The dimensionality of infection networks among viruses infecting microbial eukaryotes and bacteria.

Diverse viruses and their hosts are interconnected through complex networks of infection, which are thought to influence ecological and evolutionary processes, but the principles underlying infection network structure are not well understood. Here we focus on network dimensionality and how it varies across 37 networks of viruses infecting eukaryotic phytoplankton and bacteria. We find that dimensionality is often strikingly low, with most networks being one- or two-dimensional, although dimensionality increases with network richness, suggesting that the true dimensionality of natural systems is higher. Low-dimensional networks generally exhibit a mixture of host partitioning among viruses and nestededness of host ranges. Networks of bacteria-infecting and eukaryote-infecting viruses possess comparable distributions of dimensionality and prevalence of nestedness, indicating that fundamentals of network structure are similar among domains of life and different viral lineages. The relative simplicity of many infection networks suggests that coevolutionary dynamics are often driven by a modest number of underlying mechanisms.

Trophic strategies explain the ocean niches of small eukaryotic phytoplankton.

A large fraction of marine primary production is performed by diverse small protists, and many of these phytoplankton are phagotrophic mixotrophs that vary widely in their capacity to consume bacterial prey. Prior analyses suggest that mixotrophic protists as a group vary in importance across ocean environments, but the mechanisms leading to broad functional diversity among mixotrophs, and the biogeochemical consequences of this, are less clear. Here we use isolates from seven major taxa to demonstrate a tradeoff between phototrophic performance (growth in the absence of prey) and phagotrophic performance (clearance rate when consuming Prochlorococcus). We then show that trophic strategy along the autotrophy-mixotrophy spectrum correlates strongly with global niche differences, across depths and across gradients of stratification and chlorophyll a. A model of competition shows that community shifts can be explained by greater fitness of faster-grazing mixotrophs when nutrients are scarce and light is plentiful. Our results illustrate how basic physiological constraints and principles of resource competition can organize complexity in the surface ocean ecosystem.

Broad phylogenetic and functional diversity among mixotrophic consumers of Prochlorococcus.

Small eukaryotic phytoplankton are major contributors to global primary production and marine biogeochemical cycles. Many taxa are thought to be mixotrophic, but quantitative studies of phagotrophy exist for very few. In addition, little is known about consumers of Prochlorococcus, the abundant cyanobacterium at the base of oligotrophic ocean food webs. Here we describe thirty-nine new phytoplankton isolates from the North Pacific Subtropical Gyre (Station ALOHA), all flagellates ~2-5 µm diameter, and we quantify their ability to graze Prochlorococcus. The mixotrophs are from diverse classes (dictyochophytes, haptophytes, chrysophytes, bolidophytes, a dinoflagellate, and a chlorarachniophyte), many from previously uncultured clades. Grazing ability varied substantially, with specific clearance rate (volume cleared per body volume) varying over ten-fold across isolates and six-fold across genera. Slower grazers tended to create more biovolume per prey biovolume consumed. Using qPCR we found that the haptophyte Chrysochromulina was most abundant among the isolated mixotrophs at Station ALOHA, with 76-250 cells mL-1 across depths in the upper euphotic zone (5-100 m). Our results show that within a single ecosystem the phototrophs that ingest bacteria come from many branches of the eukaryotic tree, and are functionally diverse, indicating a broad range of strategies along the spectrum from phototrophy to phagotrophy.

Towards an integrative view of virus phenotypes.

Understanding how phenotypes emerge from genotypes is a foundational goal in biology. As challenging as this task is when considering cellular life, it is further complicated in the case of viruses. During replication, a virus as a discrete entity (the virion) disappears and manifests itself as a metabolic amalgam between the virus and the host (the virocell). Identifying traits that unambiguously constitute a virus's phenotype is straightforward for the virion, less so for the virocell. Here, we present a framework for categorizing virus phenotypes that encompasses both virion and virocell stages and considers functional and performance traits of viruses in the context of fitness. Such an integrated view of virus phenotype is necessary for comprehensive interpretation of viral genome sequences and will advance our understanding of viral evolution and ecology.

