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Demographic inference in a spatially-explicit ecological model from genomic data: a proof of concept for the Mojave Desert Tortoise

In this paper, we study the general problem of extracting information from spatially explicit genomic data to inform inference of ecologically and geographically realistic population models. We describe methods and apply them to simulations motivated by the demography of the Mojave desert tortoise (Gopherus agassizii). The tortoise is an example of a long-lived, threatened species for which we have an excellent understanding of range, habitat preference, and certain aspects of demography, but inadequate information on other life history components that are important for conservation management. We use an individual-based model on a discretized geographic landscape with overlapping generations and age and sex-specific dispersal, fecundity, and mortality to develop and test a method that uses genomic data to infer demographic parameters. We do this by seeking parameters that best match a set of spatial statistics of genomes, which we introduce and discuss. We find that for inferring only overall population density and mean migration distance, a simple statistical learning method performs well using simulated training data, inferring parameters to within 10% accuracy. In the process, we introduce spatial analogues of common population genetics statistics, and discuss how and why they are expected to contain signal about the geography of population dynamics that are key for ecological modeling generally and conservation of endangered taxa.

genomics

Underlying mechanisms and ecological consequences of variation in exploratory behavior of the Argentine ant, Linepithema humile

Uncovering how and why animals explore their environment is fundamental for understanding population dynamics, the spread of invasive species, species interactions etc. In social animals, individuals within a group can vary in their exploratory behavior and the behavioral composition of the group can determine its collective success. Workers of the invasive Argentine ant (Linepithema humile) exhibit individual variation in exploratory behavior, which affects the colonys collective nest selection behavior. Here we examine the mechanisms underlying this behavioral variation in exploratory behavior and determine its implications for the ecology of this species. We first establish that individual variation in exploratory behavior is repeatable and consistent across situations. We then show a relationship between exploratory behavior and the expression of genes that have been previously linked with other behaviors in social insects. Specifically, we find a negative relationship between exploratory behavior and the expression of the FOR gene. Finally, we determine how colonies allocate exploratory individuals in natural conditions. We find that ants from inside the nest are the least exploratory individuals, while workers on newly formed foraging trails are the most exploratory individuals. Furthermore, workers in the spring, when new resources emerge, are more exploratory than workers in the winter, potentially allowing the colony to find and exploit new resources. These findings reveal the importance of individual variation in behavior for the ecology of social animals and provide mechanistic and functional explanations for how such behavioral variation can emerge.

animal behavior and cognition

Geographic shifts in Aedes aegypti habitat suitability in Ecuador using larval surveillance data and ecological niche modeling: implications of climate change for public health vector control

