Conditional sanctioning in a legume-Rhizobium mutualism.

Legumes are high in protein and form a valuable part of human diets due to their interaction with symbiotic nitrogen-fixing bacteria known as rhizobia. Plants house rhizobia in specialized root nodules and provide the rhizobia with carbon in return for nitrogen. However, plants usually house multiple rhizobial strains that vary in their fixation ability, so the plant faces an investment dilemma. Plants are known to sanction strains that do not fix nitrogen, but nonfixers are rare in field settings, while intermediate fixers are common. Here, we modeled how plants should respond to an intermediate fixer that was otherwise isogenic and tested model predictions using pea plants. Intermediate fixers were only tolerated when a better strain was not available. In agreement with model predictions, nodules containing the intermediate-fixing strain were large and healthy when the only alternative was a nonfixer, but nodules of the intermediate-fixing strain were small and white when the plant was coinoculated with a more effective strain. The reduction in nodule size was preceded by a lower carbon supply to the nodule even before differences in nodule size could be observed. Sanctioned nodules had reduced rates of nitrogen fixation, and in later developmental stages, sanctioned nodules contained fewer viable bacteria than nonsanctioned nodules. This indicates that legumes can make conditional decisions, most likely by comparing a local nodule-dependent cue of nitrogen output with a global cue, giving them remarkable control over their symbiotic partners.

Marked differences in foraging area use and susceptibility to predation between two closely-related tropical seabirds.

Ecological theory predicts that closely-related species must occupy different niches to coexist. How marine top predators achieve this during breeding, when they often gather in large multi-species colonies and are constrained to central-place foraging, has been mostly studied in productive temperate and polar oceans with abundant resources, but less so in poorer, tropical waters. Here, we track the foraging movements of two closely-related sympatric seabirds-the white-tailed and red-tailed tropicbirds Phaethon lepturus and P. rubricauda-breeding on Aldabra Atoll, Seychelles, to investigate potential mechanisms of niche segregation and shed light on their contrasting population trends. Combining data from GPS, immersion, depth and accelerometry loggers, we show that the two species have similar behaviour at sea, but are completely segregated spatially, with red-tailed tropicbirds flying further to feed and using different feeding areas than white-tailed tropicbirds. Using nest-based camera traps, we show that low breeding success of both species-which likely drives observed population declines-is caused by high nest predation. However, the two species are targeted by different predators, with native avian predators mainly targeting red-tailed tropicbird nests, and invasive rats raiding white-tailed tropicbird nests when they leave their eggs unattended. Our findings provide new insight into the foraging ecology of tropicbirds and have important conservation implications. The extensive range and spatial segregation highlight the importance of considering large-scale protection of waters around tropical seabird colonies, while the high level of nest predation provides evidence in support of rat eradication and investigating potential nest protection from native avian predators.

Linking the influence and dependence of people on biodiversity across scales.

Biodiversity enhances many of nature's benefits to people, including the regulation of climate and the production of wood in forests, livestock forage in grasslands and fish in aquatic ecosystems. Yet people are now driving the sixth mass extinction event in Earth's history. Human dependence and influence on biodiversity have mainly been studied separately and at contrasting scales of space and time, but new multiscale knowledge is beginning to link these relationships. Biodiversity loss substantially diminishes several ecosystem services by altering ecosystem functioning and stability, especially at the large temporal and spatial scales that are most relevant for policy and conservation.

The function-dominance correlation drives the direction and strength of biodiversity-ecosystem functioning relationships.

Community composition is a primary determinant of how biodiversity change influences ecosystem functioning and, therefore, the relationship between biodiversity and ecosystem functioning (BEF). We examine the consequences of community composition across six structurally realistic plant community models. We find that a positive correlation between species' functioning in monoculture versus their dominance in mixture with regard to a specific function (the "function-dominance correlation") generates a positive relationship between realised diversity and ecosystem functioning across species richness treatments. However, because realised diversity declines when few species dominate, a positive function-dominance correlation generates a negative relationship between realised diversity and ecosystem functioning within species richness treatments. Removing seed inflow strengthens the link between the function-dominance correlation and BEF relationships across species richness treatments but weakens it within them. These results suggest that changes in species' identities in a local species pool may more strongly affect ecosystem functioning than changes in species richness.

