiversity within Drakes Estero. We amplified fish eDNA with MiFish primers and classified sequences with a 12S rRNA reference database. We identified 110 unique operational taxonomic units (OTUs, at 97% similarity) within the estuary from 40 samples across 4 sites. From these 110 OTUs, we identified 9 species and 13 taxonomic groups at the genus, family, order, or class level within the estuary. Species‐level assignments are limited by a lack of representative sequences targeted by the MiFish primers for 42% of eelgrass fishes in our region that we identified from a literature review in the Northeast Pacific (NEP) from Elkhorn Slough to Humboldt Bay. Despite this limitation, we identified some common Drakes Estero fishes with our eDNA surveys, including the three‐spined stickleback (Gasterosteus aculeatus), Pacific staghorn sculpin (Leptocottus armatus), surfperches (Embiotocidae), gobies (Gobiidae), and a hound shark (Triakidae). We also compared fish biodiversity within the estuary with that from nearby Limantour Beach, a coastal site. Limantour beach differed in community composition from Drakes Estero and was characterized by high relative abundances of anchovy (Engraulissp.) and herring (Clupeasp.). Thus, we can distinguish estuarine and non‐estuarine sites (<10 km away) with eDNA surveys. Further, eDNA surveys accounted for greater fish diversity than seine surveys conducted at one site within the estuary. Environmental DNA surveys will likely be a useful tool to monitor fish biodiversity across eelgrass estuaries in the Northeast Pacific, especially as reference databases become better populated with regional species.

     
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    Free, publicly-accessible full text available July 1, 2024
  3. Abstract

    Plant microbiomes depend on environmental conditions, stochasticity, host species, and genotype identity. Eelgrass (Zostera marina)is a unique system for plant–microbe interactions as a marine angiosperm growing in a physiologically-challenging environment with anoxic sediment, periodic exposure to air at low tide, and fluctuations in water clarity and flow. We tested the influence of host origin versus environment on eelgrass microbiome composition by transplanting 768 plants among four sites within Bodega Harbor, CA. Over three months following transplantation, we sampled microbial communities monthly on leaves and roots and sequenced the V4–V5 region of the 16S rRNA gene to assess community composition. The main driver of leaf and root microbiome composition was destination site; more modest effects of host origin site did not last longer than one month. Community phylogenetic analyses suggested that environmental filtering structures these communities, but the strength and nature of this filtering varies among sites and over time and roots and leaves show opposing gradients in clustering along a temperature gradient. We demonstrate that local environmental differences create rapid shifts in associated microbial community composition with potential functional implications for rapid host acclimation under shifting environmental conditions.

     
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  4. Abstract

    One objective of eco‐evolutionary dynamics is to understand how the interplay between ecology and evolution on contemporary timescales contributes to the maintenance of biodiversity. Disturbance is an ecological process that can alter species diversity through both ecological and evolutionary effects on colonization and extinction dynamics. While analogous mechanisms likely operate among genotypes within a population, empirical evidence demonstrating the relationship between disturbance and genotypic diversity remains limited. We experimentally tested how disturbance altered the colonization (gain) and extinction (loss) of genets within a population of the marine angiospermZostera marina(eelgrass). In a 2‐year field experiment conducted in northern California, we mimicked grazing disturbance by migratory geese by clipping leaves at varying frequencies during the winter months. Surprisingly, we found the greatest rates of new colonization in the absence of disturbance and that clipping had negligible effects on extinction. We hypothesize that genet extinction was not driven by selective mortality from clipping or from any stochastic loss resulting from the reduced shoot densities in clipped plots. We also hypothesize that increased flowering effort and facilitation within and among clones drove the increased colonization of new genets in the undisturbed treatment. This balance between colonization and extinction resulted in a negative relationship between clipping frequency and net changes in genotypic richness. We interpret our results in light of prior work showing that genotypic diversity increased resistance to grazing disturbance. We suggest that both directions of a feedback between disturbance and diversity occur in this system with consequences for the maintenance of eelgrass genotypic diversity.