Arboviral disease transmission by Aedes mosquitoes poses a major challenge to public health systems in Ecuador, where constraints on health services and resource allocation call for spatially informed management decisions. Employing a unique dataset of larval occurrence records provided by the Ecuadorian Ministry of Health, we used ecological niche models (ENMs) to estimate the current geographic distribution of Aedes aegypti in Ecuador, using mosquito presence as a proxy for risk of disease transmission. ENMs built with the Genetic Algorithm for Rule-Set Production (GARP) algorithm and a suite of environmental variables were assessed for agreement and accuracy. The top model of larval mosquito presence was projected to the year 2050 under various combinations of greenhouse gas emissions scenarios and models of climate change. Under current climatic conditions, larval mosquitoes were not predicted in areas of high elevation in Ecuador, such as the Andes mountain range, as well as the eastern portion of the Amazon basin. However, all models projected to scenarios of future climate change demonstrated potential shifts in mosquito distribution, wherein range contractions were seen throughout most of eastern Ecuador, and areas of transitional elevation became suitable for mosquito presence. Encroachment of Ae. aegypti into mountainous terrain was estimated to affect up to 4,215 km2 under the most extreme scenario of climate change, an area which would put over 12,000 people currently living in transitional areas at risk. This distributional shift into communities at higher elevations indicates an area of concern for public health agencies, as targeted interventions may be needed to protect vulnerable populations with limited prior exposure to mosquito-borne diseases. Ultimately, the results of this study serve as a tool for informing public health policy and mosquito abatement strategies in Ecuador.\n\nAuthor summaryThe yellow fever mosquito (Aedes aegypti) is a medically important vector of arboviral diseases in Ecuador, such as dengue fever and chikungunya. Managing Ae. aegypti is a challenge to public health agencies in Latin America, where the use of limited resources must be planned in an efficient, targeted manner. The spatial distribution of Ae. aegypti can be used as a proxy for risk of disease exposure, guiding policy formation and decision-making. We used ecological niche models in this study to predict the range of Ae. aegypti in Ecuador, based on agency larval mosquito surveillance records and layers of environmental predictors (e.g. climate, altitude, and human population). The best models of current range were then projected to the year 2050 under a variety of greenhouse gas emissions scenarios and models of climate change. All modeled future scenarios predicted shifts in the range of Ae. aegypti, allowing us to assess human populations that may be at risk of becoming exposed to Aedes vectored diseases. As climate changes, we predict that communities living in areas of transitional elevation along the Andes mountain range are vulnerable to the expansion of Aedes aegypti.

epidemiology

Genomic architecture of parallel ecological divergence: beyond a single environmental contrast

The genetic basis of parallel ecological divergence provides important clues to the operation of natural selection and the predictability of evolution. Many examples exist where binary environmental contrasts seem to drive parallel divergence. However, this simplified view can conceal important components of parallel divergence because environmental variation is often more complex. Here, we disentangle the genetic basis of parallel divergence across two axes of environmental differentiation (crab-predation vs. wave-action and low-shore vs. high-shore habitat contrasts) in the marine snail Littorina saxatilis, a well established natural system of parallel ecological divergence. We used whole-genome resequencing across multiple instances of these two environmental axes, at local and regional scales from Spain to Sweden. Overall, sharing of genetic differentiation is generally low but it is highly heterogeneous across the genome and increases at smaller spatial scales. We identified genomic regions, both overlapping and non-overlapping with recently described candidate chromosomal inversions, that are differentially involved in adaptation to each of the environmental axis. Thus, the evolution of parallel divergence in L. saxatilis is largely determined by the joint action of geography, history, genomic architecture and congruence between environmental axes. We argue that the maintenance of standing variation, perhaps as balanced polymorphism, and/or the re-distribution of adaptive variants via gene flow can facilitate parallel divergence in multiple directions as an adaptive response to heterogeneous environments.

evolutionary biology

The determinants of alpine butterfly richness and composition vary according to the ecological traits of species

Predicting spatial patterns of species diversity and composition using suitable environmental predictors is an essential element in conservation planning. Although species have distinct relationships to environmental conditions, some similarities may exist among species that share functional characteristics or traits. We investigated the relationship between species richness, composition and abiotic and biotic environment in different groups of butterflies that share ecological characteristics. We inventoried butterfly species richness in 192 sites and classified all inventoried species in three traits categories: the caterpillars diet breadth, the habitat requirements and the dispersal ability of the adults. We studied how environment, including influence butterfly species richness and composition within each trait category. Across four modelling approaches, the relative influence of environmental variables on butterfly species richness differed for specialists and generalists. Climatic variables were the main determinants of butterfly species richness and composition for generalists, whereas habitat diversity, and plant richness were also important for specialists. Prediction accuracy was lower for specialists than for generalists. Although climate variables represent the strongest drivers affecting butterfly species richness and composition for generalists, plant richness and habitat diversity are at least as important for specialist butterfly species. As specialist butterflies are among those species particularly threatened by global changes, devising accurate predictors to model specialist species richness is extremely important. However, our results indicate that this task will be challenging because more complex predictors are required.

