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.

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.

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.

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.

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.

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.

Fast and furious: Early differences in growth rate drive short-term plant dominance and exclusion under eutrophication.

The reduction of plant diversity following eutrophication threatens many ecosystems worldwide. Yet, the mechanisms by which species are lost following nutrient enrichment are still not completely understood, nor are the details of when such mechanisms act during the growing season, which hampers understanding and the development of mitigation strategies.Using a common garden competition experiment, we found that early-season differences in growth rates among five perennial grass species measured in monoculture predicted short-term competitive dominance in pairwise combinations and that the proportion of variance explained was particularly greater under a fertilization treatment.We also examined the role of early-season growth rate in determining the outcome of competition along an experimental nutrient gradient in an alpine meadow. Early differences in growth rate between species predicted short-term competitive dominance under both ambient and fertilized conditions and competitive exclusion under fertilized conditions.The results of these two studies suggest that plant species growing faster during the early stage of the growing season gain a competitive advantage over species that initially grow more slowly, and that this advantage is magnified under fertilization. This finding is consistent with the theory of asymmetric competition for light in which fast-growing species can intercept incident light and hence outcompete and exclude slower-growing (and hence shorter) species. We predict that the current chronic nutrient inputs into many terrestrial ecosystems worldwide will reduce plant diversity and maintain a low biodiversity state by continuously favoring fast-growing species. Biodiversity management strategies should focus on controlling nutrient inputs and reducing the growth of fast-growing species early in the season.

The costs of removing the unsanctioned import of marine plastic litter to small island states.

Small island states receive unprecedented amounts of the world's plastic waste. In March 2019, we removed as much plastic litter as possible from Aldabra Atoll, a remote UNESCO World Heritage Site, and estimated the money and effort required to remove the remaining debris. We removed 25 tonnes at a cost of $224,537, which equates to around $10,000 per day of clean-up operations or $8,900 per tonne of litter. We estimate that 513 tonnes (95% CI 212-814) remains on Aldabra, the largest accumulation reported for any single island. We calculate that removing it will cost approximately $4.68 million and require 18,000 person-hours of labour. By weight, the composition is dominated by litter from the regional fishing industry (83%) and flip-flops from further afield (7%). Given the serious detrimental effects of plastic litter on marine ecosystems, we conclude that clean-up efforts are a vital management action for islands like Aldabra, despite the high financial cost and should be integrated alongside policies directed at 'turning off the tap'. We recommend that international funding be made available for such efforts, especially considering the transboundary nature of both the marine plastic litter problem and the ecosystem services provided by biodiversity-rich islands.

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.

Contribution of epigenetic variation to adaptation in Arabidopsis.

In plants, transgenerational inheritance of some epialleles has been demonstrated but it remains controversial whether epigenetic variation is subject to selection and contributes to adaptation. Simulating selection in a rapidly changing environment, we compare phenotypic traits and epigenetic variation between Arabidopsis thaliana populations grown for five generations under selection and their genetically nearly identical ancestors. Selected populations of two distinct genotypes show significant differences in flowering time and plant architecture, which are maintained for at least 2-3 generations in the absence of selection. While we cannot detect consistent genetic changes, we observe a reduction of epigenetic diversity and changes in the methylation state of about 50,000 cytosines, some of which are associated with phenotypic changes. Thus, we propose that epigenetic variation is subject to selection and can contribute to rapid adaptive responses, although the extent to which epigenetics plays a role in adaptation is still unclear.

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.

Policing the legume-Rhizobium symbiosis: a critical test of partner choice.

In legume-Rhizobium symbioses, specialised soil bacteria fix atmospheric nitrogen in return for carbon. However, ineffective strains can arise, making discrimination essential. Discrimination can occur via partner choice, where legumes prevent ineffective strains from entering, or via sanctioning, where plants provide fewer resources. Several studies have inferred that legumes exercise partner choice, but the rhizobia compared were not otherwise isogenic. To test when and how plants discriminate ineffective strains we developed sets of fixing and non-fixing strains that differed only in the expression of nifH - essential for nitrogen fixation - and could be visualised using marker genes. We show that the plant is unable to select against the non-fixing strain at the point of entry, but that non-fixing nodules are sanctioned. We also used the technique to characterise mixed nodules (containing both a fixing and a non-fixing strain), whose frequency could be predicted using a simple diffusion model. We discuss that sanctioning is likely to evolve in preference to partner choice in any symbiosis where partner quality cannot be adequately assessed until goods or services are actively exchanged.

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.

Persistence of distinctive morphotypes in the native range of the CITES-listed Aldabra giant tortoise.