Strong responses from weakly interacting species.

The impact of species loss from competitive communities partly depends on how populations of the surviving species respond. Predicting the response should be straightforward using models that describe population growth as a function of competitor densities; but these models require accurate estimates of interaction strengths. Here, we quantified how well we could predict responses to competitor removal in a community of annual plants, using a combination of observation and experiment. It was straightforward to fit models to multi-species communities, which passed standard diagnostic tests and provided apparently sensible estimates of interaction strengths. However, the models consistently underpredicted the response to competitor removal, by a factor of at least 50%. We argue that this poor predictive ability is likely to be general in plant communities due to 'the ghost of competition present' that confines species to parts of the environment in which they compete best.

Understanding the value of plant diversity for ecosystem functioning through niche theory.

Biodiversity experiments have generated robust empirical results supporting the hypothesis that ecosystems function better when they contain more species. Given that ecosystems provide services that are valued by humans, this inevitably suggests that the loss of species from natural ecosystems could diminish their value. This raises two important questions. First, will experimental results translate into the real world, where species are being lost at an alarming rate? And second, what are the benefits and pitfalls of such valuation exercises? We argue that the empirical results obtained in experiments are entirely consistent with well-established theories of species coexistence. We then examine the current body of work through the lens of niche theory and highlight where closer links with theory could open up opportunities for future research. We argue that niche theory predicts that diversity-functioning relationships are likely to be stronger (and require more species) in the field than in simplified experimental settings. However, we caution that while many of the biological processes that promote coexistence can also generate diversity-function relationships, there is no simple mapping between the two. This implies that valuation exercises need to proceed with care.

Hierarchical nuclear and cytoplasmic genetic architectures for plant growth and defense within Arabidopsis.

To understand how genetic architecture translates between phenotypic levels, we mapped the genetic architecture of growth and defense within the Arabidopsis thaliana Kas × Tsu recombinant inbred line population. We measured plant growth using traditional size measurements and size-corrected growth rates. This population contains genetic variation in both the nuclear and cytoplasmic genomes, allowing us to separate their contributions. The cytoplasmic genome regulated a significant variance in growth but not defense, which was due to cytonuclear epistasis. Furthermore, growth adhered to an infinitesimal model of genetic architecture, while defense metabolism was more of a moderate-effect model. We found a lack of concordance between quantitative trait loci (QTL) regulating defense and those regulating growth. Given the published evidence proving the link between glucosinolates and growth, this is likely a false negative result caused by the limited population size. This size limitation creates an inability to test the entire potential genetic landscape possible between these two parents. We uncovered a significant effect of glucosinolates on growth once we accounted for allelic differences in growth QTLs. Therefore, other growth QTLs can mask the effects of defense upon growth. Investigating direct links across phenotypic hierarchies is fraught with difficulty; we identify issues complicating this analysis.

Is 'peak N' key to understanding the timing of flowering in annual plants?

Flowering time in annual plants has large fitness consequences and has been the focus of theoretical and empirical study. Previous theory has concluded that flowering time has evolved over evolutionary time to maximize fitness over a particular season length. We introduce a new model where flowering is cued by a growth-rate rule (peak nitrogen (N)). Flowering is therefore sensitive to physiological parameters and to current environmental conditions, including N availability and the presence of competitors. The model predicts that, when overall conditions are suitable for flowering, plants should never flower after 'peak N', the point during development when the whole-plant N uptake rate reaches its maximum. Our model further predicts correlations between flowering time and vegetative growth rates, and that the response to increased N depends heavily on how this extra N is made available. We compare our predictions to observations in the literature. We suggest that annual plants may have evolved to use growth-rate rules as part of the cue for flowering, allowing them to smoothly and optimally adjust their flowering time to a wide range of local conditions. If so, there are widespread implications for the study of the molecular biology behind flowering pathways.

