slimr: An R package for tailor-made integrations of data in population genomic simulations over space and time.

Software for realistically simulating complex population genomic processes is revolutionizing our understanding of evolutionary processes, and providing novel opportunities for integrating empirical data with simulations. However, the integration between standalone simulation software and R is currently not well developed. Here, we present slimr, an R package designed to create a seamless link between standalone software SLiM >3.0, one of the most powerful population genomic simulation frameworks, and the R development environment, with its powerful data manipulation and analysis tools. We show how slimr facilitates smooth integration between genetic data, ecological data and simulation in a single environment. The package enables pipelines that begin with data reading, cleaning and manipulation, proceed to constructing empirically based parameters and initial conditions for simulations, then to running numerical simulations and finally to retrieving simulation results in a format suitable for comparisons with empirical data - aided by advanced analysis and visualization tools provided by R. We demonstrate the use of slimr with an example from our own work on the landscape population genomics of desert mammals, highlighting the advantage of having a single integrated tool for both data analysis and simulation. slimr makes the powerful simulation ability of SLiM directly accessible to R users, allowing integrated simulation projects that incorporate empirical data without the need to switch between software environments. This should provide more opportunities for evolutionary biologists and ecologists to use realistic simulations to better understand the interplay between ecological and evolutionary processes.

Episodic population fragmentation and gene flow reveal a trade-off between heterozygosity and allelic richness.

In episodic environments like deserts, populations of some animal species exhibit irregular fluctuations such that populations are alternately large and connected or small and isolated. Such dynamics are typically driven by periodic resource pulses due, for example, to large but infrequent rainfall events. The repeated population bottlenecks resulting from fragmentation should lower genetic diversity over time, yet species undergoing these fluctuations appear to maintain high levels of genetic diversity. To resolve this apparent paradox, we simulated a metapopulation of constant size undergoing repeat episodes of fragmentation and change in gene flow to mimic outcomes experienced by mammals in an Australian desert. We show that episodic fragmentation and gene flow have contrasting effects on two measures of genetic diversity: heterozygosity and allelic richness. Specifically, fragmentation into many, small subpopulations, coupled with periods of infrequent gene flow, preserves allelic richness at the expense of heterozygosity. In contrast, fragmentation into a few, large subpopulations maintains heterozygosity at the expense of allelic richness. The strength of the trade-off between heterozygosity and allelic richness depends on the amount of gene flow and the frequency of gene flow events. Our results imply that the type of genetic diversity maintained among species living in strongly fluctuating environments will depend on the way populations fragment, with our results highlighting different mechanisms for maintaining allelic richness and heterozygosity in small, fragmented populations.

Priorities for conserving the world's terrestrial mammals based on over-the-horizon extinction risk.

Three major axes of global change put the world's mammal biodiversity at risk: climate change, human population growth, and land-use change.1,2,3,4,5,6,7,8,9,10,11,12 In some parts of the world the full effects of these threats on species will only be felt in decades to come, yet conservation emphasizes species currently threatened with extinction, by threats that have already occurred. There have been calls for conservation to become more proactive by anticipating and protecting species that may not yet be threatened, but have a high chance of becoming threatened in the future.3,6,8,10,12,13,14 We refer to this as "over-the-horizon" extinction risk, and we identify such species among the world's nonmarine mammals by considering not only the severity of increase in threats faced by each species, but also the way each species' biology confers sensitivity or robustness to threats. We define four future risk factors based on species' biology and projected exposure to severe change in climate, human population, and land use. We regard species with two or more of these risk factors as especially vulnerable to future extinction risk.10,15,16,17,18,19 Our models predict that by 2100 up to 1,057 (20%) of nonmarine mammal species will have combinations of two or more future risk factors. These species will be particularly concentrated in two future risk hotspots in sub-Saharan Africa and southern/eastern Australia. Proactively targeting species with over-the-horizon extinction risk could help to future-proof global conservation planning and prevent a new wave of mammal species from becoming threatened with extinction by the end of this century.

Grambank reveals the importance of genealogical constraints on linguistic diversity and highlights the impact of language loss.

While global patterns of human genetic diversity are increasingly well characterized, the diversity of human languages remains less systematically described. Here, we outline the Grambank database. With over 400,000 data points and 2400 languages, Grambank is the largest comparative grammatical database available. The comprehensiveness of Grambank allows us to quantify the relative effects of genealogical inheritance and geographic proximity on the structural diversity of the world's languages, evaluate constraints on linguistic diversity, and identify the world's most unusual languages. An analysis of the consequences of language loss reveals that the reduction in diversity will be strikingly uneven across the major linguistic regions of the world. Without sustained efforts to document and revitalize endangered languages, our linguistic window into human history, cognition, and culture will be seriously fragmented.

