Temporal stability in patterns of genetic diversity and structure of a marine foundation species (Zostera marina).

Genetic diversity and population structure reflect complex interactions among a diverse set of processes that may vary temporally, limiting their potential to predict ecological and evolutionary outcomes. Yet, the stability of these patterns is rarely tested. We resampled eelgrass (Zostera marina) meadows from published studies to determine variability in genetic diversity and structure within and between meadows over 5-12 years. The meadows sampled (San Francisco, Tomales and Bodega Bays in California and the Virginia coastal bays) represent a range of life histories (annual vs perennial), age (well-established vs restored) and environments (rural vs urbanized). In all of these systems, neither diversity nor differentiation (FST) changed over time. Differences among tidal heights within Bodega Bay were also remarkably consistent, with the high intertidal being more diverse than the subtidal, and tidal height differentiation being modest but significant at both time points. Historical studies used only a few microsatellite loci; therefore, our temporal comparisons were based on 4-5 loci. However, analysis of the current data using a set of 12 loci show that 4-5 loci are sufficient to describe diversity and differentiation patterns in this system. This temporal consistency was not because of the resampling of large clones, underscoring the feasibility and relevance of understanding drivers of the differences. Because seagrasses are declining at rapid rates, restoration and conservation are increasingly a coastal management priority. Our results argue that surveys of eelgrass genetic structure and diversity at decadal scales can provide accurate depictions of populations, increasing the utility of published genetic data for restoration and designing networks of reserves.

Trait vs. phylogenetic diversity as predictors of competition and community composition in herbivorous marine amphipods.

Field studies of community assembly patterns increasingly use phylogenetic relatedness as a surrogate for traits. Recent experiments appear to validate this approach by showing effects of correlated trait and phylogenetic distances on coexistence. However, traits governing resource use in animals are often labile. To test whether feeding trait or phylogenetic diversity can predict competition and production in communities of grazing amphipods, we manipulated both types of diversity independently in mesocosms. We found that increasing the feeding trait diversity of the community increased the number of species coexisting, reduced dominance and changed food availability. In contrast, phylogenetic diversity had no effect, suggesting that whatever additional ecological information it represents was not relevant in this context. Although community phylogenetic structure in the field may result from multiple traits with potential for phylogenetic signal, phylogenetic effects on species interactions in controlled experiments may depend on the lability of fewer key traits.

An evolutionary epigenetic clock in plants.

Molecular clocks are the basis for dating the divergence between lineages over macroevolutionary timescales (~105 to 108 years). However, classical DNA-based clocks tick too slowly to inform us about the recent past. Here, we demonstrate that stochastic DNA methylation changes at a subset of cytosines in plant genomes display a clocklike behavior. This "epimutation clock" is orders of magnitude faster than DNA-based clocks and enables phylogenetic explorations on a scale of years to centuries. We show experimentally that epimutation clocks recapitulate known topologies and branching times of intraspecies phylogenetic trees in the self-fertilizing plant Arabidopsis thaliana and the clonal seagrass Zostera marina, which represent two major modes of plant reproduction. This discovery will open new possibilities for high-resolution temporal studies of plant biodiversity.

Plant genotype and nitrogen loading influence seagrass productivity, biochemistry, and plant-herbivore interactions.

Genetic variation within and among key species can have significant ecological consequences at the population, community, and ecosystem levels. In order to understand ecological properties of systems based on habitat-forming clonal plants, it is crucial to clarify which traits vary among plant genotypes and how they influence ecological processes, and to assess their relative contribution to ecosystem functioning in comparison to other factors. Here we used a mesocosm experiment to examine the relative influence of genotypic identity and extreme levels of nitrogen loading on traits that affect ecological processes (at the population, community, and ecosystem levels) for Zostera marina, a widespread marine angiosperm that forms monospecific meadows throughout coastal areas in the Northern Hemisphere. We found effects of both genotype and nitrogen addition on many plant characteristics (e.g., aboveground and belowground biomass), and these were generally strong and similar in magnitude, whereas interactive effects were rare. Genotypes also strongly differed in susceptibility to herbivorous isopods, with isopod preference among genotypes generally matching their performance in terms of growth and survival. Chemical rather than structural differences among genotypes drove these differences in seagrass palatability. Nitrogen addition uniformly decreased plant palatability but did not greatly alter the relative preferences of herbivores among genotypes, indicating that genotype effects are strong. Our results highlight that differences in key traits among genotypes of habitat-forming species can have important consequences for the communities and ecosystems that depend on them and that such effects are not overwhelmed by known environmental stressors.

Evolution of decoration in majoid crabs: a comparative phylogenetic analysis of the role of body size and alternative defensive strategies.