Making sense of virus size and the tradeoffs shaping viral fitness.

Viruses span an impressive size range, with genome length varying a thousandfold and virion volume nearly a millionfold. For cellular organisms the scaling of traits with size is a pervasive influence on ecological processes, but whether size plays a central role in viral ecology is unknown. Here, we focus on viruses of aquatic unicellular organisms, which exhibit the greatest known range of virus size. We outline hypotheses within a quantitative framework, and analyse data where available, to consider how size affects the primary components of viral fitness. We argue that larger viruses have fewer offspring per infection and slower contact rates with host cells, but a larger genome tends to increase infection efficiency, broaden host range, and potentially increase attachment success and decrease decay rate. These countervailing selective pressures may explain why a breadth of sizes exist and even coexist when infecting the same host populations. Oligotrophic ecosystems may be enriched in "giant" viruses, because environments with resource-limited phagotrophs at low concentrations may select for broader host range, better control of host metabolism, lower decay rate and a physical size that mimics bacterial prey. Finally, we describe where further research is needed to understand the ecology and evolution of viral size diversity.

Mixotrophy in nanoflagellates across environmental gradients in the ocean.

Mixotrophy, the combination of autotrophic and heterotrophic nutrition, is a common trophic strategy among unicellular eukaryotes in the ocean. There are a number of hypotheses about the conditions that select for mixotrophy, and field studies have documented the prevalence of mixotrophy in a range of environments. However, there is currently little evidence for how mixotrophy varies across environmental gradients, and whether empirical patterns support theoretical predictions. Here I synthesize experiments that have quantified the abundance of phototrophic, mixotrophic, and heterotrophic nanoflagellates, to ask whether there are broad patterns in the prevalence of mixotrophy (relative to pure autotrophy and heterotrophy), and to ask whether observed patterns are consistent with a trait-based model of trophic strategies. The data suggest that mixotrophs increase in abundance at lower latitudes, while autotrophs and heterotrophs do not, and that this may be driven by increased light availability. Both mixotrophs and autotrophs increase greatly in productive coastal environments, while heterotrophs increase only slightly. These patterns are consistent with a model of resource competition in which nutrients and carbon can both limit growth and mixotrophs experience a trade-off in allocating biomass to phagotrophy vs. autotrophic functions. Importantly, mixotrophy is selected for under a range of conditions even when mixotrophs experience a penalty for using a generalist trophic strategy, due to the synergy between photosynthetically derived carbon and prey-derived nutrients. For this reason mixotrophy is favored relative to specialist strategies by increased irradiance, while at the same time increased nutrient supply increases the competitive ability of mixotrophs against heterotrophs.

Evolutionarily stable communities: a framework for understanding the role of trait evolution in the maintenance of diversity.

Biological diversity depends on the interplay between evolutionary diversification and ecological mechanisms allowing species to coexist. Current research increasingly integrates ecology and evolution over a range of timescales, but our common conceptual framework for understanding species coexistence requires better incorporation of evolutionary processes. Here, we focus on the idea of evolutionarily stable communities (ESCs), which are theoretical endpoints of evolution in a community context. We use ESCs as a unifying framework to highlight some important but under-appreciated theoretical results, and we review empirical research relevant to these theoretical predictions. We explain how, in addition to generating diversity, evolution can also limit diversity by reducing the effectiveness of coexistence mechanisms. The coevolving traits of competing species may either diverge or converge, depending on whether the number of species in the community is low (undersaturated) or high (oversaturated) relative to the ESC. Competition in oversaturated communities can lead to extinction or neutrally coexisting, ecologically equivalent species. It is critical to consider trait evolution when investigating fundamental ecological questions like the strength of different coexistence mechanisms, the feasibility of ecologically equivalent species, and the interpretation of different patterns of trait dispersion.

Host Traits Drive Viral Life Histories across Phytoplankton Viruses.