Understanding the extent of morphological variation in the wild population of Aldabra giant tortoises is important for conservation, as morphological variation in captive populations has been interpreted as evidence for lingering genes from extinct tortoise lineages. If true, this could impact reintroduction programmes in the region. The population of giant tortoises on Aldabra Atoll is subdivided and distributed around several islands. Although pronounced morphological variation was recorded in the late 1960s, it was thought to be a temporary phenomenon. Early researchers also raised concerns over the future of the population, which was perceived to have exceeded its carrying capacity. We analyzed monthly monitoring data from 12 transects spanning a recent 15-year period (1998-2012) during which animals from four subpopulations were counted, measured, and sexed. In addition, we analyzed survival data from individuals first tagged during the early 1970s. The population is stable with no sign of significant decline. Subpopulations differ in density, but these differences are mostly due to differences in the prevailing vegetation type. However, subpopulations differ greatly in both the size of animals and the degree of sexual dimorphism. Comparisons with historical data reveal that phenotypic differences among the subpopulations of tortoises on Aldabra have been apparent for the last 50 years with no sign of diminishing. We conclude that the giant tortoise population on Aldabra is subject to varying ecological selection pressures, giving rise to stable morphotypes in discrete subpopulations. We suggest therefore that (1) the presence of morphological differences among captive Aldabra tortoises does not alone provide convincing evidence of genes from other extinct species; and (2) Aldabra serves as an important example of how conservation and management in situ can add to the scientific value of populations and perhaps enable them to better adapt to future ecological pressures.

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.

Gains to species diversity in organically farmed fields are not propagated at the farm level.

Organic farming is promoted to reduce environmental impacts of agriculture, but surprisingly little is known about its effects at the farm level, the primary unit of decision making. Here we report the effects of organic farming on species diversity at the field, farm and regional levels by sampling plants, earthworms, spiders and bees in 1470 fields of 205 randomly selected organic and nonorganic farms in twelve European and African regions. Species richness is, on average, 10.5% higher in organic than nonorganic production fields, with highest gains in intensive arable fields (around +45%). Gains to species richness are partly caused by higher organism abundance and are common in plants and bees but intermittent in earthworms and spiders. Average gains are marginal +4.6% at the farm and +3.1% at the regional level, even in intensive arable regions. Additional, targeted measures are therefore needed to fulfil the commitment of organic farming to benefit farmland biodiversity.

Land-use intensity and the effects of organic farming on biodiversity: a hierarchical meta-analysis.

The benefits of organic farming to biodiversity in agricultural landscapes continue to be hotly debated, emphasizing the importance of precisely quantifying the effect of organic vs. conventional farming. We conducted an updated hierarchical meta-analysis of studies that compared biodiversity under organic and conventional farming methods, measured as species richness. We calculated effect sizes for 184 observations garnered from 94 studies, and for each study, we obtained three standardized measures reflecting land-use intensity. We investigated the stability of effect sizes through time, publication bias due to the 'file drawer' problem, and consider whether the current literature is representative of global organic farming patterns. On average, organic farming increased species richness by about 30%. This result has been robust over the last 30 years of published studies and shows no sign of diminishing. Organic farming had a greater effect on biodiversity as the percentage of the landscape consisting of arable fields increased, that is, it is higher in intensively farmed regions. The average effect size and the response to agricultural intensification depend on taxonomic group, functional group and crop type. There is some evidence for publication bias in the literature; however, our results are robust to its impact. Current studies are heavily biased towards northern and western Europe and North America, while other regions with large areas of organic farming remain poorly investigated. Synthesis and applications. Our analysis affirms that organic farming has large positive effects on biodiversity compared with conventional farming, but that the effect size varies with the organism group and crop studied, and is greater in landscapes with higher land-use intensity. Decisions about where to site organic farms to maximize biodiversity will, however, depend on the costs as well as the potential benefits. Current studies have been heavily biased towards agricultural systems in the developed world. We recommend that future studies pay greater attention to other regions, in particular, areas with tropical, subtropical and Mediterranean climates, in which very few studies have been conducted.

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.

Natural enemies drive geographic variation in plant defenses.

Plants defend themselves against attack by natural enemies, and these defenses vary widely across populations. However, whether communities of natural enemies are a sufficiently potent force to maintain polymorphisms in defensive traits is largely unknown. Here, we exploit the genetic resources of Arabidopsis thaliana, coupled with 39 years of field data on aphid abundance, to (i) demonstrate that geographic patterns in a polymorphic defense locus (GS-ELONG) are strongly correlated with changes in the relative abundance of two specialist aphids; and (ii) demonstrate differential selection by the two aphids on GS-ELONG, using a multigeneration selection experiment. We thereby show a causal link between variation in abundance of the two specialist aphids and the geographic pattern at GS-ELONG, which highlights the potency of natural enemies as selective forces.

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.