Diverse mangroves deviate from other angiosperms in their genome size, leaf cell size and cell packing density relationships.

BACKGROUND AND AIMS: While genome size limits the minimum sizes and maximum numbers of cells that can be packed into a given leaf volume, mature cell sizes can be substantially larger than their meristematic precursors and vary in response to abiotic conditions. Mangroves are iconic examples of how abiotic conditions can influence the evolution of plant phenotypes. METHODS: Here, we examined the coordination between genome size, leaf cell sizes, cell packing densities and leaf size in 13 mangrove species across four sites in China. Four of these species occurred at more than one site, allowing us to test the effect of climate on leaf anatomy. RESULTS: We found that genome sizes of mangroves were very small compared to other angiosperms, but, like other angiosperms, mangrove cells were always larger than the minimum size defined by genome size. Increasing mean annual temperature of a growth site led to higher packing densities of veins (Dv) and stomata (Ds) and smaller epidermal cells but had no effect on stomatal size. In contrast to other angiosperms, mangroves exhibited (1) a negative relationship between guard cell size and genome size; (2) epidermal cells that were smaller than stomata; and (3) coordination between Dv and Ds that was not mediated by epidermal cell size. Furthermore, mangrove epidermal cell sizes and packing densities covaried with leaf size. CONCLUSIONS: While mangroves exhibited coordination between veins and stomata and attained a maximum theoretical stomatal conductance similar to that of other angiosperms, the tissue-level tradeoffs underlying these similar relationships across species and environments were markedly different, perhaps indicative of the unique structural and physiological adaptations of mangroves to their stressful environments.

Global predictors of language endangerment and the future of linguistic diversity.

Language diversity is under threat. While each language is subject to specific social, demographic and political pressures, there may also be common threatening processes. We use an analysis of 6,511 spoken languages with 51 predictor variables spanning aspects of population, documentation, legal recognition, education policy, socioeconomic indicators and environmental features to show that, counter to common perception, contact with other languages per se is not a driver of language loss. However, greater road density, which may encourage population movement, is associated with increased endangerment. Higher average years of schooling is also associated with greater endangerment, evidence that formal education can contribute to loss of language diversity. Without intervention, language loss could triple within 40 years, with at least one language lost per month. To avoid the loss of over 1,500 languages by the end of the century, urgent investment is needed in language documentation, bilingual education programmes and other community-based programmes.

Ecological interactions shape the evolution of flower color in communities across a temperate biodiversity hotspot.

Processes driving the divergence of floral traits may be integral to the extraordinary richness of flowering plants and the assembly of diverse plant communities. Several models of pollinator-mediated floral evolution have been proposed; floral divergence may (i) be directly involved in driving speciation or may occur after speciation driven by (ii) drift or local adaptation in allopatry or (iii) negative interactions between species in sympatry. Here, we generate predictions for patterns of trait divergence and community assembly expected under these three models, and test these predictions in Hakea (Proteaceae), a diverse genus in the Southwest Australian biodiversity hotspot. We quantified functional richness for two key floral traits (pistil length and flower color), as well as phylogenetic distances between species, across ecological communities, and compared these to patterns generated from null models of community assembly. We also estimated the statistical relationship between rates of trait evolution and lineage diversification across the phylogeny. Patterns of community assembly suggest that flower color, but not floral phenology or morphology, or phylogenetic relatedness, is more divergent in communities than expected. Rates of lineage diversification and flower color evolution were negatively correlated across the phylogeny and rates of flower colour evolution were positively related to branching times. These results support a role for diversity-dependent species interactions driving floral divergence during the Hakea radiation, contributing to the development of the extraordinary species richness of southwest Australia.

There is little evidence that spicy food in hot countries is an adaptation to reducing infection risk.

Spicier food in hot countries has been explained in terms of natural selection on human cultures, with spices with antimicrobial effects considered to be an adaptation to increased risk of foodborne infection. However, correlations between culture and environment are difficult to interpret, because many cultural traits are inherited together from shared ancestors, neighbouring cultures are exposed to similar conditions, and many cultural and environmental variables show strong covariation. Here, using a global dataset of 33,750 recipes from 70 cuisines containing 93 different spices, we demonstrate that variation in spice use is not explained by temperature and that spice use cannot be accounted for by diversity of cultures, plants, crops or naturally occurring spices. Patterns of spice use are not consistent with an infection-mitigation mechanism, but are part of a broader association between spice, health, and poverty. This study highlights the challenges inherent in interpreting patterns of human cultural variation in terms of evolutionary pressures.

Spatiophylogenetic modelling of extinction risk reveals evolutionary distinctiveness and brief flowering period as threats in a hotspot plant genus.