Viruses are integral to ecological and evolutionary processes, but we have a poor understanding of what drives variation in key traits across diverse viruses. For lytic viruses, burst size, latent period, and genome size are primary characteristics controlling host-virus dynamics. Here we synthesize data on these traits for 75 strains of phytoplankton viruses, which play an important role in global biogeochemistry. We find that primary traits of the host (genome size, growth rate) explain 40%-50% of variation in burst size and latent period. Specifically, burst size and latent period both exhibit saturating relationships versus the host∶virus genome size ratio, with both traits increasing at low genome size ratios while showing no relationship at high size ratios. In addition, latent period declines as host growth rate increases. We analyze a model of latent period evolution to explore mechanisms that could cause these patterns. The model predicts that burst size may often be set by the host genomic resources available for viral construction, while latent period evolves to permit this maximal burst size, modulated by host metabolic rate. These results suggest that general mechanisms may underlie the evolution of diverse viruses. Future extensions of this work could help explain viral regulation of host populations, viral influence on community structure and diversity, and viral roles in biogeochemical cycles.

Community trait structure in phytoplankton: seasonal dynamics from a method for sparse trait data.

The distribution of functional traits in communities, and how trait distributions shift over time and space, is critical information for understanding community structure, the maintenance of diversity, and community effects on ecosystem function. It is often the case that traits tightly linked to ecological performance, such as physiological capacities, are laborious to measure and largely unknown for speciose communities; however, these traits are particularly important for unraveling the mechanistic basis of community structure. Here I develop a method combining sparse trait data with a statistical niche model to infer trait distributions for phytoplankton communities and how they vary over 10 yr in the western English Channel. I find that community-average nitrate affinity, light-limited growth rate, and maximum growth rate all show major seasonal patterns, reflecting alternate limitation by light vs. nitrogen. Trait diversity exhibits a variety of patterns distinct from community trait means, which suggests complex regulation of functional diversity. Patterns such as these are important for predicting how ocean ecosystems will respond to global change, and for developing trait-based models of emergent community structure. The statistical approach used here could be applied to any kind of organism, if it exhibits strong relationships between traits and statistical niche estimates.

Microbial resource utilization traits and trade-offs: implications for community structure, functioning, and biogeochemical impacts at present and in the future.

Trait-based approaches provide a mechanistic framework to understand and predict the structure and functioning of microbial communities. Resource utilization traits and trade-offs are among key microbial traits that describe population dynamics and competition among microbes. Several important trade-offs have been identified for prokaryotic and eukaryotic microbial taxa that define contrasting ecological strategies and contribute to species coexistence and diversity. The shape, dimensionality, and hierarchy of trade-offs may determine coexistence patterns and need to be better characterized. Laboratory measured resource utilization traits can be used to explain temporal and spatial structure and dynamics of natural microbial communities and predict biogeochemical impacts. Global environmental change can alter microbial community composition through altering resource utilization by different microbes and, consequently, may modify biogeochemical impacts of microbes.

Volatile communication between plants that affects herbivory: a meta-analysis.

Volatile communication between plants causing enhanced defence has been controversial. Early studies were not replicated, and influential reviews questioned the validity of the phenomenon. We collected 48 well-replicated studies and found overall support for the hypothesis that resistance increased for individuals with damaged neighbours. Laboratory or greenhouse studies and those conducted on agricultural crops showed stronger induced resistance than field studies on undomesticated species, presumably because other variation had been reduced. A cumulative analysis revealed that early, non-replicated studies were more variable and showed less evidence for communication. Effects of habitat and plant growth form were undetectable. In most cases, the mechanisms of resistance and alternative hypotheses were not considered. There was no indication that some response variables were more likely to produce large effects. These results indicate that plants of diverse taxonomic affinities and ecological conditions become more resistant to herbivores when exposed to volatiles from damaged neighbours.

A three-way trade-off maintains functional diversity under variable resource supply.

The resources that organisms depend on often fluctuate over time, and a variety of common traits are thought to be adaptations to variable resource supply. To understand the trait structure of communities, it is necessary to understand the functional trade-offs that determine what trait combinations are possible and which species can persist and coexist in a given environment. We compare traits across phytoplankton species in order to test for proposed trade-offs between maximum growth rate, equilibrium competitive ability for phosphorus (P), and ability to store P. We find evidence for a three-way trade-off between these traits, and we use empirical trait covariation to parameterize a mechanistic model of competition under pulsed P supply. The model shows that different strategies are favored under different conditions of nutrient supply regime, productivity, and mortality. Furthermore, multiple strategies typically coexist, and the range of traits that persist in the model is similar to the range of traits found in real species. These results suggest that mechanistic models informed by empirical trait variation, in combination with data on the trait structure of natural communities, will play an important role in uncovering the mechanisms that underlie the diversity and structure of ecological communities.