Integration of population genetics with oceanographic models reveals strong connectivity among coral reefs across Seychelles.

Many countries with tropical reef systems face hard choices preserving coral reefs in the face of climate change on limited budgets. One approach to maximising regional reef resilience is targeting management efforts and resources at reefs that export large numbers of larvae to other reefs. However, this requires reef connectivity to be quantified. To map coral connectivity in the Seychelles reef system we carried out a population genomic study of the Porites lutea species complex using 241 sequenced colonies from multiple islands. To identify oceanographic drivers of this connectivity and quantify variability, we further used a 2 km resolution regional ocean simulation coupled with a larval dispersal model to predict the flow of coral larvae between reef sites. Patterns of admixture and gene flow are broadly supported by model predictions, but the realised connectivity is greater than that predicted from model simulations. Both methods detected a biogeographic dispersal barrier between the Inner and Outer Islands of Seychelles. However, this barrier is permeable and substantial larval transport is possible across Seychelles, particularly for one of two putative species found in our genomic study. The broad agreement between predicted connectivity and observed genetic patterns supports the use of such larval dispersal simulations in reef system management in Seychelles and the wider region.

Adaptation and extinction in experimentally fragmented landscapes.

Competition and disturbance are potent ecological forces that shape evolutionary trajectories. These forces typically work in opposition: when disturbance is infrequent, densities are high and competition is intense. In contrast, frequent disturbance creates a low-density environment in which competition is weak and good dispersal essential. We exploited recent advances in genomic research to quantify the response to selection by these powerful ecological forces at the phenotypic and molecular genetic level in experimental landscapes. We grew the annual plant Arabidopsis thaliana in discrete patches embedded in a hostile matrix and varied the number and size of patches and the intensity of disturbance, by creating both static and dynamic landscapes. In static landscapes all patches were undisturbed, whereas in dynamic landscapes all patches were destroyed in each generation, forcing seeds to disperse to new locations. We measured the resulting changes in phenotypic, genetic, and genotypic diversity after five generations of selection. Simulations revealed that the observed loss of genetic diversity dwarfed that expected under drift, with dramatic diversity loss, particularly from dynamic landscapes. In line with ecological theory, static landscapes favored good competitors; however, competitive ability was linked to growth rate and not, as expected, to seed mass. In dynamic landscapes, there was strong selection for increased dispersal ability in the form of increased inflorescence height and reduced seed mass. The most competitive genotypes were almost eliminated from highly disturbed landscapes, raising concern over the impact of increased levels of human-induced disturbance in natural landscapes.

Sources of marine debris for Seychelles and other remote islands in the western Indian Ocean.

Vast quantities of debris are beaching at remote islands in the western Indian Ocean. We carry out marine dispersal simulations incorporating currents, waves, winds, beaching, and sinking, for both terrestrial and marine sources of debris, to predict where this debris comes from. Our results show that most terrestrial debris beaching at these remote western Indian Ocean islands drifts from Indonesia, India, and Sri Lanka. Debris associated with fisheries and shipping also poses a major risk. Debris accumulation at Seychelles is likely seasonal, peaking during February-April. This pattern is driven by monsoonal winds and may be amplified during positive Indian Ocean Dipole and El-Niño events. Our results underline the vulnerability of small island states to marine plastic pollution, and are a crucial step towards improved management of the issue. The trajectories used in this study are available for download, and our analyses can be rerun under different parameter choices.

Fear of the dark or dinner by moonlight? Reduced temporal partitioning among Africa's large carnivores.

