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Coastal wetland resilience through local, regional and global conservation

Coastal wetlands, including tidal marshes, mangrove forests and tidal flats, support the livelihoods of millions of people. Understanding the resilience of coastal wetlands to the increasing number and intensity of anthropogenic threats (such as habitat conversion, pollution, fishing and climate change) can inform what conservation actions will be effective. In this Review, we synthesize anthropogenic threats to coastal wetlands and their resilience through the lens of scale. Over decades and centuries, anthropogenic threats have unfolded across local, regional and global scales, reducing both the extent and quality of coastal wetlands. The resilience of existing coastal wetlands is driven by their quality, which is modulated by both physical conditions (such as sediment supply) and ecological conditions (such as species interactions operating from local through to global scales). Protection and restoration efforts, however, are often localized and focus on the extent of coastal wetlands. The future of coastal wetlands will depend on an improved understanding of their resilience, and on society’s actions to enhance both their extent and quality across different scales.

Dispersal, habitat filtering, and eco-evolutionary dynamics as drivers of local and global wetland viral biogeography

Wetlands store 20–30% of the world’s soil carbon, and identifying the microbial controls on these carbon reserves is essential to predicting feedbacks to climate change. Although viral infections likely play important roles in wetland ecosystem dynamics, we lack a basic understanding of wetland viral ecology. Here 63 viral size-fraction metagenomes (viromes) and paired total metagenomes were generated from three time points in 2021 at seven fresh- and saltwater wetlands in the California Bodega Marine Reserve. We recovered 12,826 viral population genomic sequences (vOTUs), only 4.4% of which were detected at the same field site two years prior, indicating a small degree of population stability or recurrence. Viral communities differed most significantly among the seven wetland sites and were also structured by habitat (plant community composition and salinity). Read mapping to a new version of our reference database, PIGEONv2.0 (515,763 vOTUs), revealed 196 vOTUs present over large geographic distances, often reflecting shared habitat characteristics. Wetland vOTU microdiversity was significantly lower locally than globally and lower within than between time points, indicating greater divergence with increasing spatiotemporal distance. Viruses tended to have broad predicted host ranges via CRISPR spacer linkages to metagenome-assembled genomes, and increased SNP frequencies in CRISPR-targeted major tail protein genes suggest potential viral eco-evolutionary dynamics in response to both immune targeting and changes in host cell receptors involved in viral attachment. Together, these results highlight the importance of dispersal, environmental selection, and eco-evolutionary dynamics as drivers of local and global wetland viral biogeography.

Accelerated differentiation of neo-W nuclear-encoded mitochondrial genes between two climate-associated bird lineages signals potential co-evolution with mitogenomes

There is considerable evidence for mitochondrial-nuclear co-adaptation as a key evolutionary driver. Hypotheses regarding the roles of sex-linkage have emphasized Z-linked nuclear genes with mitochondrial function (N-mt genes), whereas it remains contentious whether the perfect co-inheritance of W genes with mitogenomes could hinder or facilitate co-adaptation. Young (neo-) sex chromosomes that possess relatively many N-mt genes compared to older chromosomes provide unprecedented hypothesis-testing opportunities. Eastern Yellow Robin (EYR) lineages in coastal and inland habitats with different climates are diverged in mitogenomes, and in a ~ 15.4 Mb nuclear region enriched with N-mt genes, in contrast with otherwise-similar nuclear genomes. This nuclear region maps to passerine chromosome 1A, previously found to be neo-sex in the inland EYR genome. To compare sex-linked Chr1A-derived genes between lineages, we assembled and annotated the coastal EYR genome. We found that: (i) the coastal lineage shares a similar neo-sex system with the inland lineage, (ii) neo-W and neo-Z N-mt genes are not more diverged between lineages than are comparable non-N-mt genes, and showed little evidence for broad positive selection, (iii) however, W-linked N-mt genes are more diverged between lineages than are their Z-linked gametologs. The latter effect was ~7 times stronger for N-mt than non-N-mt genes, suggesting that W-linked N-mt genes might have diverged between lineages under environmental selection through co-evolution with mitogenomes. Finally, we identify a candidate gene driver for divergent selection, NDUFA12. Our data represent a rare example suggesting a possible role for W-associated mitochondrial-nuclear interactions in climate-associated adaptation and lineage differentiation.

Impact of climate-induced water-table drawdown on carbon and nitrogen sequestration in a Kobresia-dominated peatland on the central Qinghai-Tibetan Plateau

Peatlands on the Qinghai-Tibetan Plateau (QTP) represent one of the world’s largest reservoirs of soil organic carbon (C) and nitrogen (N), but their future stability is uncertain. This study utilizes high-resolution multi-core records of C and N contents, stable isotopes, and infrared spectroscopy to reconstruct water table depths and their impacts on C and N accumulation and decomposition over the past 2.7 kyr in a slope peatland from the central QTP. Our paleo records reveal that increased decomposition in the surface oxic layer has led to decreased C and N accumulation rates over the last millennium, primarily due to water-table drawdown driven by climate warming and drying. Supporting evidence from nearby records suggests that this trend of surface drying may be widespread across QTP peatlands. Despite this, QTP peatlands retain some of the highest 1-m C and N densities globally, with values of 54.1 ± 18.9 kg C m-2 and 3.2 ± 1.5 kg N m-2. These findings highlight the vulnerability of substantial C and N reservoirs and sequestration capabilities in QTP peatlands to continued water table declines in a warming and drying climate.

Protein signatures predict coral resilience and survival to thermal bleaching events

Coral bleaching events from thermal stress are increasing globally in duration, frequency, and intensity. While bleaching can cause mortality, some corals survive, reacquire symbionts, and recover. We experimentally bleached Montipora capitata to examine molecular and physiological differences between corals that recover (resilient) and those that die (susceptible). Corals were collected and monitored for eight months post-bleaching to identify genets with long-term resilience. Using an integrated systems-biology approach that included quantitative proteomics, 16S rRNA sequencing to characterize the coral microbiome, total coral lipids, symbiont community composition and density, we explored molecular-level mechanisms of tolerance in corals pre- and post-bleaching. Prior to thermal stress, resilient corals have a more diverse microbiome and abundant proteins essential for carbon acquisition, symbiont retention, and pathogen resistance. Protein signatures of susceptible corals showed early symbiont rejection and utilized urea for carbon and nitrogen. Our results reveal molecular factors for surviving bleaching events and identify diagnostic protein biomarkers for reef management and restoration.

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