Dual thermal ecotypes coexist within a nearly genetically identical population of the unicellular marine cyanobacterium Synechococcus.

The extent and ecological significance of intraspecific functional diversity within marine microbial populations is still poorly understood, and it remains unclear if such strain-level microdiversity will affect fitness and persistence in a rapidly changing ocean environment. In this study, we cultured 11 sympatric strains of the ubiquitous marine picocyanobacterium Synechococcus isolated from a Narragansett Bay (RI) phytoplankton community thermal selection experiment. Thermal performance curves revealed selection at cool and warm temperatures had subdivided the initial population into thermotypes with pronounced differences in maximum growth temperatures. Curiously, the genomes of all 11 isolates were almost identical (average nucleotide identities of >99.99%, with >99% of the genome aligning) and no differences in gene content or single nucleotide variants were associated with either cool or warm temperature phenotypes. Despite a very high level of genomic similarity, sequenced epigenomes for two strains showed differences in methylation on genes associated with photosynthesis. These corresponded to measured differences in photophysiology, suggesting a potential pathway for future mechanistic research into thermal microdiversity. Our study demonstrates that present-day marine microbial populations can harbor cryptic but environmentally relevant thermotypes which may increase their resilience to future rising temperatures.

Ecological limits to evolutionary rescue.

Environments change, for both natural and anthropogenic reasons, which can threaten species persistence. Evolutionary adaptation is a potentially powerful mechanism to allow species to persist in these changing environments. To determine the conditions under which adaptation will prevent extinction (evolutionary rescue), classic quantitative genetics models have assumed a constantly changing environment. They predict that species traits will track a moving environmental optimum with a lag that approaches a constant. If fitness is negative at this lag, the species will go extinct. There have been many elaborations of these models incorporating increased genetic realism. Here, we review and explore the consequences of four ecological complications: non-quadratic fitness functions, interacting density- and trait-dependence, species interactions and fundamental limits to adaptation. We show that non-quadratic fitness functions can result in evolutionary tipping points and existential crises, as can the interaction between density- and trait-dependent mortality. We then review the literature on how interspecific interactions affect adaptation and persistence. Finally, we suggest an alternative theoretical framework that considers bounded environmental change and fundamental limits to adaptation. A research programme that combines theory and experiments and integrates across organizational scales will be needed to predict whether adaptation will prevent species extinction in changing environments. This article is part of the theme issue 'Integrative research perspectives on marine conservation'.

Genomic and Fitness Consequences of Genetic Rescue in Wild Populations.

Gene flow is an enigmatic evolutionary force because it can limit adaptation but may also rescue small populations from inbreeding depression [1-3]. Several iconic examples of genetic rescue-increased population growth caused by gene flow [4, 5]-have reversed population declines [6, 7]. However, concerns about outbreeding depression and maladaptive gene flow limit the use of human-mediated gene flow in conservation [8, 9]. Rescue effects of immigration through demographic and/or genetic mechanisms have received theoretical and empirical support, but studies that monitor initial and long-term effects of gene flow on individuals and populations in the wild are lacking. Here, we used individual-based mark-recapture, multigenerational pedigrees, and genomics to test the demographic and evolutionary consequences of manipulating gene flow in two isolated, wild Trinidadian guppy populations. Recipient and source populations originated from environments with different predation, flow, and resource regimes [10]. We documented 10-fold increases in population size following gene flow and found that, on average, hybrids lived longer and reproduced more than residents and immigrants. Despite overall genomic homogenization, alleles potentially associated with local adaptation were not entirely swamped by gene flow. Our results suggest that genetic rescue was caused not just by increasing individual genetic diversity, rather new genomic variation from immigrants combined with alleles from the recipient population resulted in highly fit hybrids and subsequent increases in population size. Contrary to the classic view of maladaptive gene flow, our study reveals conditions under which immigration can produce long-term fitness benefits in small populations without entirely swamping adaptive variation.

Nitrogen limitation inhibits marine diatom adaptation to high temperatures.

Ongoing climate change is shifting species distributions and increasing extinction risks globally. It is generally thought that large population sizes and short generation times of marine phytoplankton may allow them to adapt rapidly to global change, including warming, thus limiting losses of biodiversity and ecosystem function. Here, we show that a marine diatom survives high, previously lethal, temperatures after adapting to above-optimal temperatures under nitrogen (N)-replete conditions. N limitation, however, precludes thermal adaptation, leaving the diatom vulnerable to high temperatures. A trade-off between high-temperature tolerance and increased N requirements may explain why N limitation inhibited adaptation. Because oceanic N limitation is common and likely to intensify in the future, the assumption that phytoplankton will readily adapt to rising temperatures may need to be reevaluated.

Live cell analysis at sea reveals divergent thermal performance between photosynthetic ocean microbial eukaryote populations.