Africa is home to the last intact guild of large carnivores and thus provides the only opportunity to investigate mechanisms of coexistence among large predator species. Strong asymmetric dominance hierarchies typically characterize guilds of large carnivores; but despite this asymmetry, subdominant species may persist alongside their stronger counterparts through temporal partitioning of habitat and resources. In the African guild, the subdominant African wild dogs and cheetahs are routinely described as diurnal and crepuscular. These activity patterns have been interpreted to result from the need to avoid encounters with the stronger, nocturnal spotted hyenas and lions. However, the idea that diel activity patterns of carnivore species are strongly shaped by competition and predation has recently been challenged by new observations. In a three-year study in the Okavango Delta, we investigated daily activity patterns and temporal partitioning for wild dogs, cheetahs, spotted hyenas and lions by fitting radio collars that continuously recorded activity bursts, to a total of 25 individuals. Analysis of activity patterns throughout the 24-h cycle revealed an unexpectedly high degree of temporal overlap among the four species. This was mainly due to the extensive and previously undescribed nocturnal activity of wild dogs and cheetahs. Their nocturnal activity fluctuated with the lunar cycle, represented up to 40% of the diel activity budget and was primarily constrained by moonlight availability. In contrast, the nocturnal activity patterns of lions and hyenas were unaffected by moonlight and remained constant over the lunar cycle. Our results suggest that other ecological factors such as optimal hunting conditions have shaped the diel activity patterns of subdominant, large predators. We suggest that they are "starvation driven" and must exploit every opportunity to obtain a meal. The benefits of activity on moonlit nights therefore offset the risks of encountering night-active predators and competitors.

Plant growth rates and seed size: a re-evaluation.

Small-seeded plant species are often reported to have high relative growth rate or RGR. However, because RGR declines as plants grow larger, small-seeded species could achieve higher RGR simply by virtue of their small size. In contrast, size-standardized growth rate or SGR factors out these size effects. Differences in SGR can thus only be due to differences in morphology, allocation, or physiology. We used nonlinear regression to calculate SGR for comparison with RGR for 10 groups of species spanning a wide range of life forms. We found that RGR was negatively correlated with seed mass in nearly all groups, but the relationship between SGR and seed mass was highly variable. We conclude that small-seeded species only sometimes possess additional adaptations for rapid growth over and above their general size advantage.

Limited domestic introgression in a final refuge of the wild pigeon.

Domesticated animals have been culturally and economically important throughout history. Many of their ancestral lineages are extinct or genetically endangered following hybridization with domesticated relatives. Consequently, they have been understudied compared to the ancestral lineages of domestic plants. The domestic pigeon Columba livia, which was pivotal in Darwin's studies, has maintained outsized cultural significance. Its role as a model organism spans the fields of behavior, genetics, and evolution. Domestic pigeons have hybridized with their progenitor, the Rock Dove, rendering the latter of dubious genetic status. Here, we use genomic and morphological data from the putative Rock Doves of the British Isles to identify relictual undomesticated populations. We reveal that Outer Hebridean Rock Doves have experienced minimal levels of introgression. Our results outline the contemporary status of these wild pigeons, highlighting the role of hybridization in the homogenization of genetic lineages.

Using knockout mutants to reveal the growth costs of defensive traits.

We used a selection of Arabidopsis thaliana mutants with knockouts in defence genes to demonstrate growth costs of trichome development and glucosinolate production. Four of the seven defence mutants had significantly higher size-standardized growth rates (SGRs) than the wild-type in early life, although this benefit declined as plants grew larger. SGR is known to be a good predictor of success under high-density conditions, and we confirmed that mutants with higher growth rates had a large advantage when grown in competition. Despite the lack of differences in flowering-time genes, the mutants differed in flowering time, a trait that strongly correlated with early growth rate. Aphid herbivory decreased plant growth rate and increased flowering time, and aphid population growth rate was closely coupled to the growth rate of the host plant. Small differences in early SGR thus had cascading effects on both flowering time and herbivore populations.

Partitioning the components of relative growth rate: how important is plant size variation?

Plant growth plays a key role in the functioning of the terrestrial biosphere, and there have been substantial efforts to understand why growth varies among species. To this end, a large number of experimental analyses have been undertaken; however, the emergent patterns between growth rate and its components are often contradictory. We believe that these conflicting results are a consequence of the way growth is measured. Growth is typically characterized by relative growth rate (RGR); however, RGR often declines as organisms get larger, making it difficult to compare species of different sizes. To overcome this problem, we advocate using nonlinear mixed-effects models so that RGR can be calculated at a standard size, and we present easily implemented methods for doing this. We then present new methods for analyzing the traditional components of RGR that explicitly allow for the fact that (log)(RGR) is the sum of its components. These methods provide an exact decomposition of the variance in (log)(RGR). Finally, we use simple analytical and simulation approaches to explore the effect of size variation on growth and its components and show that the relative importance of the components of RGR is influenced by the extent to which analyses standardize for plant size.