Functional traits explain phytoplankton responses to environmental gradients across lakes of the United States.

Ecological communities exhibit regular shifts in structure along environmental gradients, but it has proved difficult to dissect the mechanisms by which environmental conditions determine the relative success of species. Functional traits may provide a link between environmental drivers and mechanisms of community membership, but this has not been well tested for phytoplankton, which dominate primary production in many aquatic ecosystems. Here we test whether functional traits of phytoplankton can explain how species respond to gradients of light and phosphorus across U.S. lakes. We find that traits related to light utilization and maximum growth rate can predict species' differential responses to the relative availability of these resources. These results show that laboratory-measured traits are predictive of species' performance under natural conditions, that functional traits provide a mechanistic foundation for community ecology, and that variation in community structure is predictable in spite of the complexity of ecological communities.

The biogeography of marine plankton traits.

Changes in marine plankton communities driven by environmental variability impact the marine food web and global biogeochemical cycles of carbon and other elements. To predict and assess these community shifts and their consequences, ecologists are increasingly investigating how the functional traits of plankton determine their relative fitness along environmental and biological gradients. Laboratory, field and modelling studies are adopting this trait-based approach to map the biogeography of plankton traits that underlies variations in plankton communities. Here, we review progress towards understanding the regulatory roles of several key plankton functional traits, including cell size, N2 -fixation and mixotrophy among phytoplankton, and body size, ontogeny and feeding behaviour for zooplankton. The trait biogeographical approach sheds light on what structures plankton communities in the current ocean, as well as under climate change scenarios, and also allows for finer resolution of community function because community trait composition determines the rates of significant processes, including carbon export. Although understanding of trait biogeography is growing, uncertainties remain that stem, in part, from the paucity of observations describing plankton functional traits. Thus, in addition to recommending widespread adoption of the trait-based approach, we advocate for enhanced collection, standardisation and dissemination of plankton functional trait data.

Functional traits explain phytoplankton community structure and seasonal dynamics in a marine ecosystem.

A fundamental yet elusive goal of ecology is to predict the structure of communities from the environmental conditions they experience. Trait-based approaches to terrestrial plant communities have shown that functional traits can help reveal the mechanisms underlying community assembly, but such approaches have not been tested on the microbes that dominate ecosystem processes in the ocean. Here, we test whether functional traits can explain community responses to seasonal environmental fluctuation, using a time series of the phytoplankton of the English Channel. We show that interspecific variation in response to major limiting resources, light and nitrate, can be well-predicted by lab-measured traits characterising light utilisation, nitrate utilisation and maximum growth rate. As these relationships were predicted a priori, using independently measured traits, our results show that functional traits provide a strong mechanistic foundation for understanding the structure and dynamics of ecological communities.

Evidence for a three-way trade-off between nitrogen and phosphorus competitive abilities and cell size in phytoplankton.

Trade-offs among functional traits are essential for explaining community structure and species coexistence. While two-way trade-offs have been investigated in many systems, higher-dimensional trade-offs remain largely hypothetical. Here we demonstrate a three-way trade-off between cell size and competitive abilities for nitrogen and phosphorus in marine and freshwater phytoplankton. At a given cell size, competitive abilities for N and P are negatively correlated, but as cell size increases, competitive ability decreases for both nutrients. The relative importance of the two trade-off axes appears to be environment dependent, suggesting different selective pressures: freshwater phytoplankton separate more along the N vs. P competition axis, and marine phytoplankton separate more along the nutrient competition vs. cell size axis. Our results demonstrate the multidimensional nature of key trade-offs among traits and suggest that such trade-offs may drive species interactions and structure ecological communities.