Ecology

Synthetic datasets and community tools for the rapid testing of ecological hypotheses

The increased availability of both open ecological data, and software to interact with it, allows the fast collection and integration of information at all spatial and taxonomic scales. This offers the opportunity to address macroecological questions in a cost-effective way. In this contribution, we illustrate this approach by forecasting the structure of a stream food web at the global scale. In so doing, we highlight the most salient issues needing to be addressed before this approach can be used with a high degree of confidence.

Ecology

Nested metabarcode tagging: a robust tool for studying species interactions in ecology and evolution

Determining the host-parasitoid interactions and parasitism rates for invasive species entering novel environments is an important first step in assessing potential routes for biocontrol and integrated pest management. Conventional insect rearing techniques followed by taxonomic identification are widely used to obtain such data, but this can be time consuming and prone to biases. Here we present a Next Generation Sequencing approach for use in ecological studies which allows for individual level metadata tracking of large numbers of invertebrate samples through the use of hierarchically organised molecular identification tags. We demonstrate its utility using a sample data set examining both species identity and levels of parasitism in late larval stages of the Oak Processionary Moth (Thaumetopoea processionea - Linn. 1758), an invasive species recently established in the UK. Overall we find that there are two main species exploiting the late larval stages of Oak Processionary Moth in the UK with the main parasitoid (Carcelia iliaca-Ratzeburg, 1840) parasitising 45.7% of caterpillars, while a rare secondary parasitoid (Compsilura conccinata-Meigen, 1824) was also detected in 0.4% of caterpillars. Using this approach on all life stages of the Oak Processionary Moth may demonstrate additional parasitoid diversity. We discuss the wider potential of nested tagging DNA-metabarcoding for constructing large, highly-resolved species interaction networks.

Ecology

Symmetric assembly and disassembly of an ecological network

The processes whereby ecological networks emerge, persist and decay throughout ecosystem development are largely unknown. Here we study networks of plant and arbuscular mycorrhizal fungal (AMF) communities along a 120,000 yr soil chronosequence, as they undergo assembly (progression) and then disassembly (retrogression). We found that network assembly and disassembly were symmetrical, self-reinforcing processes that together were capable of generating key attributes of network architecture. Plant and AMF species that had short indirect paths to others in the community (i.e. high centrality), rather than many direct interaction partners (i.e. high degree), were best able to attract new interaction partners and in the case of AMF species, also to retain existing interactions with plants during retrogression. We then show using simulations that these non-random patterns of attachment and detachment promote nestedness of the network. These results have implications for predicting extinction sequences, identifying focal points for invasions, and suggesting trajectories for restoration.

Ecology

A new dispersal-informed null model for community ecology shows strong performance

Null models in ecology have been developed that, by maintaining some aspects of observed communities and repeatedly randomizing others, allow researchers to test for the action of community assembly processes like habitat filtering and competitive exclusion. Such processes are often detected using phylogenetic community structure metrics. When biologically significant elements, such as the number of species per assemblage, break down during randomizations, it can lead to high error rates. Realistic dispersal probabilities are often neglected during randomization, and existing models make the oftentimes empirically unreasonable assumption that all species are equally probable of dispersing to a given site. When this assumption is unwarranted, null models need to incorporate dispersal probabilities. I do so here, and present a dispersal null model (DNM) that strictly maintains species richness, and approximately maintains species occurrence frequencies and total abundance. I tested its statistical performance when used with a wide breadth of phylogenetic community structure metrics across 3,000 simulated communities assembled according to neutral, habitat filtering, and competitive exclusion processes. The DNM performed well, exhibiting low error rates (both type I and II). I also implemented it in a re-analysis of a large empirical dataset, an abundance matrix of 696 sites and 75 species of Australian Meliphagidae. Although the overall signal from that study remained unchanged, it showed that statistically significant phylogenetic clustering could have been an artifact of dispersal limitations.