A new method for measuring relative growth rate can uncover the costs of defensive compounds in Arabidopsis thaliana.

*Most plants suffer some degree of herbivore attack and many actively defend themselves against such an event. However, while such defence is generally assumed to be costly, it has sometimes proved difficult to demonstrate the costs of defensive compounds. *Here, we present a method for analysing growth rates which allows the effects of variation in initial plant size to be properly accounted for and apply it to 30 lines from a recombinant inbred population of Arabidopsis thaliana. We then relate different measures of relative growth rate (RGR) to damage caused by a specialist lepidopteran insect and to levels of putative defensive compounds measured on the same lines. *We show that seed size variation within the recombinant inbred population is large enough to generate differences in RGR, even when no other physiological differences exist. However, once size-standardized, RGR was positively correlated with herbivore damage (fast-growing lines suffered more damage) and was negatively correlated with the concentration of several glucosinolate compounds. *We conclude that defensive compounds do have a growth cost and that the production of such compounds results in reduced herbivore damage. However, size standardization of RGR was essential to uncovering the growth costs of defensive compounds.

Biology, chance, or history? The predictable reassembly of temperate grassland communities.

Many studies have examined invasion resistance in plant communities, but few have explored the mechanisms of invasion and how subsequent community reassembly affects community functioning. Using natural dispersal and deliberate seed addition into grassland communities with different compositional and richness histories, we show that invaders establish in a nonrandom manner due to negative effects of resident functional groups on invading species from the same functional group. Invaders hence complement communities with originally low richness levels. Consequently, communities converge toward similar levels of species richness, high functional richness, and evenness, but not always maximum productivity. Invasion processes are faster but qualitatively similar when the effect of chance, in the form of dispersal stochasticity, is reduced by seed addition. Thus, dispersal limitation may influence community assembly, but it does not override functionally predictable assembly mechanisms. Some of the most productive communities prior to invasion are unstable in the face of invasion, leading to decreased productivity following invasion. We suggest that invasion into such communities occurs possibly because a pathogen-free niche is available rather than a resource niche. Thus, pathogens in addition to resource niches may be important biological drivers of community assembly.

Different but equal: the implausible assumption at the heart of neutral theory.

1. The core assumption of neutral theory is that all individuals in a community have equal fitness regardless of species, and regardless of the species composition of the community. But, real communities consist of species exhibiting large trait differences; hence these differences must be subject to perfect fitness-equalizing trade-offs for neutrality to hold. 2. Here we explain that perfect equalizing trade-offs are extremely unlikely to occur in reality, because equality of fitness among species is destroyed by: (i) any deviation in the functional form of the trade-off away from the one special form that gives equal fitness; (ii) spatial or temporal variation in performance; (iii) random species differences in performance. 3. In the absence of the density-dependent processes stressed by traditional niche-based community ecology, communities featuring small amounts of (i) or (ii) rapidly lose trait variation, becoming dominated by species with similar traits, and exhibit substantially lower species richness compared to the neutral case. Communities featuring random interspecific variation in traits (iii) lose all but a few fortuitous species. 4. Thus neutrality should be viewed, a priori, as a highly improbable explanation for the long-term co-occurrence of measurably different species within ecological communities. In contrast, coexistence via niche structure and density dependence, is robust to species differences in baseline fitness, and so remains plausible. 5. We conclude that: (i) co-occurring species will typically exhibit substantial differences in baseline fitness even when (imperfect) equalizing trade-offs have been taken into account; (ii) therefore, communities must be strongly niche structured, otherwise they would lose both trait variation and species richness; (iii) nonetheless, even in strongly niche-structured communities, it is possible that the abundance of species with similar traits are at least partially free to drift.