Although experimental studies have demonstrated the antipredatory advantages of camouflage and its associated costs, few studies have examined the evolution of camouflage in a phylogenetic context. We use phylogenetic comparative methods to examine evolutionary trade-offs associated with camouflage in the crab superfamily Majoidea. The majoids, or spider crabs, are known for their decoration behavior in which they attach materials from their environment to hooked setae on their carapace. We found that coverage of hooked setae on a crab (morphology) strongly predicts decoration cover in the field (behavior). Half of the species examined exhibited decreases in the coverage of hooked setae with ontogeny, and we also found a strong negative correlation between the extent of hooked setae and adult body size among species using independent contrasts, suggesting that size may constrain the evolution of camouflage. Finally, using a well-resolved clade of epialtids (kelp crabs)--many of which decorate little but use color change as an alternative camouflage strategy--we found a negative correlation between utilization of decoration versus color camouflage strategies. Our findings suggest that the costs of hook production and decoration maintenance and/or the lowered adaptive value of camouflage for larger species may limit the evolutionary distribution of decoration camouflage among the majoids.

Molecular phylogeny of the brachyuran crab superfamily Majoidea indicates close congruence with trees based on larval morphology.

In this study, we constructed the first molecular phylogeny of the diverse crab superfamily Majoidea (Decapoda: Pleocyemata: Brachyura), using three loci (16S, COI, and 28S) from 37 majoid species. We used this molecular phylogeny to evaluate evidence for phylogenetic hypotheses based on larval and adult morphology. Our study supports several relationships predicted from larval morphology. These include a monophyletic Oregoniidae family branching close to the base of the tree; a close phylogenetic association among the Epialtidae, Pisidae, Tychidae, and Mithracidae families; and some support for the monophyly of the Inachidae and Majidae families. However, not all majoid families were monophyletic in our molecular tree, providing weaker support for phylogenetic hypotheses inferred strictly from adult morphology (i.e., monophyly of individual families). This suggests the adult morphological characters traditionally used to classify majoids into different families may be subject to convergence. Furthermore, trees constructed with data from any single locus were more poorly resolved than trees constructed from the combined dataset, suggesting that utilization of multiple loci are necessary to reconstruct relationships in this group.

The invasion paradox: reconciling pattern and process in species invasions.

The invasion paradox describes the co-occurrence of independent lines of support for both a negative and a positive relationship between native biodiversity and the invasions of exotic species. The paradox leaves the implications of native-exotic species richness relationships open to debate: Are rich native communities more or less susceptible to invasion by exotic species? We reviewed the considerable observational, experimental, and theoretical evidence describing the paradox and sought generalizations concerning where and why the paradox occurs, its implications for community ecology and assembly processes, and its relevance for restoration, management, and policy associated with species invasions. The crux of the paradox concerns positive associations between native and exotic species richness at broad spatial scales, and negative associations at fine scales, especially in experiments in which diversity was directly manipulated. We identified eight processes that can generate either negative or positive native-exotic richness relationships, but none can generate both. As all eight processes have been shown to be important in some systems, a simple general theory of the paradox, and thus of the relationship between diversity and invasibility, is probably unrealistic. Nonetheless, we outline several key issues that help resolve the paradox, discuss the difficult juxtaposition of experimental and observational data (which often ask subtly different questions), and identify important themes for additional study. We conclude that natively rich ecosystems are likely to be hotspots for exotic species, but that reduction of local species richness can further accelerate the invasion of these and other vulnerable habitats.

Hydroid defenses against predators: the importance of secondary metabolites versus nematocysts.

Marine hydroids are commonly thought to be defended by stinging organelles called nematocysts that penetrate predator tissues and inject proteinaceous venoms, but not all hydroids possess these nematocysts. Although an increasing number of bioactive secondary metabolites have been isolated from marine hydroids, ecological roles of these compounds are poorly known. To test the hypothesis that nematocysts and noxious secondary metabolites represent alternative defenses against predation, we examined hydroids from North Carolina, United States for: (1) the palatability of whole polyps before and after nematocysts had been deactivated; (2) the palatability of their chemical extracts; and (3) their nutritional value in terms of organic content, protein content, and levels of refractory structural material (chitin). All hydroids were avoided by a generalist predator, the pinfish Lagodon rhomboides, compared with palatable control foods. Two of these (Halocordyle disticha and Tubularia crocea) became palatable after being treated with potassium chloride to discharge their nematocysts, suggesting that these species rely on nematocysts for defenses against predators. Chemical extracts from nematocyst-defended species had no effect on fish feeding. The four species that remained unpalatable after nematocysts had been discharged (Corydendrium parasiticum, Eudendrium carneum, Hydractinia symbiolongicarpus, Tridentata marginata) possessed chemical extracts that deterred feeding by pinfish. We have isolated and characterized the structures of the deterrent metabolites in two of these species. We found no differences in nutritional content or levels of chitin between nematocyst-defended and chemically defended species, and no evidence that either of these played a role in the rejection of hydroids as prey. Our results suggest that, among hydroids, chemical defenses may be at least as common as nematocyst-based defenses and that the two may represent largely alternative defensive strategies. The four hydroid species with deterrent extracts represent four families and both sub-orders of hydroids, suggesting that chemical defenses in this group may be widespread and have multiple origins.