Comparative models used to predict species threat status can help identify the diagnostic features of species at risk. Such models often combine variables measured at the species level with spatial variables, causing multiple statistical challenges, including phylogenetic and spatial non-independence. We present a novel Bayesian approach for modelling threat status that simultaneously deals with both forms of non-independence and estimates their relative contribution, and we apply the approach to modelling threat status in the Australian plant genus Hakea. We find that after phylogenetic and spatial effects are accounted for, species with greater evolutionary distinctiveness and a shorter annual flowering period are more likely to be threatened. The model allows us to combine information on evolutionary history, species biology and spatial data, calculate latent extinction risk (potential for non-threatened species to become threatened), estimate the most important drivers of risk for individual species and map spatial patterns in the effects of different predictors on extinction risk. This could be of value for proactive conservation decision-making based on the early identification of species and regions of potential conservation concern.

Explaining ecosystem multifunction with evolutionary models.

Ecosystem function is the outcome of species interactions, traits, and niche overlap - all of which are influenced by evolution. However, it is not well understood how the tempo and mode of niche evolution can influence ecosystem function. In evolutionary models where either species differences accumulate through random drift in a single trait or species differences accumulate through divergent selection among close relatives, we should expect that ecosystem function is strongly related to diversity. However, when strong selection causes species to converge on specific niches or when novel traits that directly affect function evolve in some clades but not others, the relationship between diversity and ecosystem function might not be very strong. We test these ideas using a field experiment that established plant mixtures with differing phylogenetic diversities and we measured ten different community functions. We show that some functions were strongly predicted by species richness and mean pairwise phylogenetic distance (MPD, a measure of phylogenetic diversity), including biomass production and the reduction of herbivore and pathogen damage in polyculture, while other functions had weaker (litter production and structural complexity) or nonsignificant relationships (e.g., flower production and arthropod abundance) with MPD and richness. However, these divergent results can be explained by different models of niche evolution. These results show that diversity-ecosystem function relationships are the product of evolution, but that the nature of how evolution influences ecosystem function is complex.

Symbiosis limits establishment of legumes outside their native range at a global scale.

Microbial symbiosis is integral to plant growth and reproduction, but its contribution to global patterns of plant distribution is unknown. Legumes (Fabaceae) are a diverse and widely distributed plant family largely dependent on symbiosis with nitrogen-fixing rhizobia, which are acquired from soil after germination. This dependency is predicted to limit establishment in new geographic areas, owing to a disruption of compatible host-symbiont associations. Here we compare non-native establishment patterns of symbiotic and non-symbiotic legumes across over 3,500 species, covering multiple independent gains and losses of rhizobial symbiosis. We find that symbiotic legume species have spread to fewer non-native regions compared to non-symbiotic legumes, providing strong support for the hypothesis that lack of suitable symbionts or environmental conditions required for effective nitrogen-fixation are driving these global introduction patterns. These results highlight the importance of mutualisms in predicting non-native species establishment and the potential impacts of microbial biogeography on global plant distributions.

Interdisciplinary research has consistently lower funding success.

Interdisciplinary research is widely considered a hothouse for innovation, and the only plausible approach to complex problems such as climate change. One barrier to interdisciplinary research is the widespread perception that interdisciplinary projects are less likely to be funded than those with a narrower focus. However, this commonly held belief has been difficult to evaluate objectively, partly because of lack of a comparable, quantitative measure of degree of interdisciplinarity that can be applied to funding application data. Here we compare the degree to which research proposals span disparate fields by using a biodiversity metric that captures the relative representation of different fields (balance) and their degree of difference (disparity). The Australian Research Council's Discovery Programme provides an ideal test case, because a single annual nationwide competitive grants scheme covers fundamental research in all disciplines, including arts, humanities and sciences. Using data on all 18,476 proposals submitted to the scheme over 5 consecutive years, including successful and unsuccessful applications, we show that the greater the degree of interdisciplinarity, the lower the probability of being funded. The negative impact of interdisciplinarity is significant even when number of collaborators, primary research field and type of institution are taken into account. This is the first broad-scale quantitative assessment of success rates of interdisciplinary research proposals. The interdisciplinary distance metric allows efficient evaluation of trends in research funding, and could be used to identify proposals that require assessment strategies appropriate to interdisciplinary research.

Phylogenetic diversity of plants alters the effect of species richness on invertebrate herbivory.