Experimentation at sea provides insight into which traits of ocean microbes are linked to performance in situ. Here we show distinct patterns in thermal tolerance of microbial phototrophs from adjacent water masses sampled in the south-west Pacific Ocean, determined using a fluorescent marker for reactive oxygen species (ROS). ROS content of pico-eukaryotes was assessed after 1, 5 and 25 h of incubation along a temperature gradient (15.6-32.1 °C). Pico-eukaryotes from the East Australian Current (EAC) had relatively constant ROS and showed greatest mortality after 25 h at 7 °C below ambient, whereas those from the Tasman Sea had elevated ROS in both warm and cool temperature extremes and greatest mortality at temperatures 6-10 °C above ambient, interpreted as the outcome of thermal stress. Tracking of water masses within an oceanographic circulation model showed populations had distinct thermal histories, with EAC pico-eukaryotes experiencing higher average temperatures for at least 1 week prior to sampling. While acclimatization and community assembly could both influence biological responses, this study clearly demonstrates that phenotypic divergence occurs along planktonic drift trajectories.

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.

Rapid thermal adaptation in a marine diatom reveals constraints and trade-offs.

Rapid evolution in response to environmental change will likely be a driving force determining the distribution of species across the biosphere in coming decades. This is especially true of microorganisms, many of which may evolve in step with warming, including phytoplankton, the diverse photosynthetic microbes forming the foundation of most aquatic food webs. Here we tested the capacity of a globally important, model marine diatom Thalassiosira pseudonana, for rapid evolution in response to temperature. Selection at 16 and 31°C for 350 generations led to significant divergence in several temperature response traits, demonstrating local adaptation and the existence of trade-offs associated with adaptation to different temperatures. In contrast, competitive ability for nitrogen (commonly limiting in marine systems), measured after 450 generations of temperature selection, did not diverge in a systematic way between temperatures. This study shows how rapid thermal adaptation affects key temperature and nutrient traits and, thus, a population's long-term physiological, ecological, and biogeographic response to climate change.

Gradual plasticity alters population dynamics in variable environments: thermal acclimation in the green alga Chlamydomonas reinhartdii.

Environmental variability is ubiquitous, but its effects on populations are not fully understood or predictable. Recent attention has focused on how rapid evolution can impact ecological dynamics via adaptive trait change. However, the impact of trait change arising from plastic responses has received less attention, and is often assumed to optimize performance and unfold on a separate, faster timescale than ecological dynamics. Challenging these assumptions, we propose that gradual plasticity is important for ecological dynamics, and present a study of the plastic responses of the freshwater green algae Chlamydomonas reinhardtii as it acclimates to temperature changes. First, we show that C. reinhardtii's gradual acclimation responses can both enhance and suppress its performance after a perturbation, depending on its prior thermal history. Second, we demonstrate that where conventional approaches fail to predict the population dynamics of C. reinhardtii exposed to temperature fluctuations, a new model of gradual acclimation succeeds. Finally, using high-resolution data, we show that phytoplankton in lake ecosystems can experience thermal variation sufficient to make acclimation relevant. These results challenge prevailing assumptions about plasticity's interactions with ecological dynamics. Amidst the current emphasis on rapid evolution, it is critical that we also develop predictive methods accounting for plasticity.

Integrating community assembly and biodiversity to better understand ecosystem function: the Community Assembly and the Functioning of Ecosystems (CAFE) approach.

The research of a generation of ecologists was catalysed by the recognition that the number and identity of species in communities influences the functioning of ecosystems. The relationship between biodiversity and ecosystem functioning (BEF) is most often examined by controlling species richness and randomising community composition. In natural systems, biodiversity changes are often part of a bigger community assembly dynamic. Therefore, focusing on community assembly and the functioning of ecosystems (CAFE), by integrating both species richness and composition through species gains, losses and changes in abundance, will better reveal how community changes affect ecosystem function. We synthesise the BEF and CAFE perspectives using an ecological application of the Price equation, which partitions the contributions of richness and composition to function. Using empirical examples, we show how the CAFE approach reveals important contributions of composition to function. These examples show how changes in species richness and composition driven by environmental perturbations can work in concert or antagonistically to influence ecosystem function. Considering how communities change in an integrative fashion, rather than focusing on one axis of community structure at a time, will improve our ability to anticipate and predict changes in ecosystem function.

Species packing in eco-evolutionary models of seasonally fluctuating environments.