Spatially stochastic settlement and the coexistence of benthic marine animals.

For sessile organisms, dispersal and recruitment are typically spatially stochastic, but there is little understanding of how this variability scales up to influence processes such as competitive coexistence. Here we argue that coexistence of benthic marine animals is enhanced by stochastic differences between species in the spatial distribution of larval settlement. Differentiation of settlement distributions among competitors results in intraspecifically aggregated settlement, which can reduce overall interspecific competition and increase overall intraspecific competition. We test for the components of this mechanism using a pair of subtidal invertebrates, and we find that the mean interspecific effect of the dominant competitor is substantially reduced by natural settlement variability. Using a simulation parameterized with experimental data, we find that variable settlement could play an important role in long-term coexistence between these species. This mechanism may apply broadly to benthic marine communities, which can be highly diverse and typically exhibit large settlement fluctuation over a range of scales.

Multivariate trade-offs, succession, and phenological differentiation in a guild of colonial invertebrates.

For competing species limited by one or few resources, diversity is thought to be maintained by trade-offs that allow niche differentiation without resource partitioning. However, few studies have quantified multiple key traits for each species in a guild and shown that trade-offs among these traits apply across the guild. Here we document strong bivariate and multivariate relationships among growth rate, fecundity, longevity, and overgrowth ability for six co-occurring colonial invertebrates. We find that all four of these traits are constrained to a single "fast-slow" niche axis that mechanistically relates life history variation to a colonization-competition trade-off. The location of species on this axis strongly predicts the timing of their peak abundance during succession. We also find that species closer to each other on the fast-slow axis are more likely to differ in reproductive phenology, suggesting a secondary dimension of niche differentiation for otherwise similar species.

Prey diversity is associated with weaker consumer effects in a meta-analysis of benthic marine experiments.

A rapidly accumulating body of research has shown that species diversity consistently affects the functioning of ecosystems. The incorporation of trophic complexity and the extension of this research to larger scales and natural ranges in species diversity remain as important challenges for understanding the true magnitude of these effects in natural systems. Here, we test whether the diversity of prey communities affects the magnitude of aggregate consumer effects. We conducted a meta-analysis of 57 consumer removal field experiments from a range of intertidal and subtidal hard substrate marine communities. We found that the richness of the prey community was the strongest predictor of the magnitude of consumer effects while controlling for habitat type, taxonomic composition, and other variables. Consumer removal increased aggregate prey abundance on average by 1200% at the lower limit of prey diversity (two species), but only 200% at the upper limit of 37 species. Importantly, compositional change was substantial at both high and low prey diversity, suggesting predation intensity did not vary with prey richness. Rather diverse prey communities appear to be more capable of maintaining abundance via compensatory responses, by containing prey species that are resistant to (or tolerant of) predators. These results suggest that the effects of species diversity on trophic interactions may scale consistently from small-scale manipulations to cross-community comparisons.

Genetic, genomic, and functional analysis of the granule lattice proteins in Tetrahymena secretory granules.

In some cells, the polypeptides stored in dense core secretory granules condense as ordered arrays. In ciliates such as Tetrahymena thermophila, the resulting crystals function as projectiles, expanding upon exocytosis. Isolation of granule contents previously defined five Granule lattice (Grl) proteins as abundant core constituents, whereas a functional screen identified a sixth family member. We have now expanded this screen to identify the nonredundant components required for projectile assembly. The results, further supported by gene disruption experiments, indicate that six Grl proteins define the core structure. Both in vivo and in vitro data indicate that core assembly begins in the endoplasmic reticulum with formation of specific hetero-oligomeric Grl proprotein complexes. Four additional GRL-like genes were found in the T. thermophila genome. Grl2p and Grl6p are targeted to granules, but the transcripts are present at low levels and neither is essential for core assembly. The DeltaGRL6 cells nonetheless showed a subtle change in granule morphology and a marked reduction in granule accumulation. Epistasis analysis suggests this results from accelerated loss of DeltaGRL6 granules, rather than from decreased synthesis. Our results not only provide insight into the organization of Grl-based granule cores but also imply that the functions of Grl proteins extend beyond core assembly.