Long-standing ecological theory proposes that diverse communities of plants should experience a decrease in herbivory. Yet previous empirical examinations of this hypothesis have revealed that plant species richness increases herbivory in just as many systems as it decreases it. In this study, I ask whether more insight into the role of plant diversity in promoting or suppressing herbivory can be gained by incorporating information about the evolutionary history of species in a community. In an old field system in southern Ontario, I surveyed communities of plants and measured levels of leaf damage on 27 species in 38 plots. I calculated a measure of phylogenetic diversity (PSE) that encapsulates information about the amount of evolutionary history represented in each of the plots and looked for a relationship between levels of herbivory and both species richness and phylogenetic diversity using a generalized linear mixed model (GLMM) that could account for variation in herbivory levels between species. I found that species richness was positively associated with herbivore damage at the plot-level, in keeping with the results from several other recent studies on this question. On the other hand, phylogenetic diversity was associated with decreased herbivory. Importantly, there was also an interaction between species richness and phylogenetic diversity, such that plots with the highest levels of herbivory were plots which had many species but only if those species tended to be closely related to one another. I propose that these results are the consequence of interactions with herbivores whose diets are phylogenetically specialized (for which I introduce the term cladophage), and how phylogenetic diversity may alter their realized host ranges. These results suggest that incorporating a phylogenetic perspective can add valuable additional insight into the role of plant diversity in explaining or predicting levels of herbivory at a whole-community scale.

Diversity of plant evolutionary lineages promotes arthropod diversity.

Large-scale habitat destruction and climate change result in the non-random loss of evolutionary lineages, reducing the amount of evolutionary history represented in ecological communities. Yet, we have limited understanding of the consequences of evolutionary history on the structure of food webs and the services provided by biological communities. Drawing on 11 years of data from a long-term plant diversity experiment, we show that evolutionary history of plant communities - measured as phylogenetic diversity - strongly predicts diversity and abundance of herbivorous and predatory arthropods. Effects of plant species richness on arthropods become stronger when phylogenetic diversity is high. Plant phylogenetic diversity explains predator and parasitoid richness as strongly as it does herbivore richness. Our findings indicate that accounting for evolutionary relationships is critical to understanding the severity of species loss for food webs and ecosystems, and for developing conservation and restoration policies.

Disturbance alters the phylogenetic composition and structure of plant communities in an old field system.

The changes in phylogenetic composition and structure of communities during succession following disturbance can give us insights into the forces that are shaping communities over time. In abandoned agricultural fields, community composition changes rapidly when a field is plowed, and is thought to reflect a relaxation of competition due to the elimination of dominant species which take time to re-establish. Competition can drive phylogenetic overdispersion, due to phylogenetic conservation of 'niche' traits that allow species to partition resources. Therefore, undisturbed old field communities should exhibit higher phylogenetic dispersion than recently disturbed systems, which should be relatively 'clustered' with respect to phylogenetic relationships. Several measures of phylogenetic structure between plant communities were measured in recently plowed areas and nearby 'undisturbed' sites. There was no difference in the absolute values of these measures between disturbed and 'undisturbed' sites. However, there was a difference in the 'expected' phylogenetic structure between habitats, leading to significantly lower than expected phylogenetic diversity in disturbed plots, and no difference from random expectation in 'undisturbed' plots. This suggests that plant species characteristic of each habitat are fairly evenly distributed on the shared species pool phylogeny, but that once the initial sorting of species into the two habitat types has occurred, the processes operating on them affect each habitat differently. These results were consistent with an analysis of correlation between phylogenetic distance and co-occurrence indices of species pairs in the two habitat types. This study supports the notion that disturbed plots are more clustered than expected, rather than 'undisturbed' plots being more overdispersed, suggesting that disturbed plant communities are being more strongly influenced by environmental filtering of conserved niche traits.

Competition-similarity relationships and the nonlinearity of competitive effects in consumer-resource systems.

Much previous ecological and evolutionary theory about exploitative competition for a continuous spectrum of resources has used the Lotka-Volterra model with competition coefficients given by a Gaussian function of niche separation. Using explicit consumer-resource models, we show that the Lotka-Volterra model and the assumption of a Gaussian competition-similarity relationship both fail to reflect the impact of strong resource depletion, which typically reduces the influence of the most heavily used resources on the competitive interaction. Taking proper account of resource depletion reveals that strong exploitative competition between efficient consumers is usually a highly nonlinear interaction, implying that a single measure is no longer sufficient to characterize the process. The nonlinearity usually entails weak coupling of competing species when their abundances are high and equal. Rare invaders are likely to have effects on abundant residents much larger than those of the resident on the invader. Asymmetrical utilization curves often produce asymmetrical competition coefficients. Competition coefficients are typically non-Gaussian and are often nonmonotonic functions of niche separation. Utilization curve shape and resource growth functions can have major effects on competition-similarity relationships. A variety of previous theoretical findings need to be reassessed in light of these results.