As ecology and evolution become ever more entwined, many areas of ecological theory are being re-examined. Eco-evolutionary analyses of classic coexistence mechanisms are yielding new insights into the structure and stability of communities. We examine fluctuation-dependent coexistence models, identifying communities that are both ecologically and evolutionarily stable. Members of these communities possess distinct environmental preferences, revealing widespread patterns of limiting similarity. This regularity leads to consistent changes in the structure of communities across fluctuation regimes. However, at high amplitudes, subtle differences in the form of fluctuations dramatically affect the collapse of communities. We also show that identical fluctuations can support multiple evolutionarily stable communities - a novel example of alternative stable states within eco-evolutionary systems. Consequently, the configuration of communities will depend on historical contingencies, including details of the adaptive process. Integrating evolution into the study of coexistence offers new insights, while enriching our understanding of ecology.

Isolation by distance and isolation by environment contribute to population differentiation in Protea repens (Proteaceae L.), a widespread South African species.

PREMISE OF THE STUDY: The Cape Floristic Region (CFR) of South Africa is renowned for its botanical diversity, but the evolutionary origins of this diversity remain controversial. Both neutral and adaptive processes have been implicated in driving diversification, but population-level studies of plants in the CFR are rare. Here, we investigate the limits to gene flow and potential environmental drivers of selection in Protea repens L. (Proteaceae L.), a widespread CFR species. METHODS: We sampled 19 populations across the range of P. repens and used genotyping by sequencing to identify 2066 polymorphic loci in 663 individuals. We used a Bayesian FST outlier analysis to identify single-nucleotide polymorphisms (SNPs) marking genomic regions that may be under selection; we used those SNPs to identify potential drivers of selection and excluded them from analyses of gene flow and genetic structure. RESULTS: A pattern of isolation by distance suggested limited gene flow between nearby populations. The populations of P. repens fell naturally into two or three groupings, which corresponded to an east-west split. Differences in rainfall seasonality contributed to diversification in highly divergent loci, as do barriers to gene flow that have been identified in other species. CONCLUSIONS: The strong pattern of isolation by distance is in contrast to the findings in the only other widespread species in the CFR that has been similarly studied, while the effects of rainfall seasonality are consistent with well-known patterns. Assessing the generality of these results will require investigations of other CFR species.

Temperature-nutrient interactions exacerbate sensitivity to warming in phytoplankton.

Temperature and nutrients are fundamental, highly nonlinear drivers of biological processes, but we know little about how they interact to influence growth. This has hampered attempts to model population growth and competition in dynamic environments, which is critical in forecasting species distributions, as well as the diversity and productivity of communities. To address this, we propose a model of population growth that includes a new formulation of the temperature-nutrient interaction and test a novel prediction: that a species' optimum temperature for growth, Topt , is a saturating function of nutrient concentration. We find strong support for this prediction in experiments with a marine diatom, Thalassiosira pseudonana: Topt decreases by 3-6 °C at low nitrogen and phosphorus concentrations. This interaction implies that species are more vulnerable to hot, low-nutrient conditions than previous models accounted for. Consequently the interaction dramatically alters species' range limits in the ocean, projected based on current temperature and nitrate levels as well as those forecast for the future. Ranges are smaller not only than projections based on the individual variables, but also than those using a simpler model of temperature-nutrient interactions. Nutrient deprivation is therefore likely to exacerbate environmental warming's effects on communities.

Coexistence in a variable environment: eco-evolutionary perspectives.

A central question in community ecology is the means by which species coexist. Models of coexistence often assume that species have fixed trait values and consider questions such as how tradeoffs and environmental variation influence coexistence and diversity. However, species traits can be dynamic, varying between populations and individuals and changing over time as species adapt and evolve, at rates that are relevant to ecological processes. Consequently, adding evolution to ecological coexistence models may modify their predictions and stability in complex or unexpected ways. We extend a well-studied coexistence mechanism depending on resource fluctuations by allowing evolution along a tradeoff between maximum growth rate and competitive ability. Interactions between favorable season length and the period of fluctuations constrain coexistence, with two species coexistence favored by intermediate season length and arising through evolutionary branching or non-local invasion. However, these results depend on the relative rates of ecological and evolutionary processes: rapid evolution leads to a complete breakdown of otherwise stable coexistence. Other coexistence mechanisms should be evaluated from an evolutionary perspective to examine how evolutionary forces may alter predicted ecological dynamics.

A global pattern of thermal adaptation in marine phytoplankton.

Rising ocean temperatures will alter the productivity and composition of marine phytoplankton communities, thereby affecting global biogeochemical cycles. Predicting the effects of future ocean warming on biogeochemical cycles depends critically on understanding how existing global temperature variation affects phytoplankton. Here we show that variation in phytoplankton temperature optima over 150 degrees of latitude is well explained by a gradient in mean ocean temperature. An eco-evolutionary model predicts a similar relationship, suggesting that this pattern is the result of evolutionary adaptation. Using mechanistic species distribution models, we find that rising temperatures this century will cause poleward shifts in species' thermal niches and a sharp decline in tropical phytoplankton diversity in the absence of an evolutionary response.