     
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  5. The extent of parallel genomic responses to similar selective pressures depends on a complex array of environmental, demographic, and evolutionary forces. Laboratory experiments with replicated selective pressures yield mixed outcomes under controlled conditions and our understanding of genomic parallelism in the wild is limited to a few well-established systems. Here, we examine genomic signals of selection in the eelgrass Zostera marina across temperature gradients in adjacent embayments. Although we find many genomic regions with signals of selection within each bay, there is little overlap at the SNP level across bays. We do find overlap at the gene level, potentially suggesting multiple mutational pathways to the same phenotype. Using polygenic models we find that some sets of candidate SNPs are able to predict temperature across both bays, suggesting that small but parallel shifts in allele frequencies may be missed by independent genome scans. Together, these results highlight the continuous rather than binary nature of parallel evolution in polygenic traits and the complexity of evolutionary predictability. 
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  6. Abstract

    Currents are unique drivers of oceanic phylogeography and thus determine the distribution of marine coastal species, along with past glaciations and sea-level changes. Here we reconstruct the worldwide colonization history of eelgrass (Zostera marinaL.), the most widely distributed marine flowering plant or seagrass from its origin in the Northwest Pacific, based on nuclear and chloroplast genomes. We identified two divergent Pacific clades with evidence for admixture along the East Pacific coast. Two west-to-east (trans-Pacific) colonization events support the key role of the North Pacific Current. Time-calibrated nuclear and chloroplast phylogenies yielded concordant estimates of the arrival ofZ. marinain the Atlantic through the Canadian Arctic, suggesting that eelgrass-based ecosystems, hotspots of biodiversity and carbon sequestration, have only been present there for ~243 ky (thousand years). Mediterranean populations were founded ~44 kya, while extant distributions along western and eastern Atlantic shores were founded at the end of the Last Glacial Maximum (~19 kya), with at least one major refuge being the North Carolina region. The recent colonization and five- to sevenfold lower genomic diversity of the Atlantic compared to the Pacific populations raises concern and opportunity about how Atlantic eelgrass might respond to rapidly warming coastal oceans.

     
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    Free, publicly-accessible full text available August 1, 2024
  7. Abstract

    Understanding the mechanisms by which individual organisms respond and populations adapt to global climate change is a critical challenge. The role of plasticity and acclimation, within and across generations, may be essential given the pace of change. We investigated plasticity across generations and life stages in response to ocean acidification (OA), which poses a growing threat to both wild populations and the sustainable aquaculture of shellfish. Most studies of OA on shellfish focus on acute effects, and less is known regarding the longer term carryover effects that may manifest within or across generations. We assessed these longer term effects in red abalone (Haliotis rufescens) using a multi‐generational split‐brood experiment. We spawned adults raised in ambient conditions to create offspring that we then exposed to high pCO2(1180 μatm; simulating OA) or low pCO2(450 μatm; control or ambient conditions) during the first 3 months of life. We then allowed these animals to reach maturity in ambient common garden conditions for 4 years before returning the adults into high or low pCO2treatments for 11 months and measuring growth and reproductive potential. Early‐life exposure to OA in the F1 generation decreased adult growth rate even after 5 years especially when abalone were re‐exposed to OA as adults. Adult but not early‐life exposure to OA negatively impacted fecundity. We then exposed the F2 offspring to high or low pCO2treatments for the first 3 months of life in a fully factorial, split‐brood design. We found negative transgenerational effects of parental OA exposure on survival and growth of F2 offspring, in addition to significant direct effects of OA on F2 survival. These results show that the negative impacts of OA can last within and across generations, but that buffering against OA conditions at critical life‐history windows can mitigate these effects.

     
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  8. Abstract

    The extent of parallel genomic responses to similar selective pressures depends on a complex array of environmental, demographic, and evolutionary forces. Laboratory experiments with replicated selective pressures yield mixed outcomes under controlled conditions and our understanding of genomic parallelism in the wild is limited to a few well‐established systems. Here, we examine genomic signals of selection in the eelgrassZostera marinaacross temperature gradients in adjacent embayments. Although we find many genomic regions with signals of selection within each bay there is very little overlap in signals of selection at the SNP level, despite most polymorphisms being shared across bays. We do find overlap at the gene level, potentially suggesting multiple mutational pathways to the same phenotype. Using polygenic models we find that some sets of candidate SNPs are able to predict temperature across both bays, suggesting that small but parallel shifts in allele frequencies may be missed by independent genome scans. Together, these results highlight the continuous rather than binary nature of parallel evolution in polygenic traits and the complexity of evolutionary predictability.

     
    more » « less