Ecology

Ecological homogenisation in North American urban yards: vegetation diversity, composition, and structure

Urban ecosystems are widely hypothesised to be more ecologically homogeneous than natural ecosystems. We argue that urban plant communities assemble from a complex mix of horticultural and regional species pools and thus evaluate the homogenisation hypothesis by comparing cultivated and spontaneously occurring urban vegetation to natural area vegetation across seven major US cities. Urban yards were homogenised across cities in terms of their diversity, composition, and structure. First, cultivated and spontaneous yard flora had higher numbers of species than did natural areas but similar phylogenetic diversity, indicating that yard species were drawn from a relatively small number of lineages. Second, yards were compositionally more similar across regions than were natural areas. Finally, vegetation structure, specifically cultivated tree density, was less variable in yards than natural areas across cities. Biodiversity homogenisation likely reflects similar horticultural source pools, homeowner preferences, management practices, and environmental filters across US cities.

Ecology

Resilience, invariability, and ecological stability across levels of organization

Ecological stability is a bewildering broad concept. The most common stability measures are asymptotic resilience, widely used in theoretical studies, and measures based on temporal variability, commonly used in empirical studies. We construct measures of invariability, defined as the inverse of variability, that can be directly compared with asymptotic resilience. We show that asymptotic resilience behaves like the invariability of the most variable species, which is often a rare species close to its extinction boundary. Therefore, asymptotic resilience displays complete loss of stability with changes in community composition. In contrast, mean population invariability and ecosystem invariability are insensitive to rare species and quantify stability consistently whether details of species composition are considered or not. Invariability provides a consistent framework to predict diversity-stability relationships that agree with empirical data at population and ecosystem levels. Our findings can enhance the dialogue between theoretical and empirical stability studies.

ecology

Ecological selection of siderophore-producing microbial taxa in response to heavy metal contamination

Some microbial public goods can provide both individual and community-wide benefits, and are open to exploitation by non-producing species. One such example is the production of metal-detoxifying siderophores. Here, we investigate whether heavy metals select for increased siderophore production in natural microbial communities, or whether exploitation of this detoxifying effect reduces siderophore production. We show that the proportion of siderophore-producing taxa increases along a natural heavy metal gradient. A causal link between metal contamination and siderophore production was subsequently demonstrated in a microcosm experiment in compost, in which we observed changes in community composition towards taxa that produce relatively more siderophores following copper contamination. We confirmed the selective benefit of siderophores by showing that taxa producing large amount of siderophores suffered less growth inhibition in toxic copper. Our results suggest that ecological selection will favour siderophore-mediated decontamination, with important consequences for potential remediation strategies.\n\nAuthorshipEH, SOB, AL, DJH, EvV, AB conceived and designed the experiment. DJH provided new perspectives. EH, SOB, FB, AL collected the data. EH, FB, NT, DJH carried out the data analyses. EH & AB wrote the first draft of the manuscript, and all authors contributed substantially to revisions.\n\nData accessibilityUpon acceptance, data presented in the manuscript will be made available on Dryad.

ecology

Cheater-altruist synergy in immunopathogenic ecological public goods games

Much research has focused on the deleterious effects of free-riding in public goods games, and a variety of mechanisms that suppresses cheating behavior. Here we argue that under certain conditions cheating behavior can be beneficial to the population. In a public goods game, cheaters do not pay for the cost of the public goods, yet they receive the benefit. Although this free-riding harms the entire population in the long run, the success of cheaters may aid the population when there is a common enemy that antagonizes both cooperators and cheaters. Here we study models in which an immune system antagonizes a cooperating pathogen. We investigate three population dynamics models, and determine under what conditions the presence of cheaters help defeat the immune system. The mechanism of action is that a polymorphism of cheaters and altruists optimizes the average growth rate. Our results give support for a possible synergy between cooperators and cheaters in ecological public goods games.

ecology

Designing oil palm landscapes to retain biodiversity using insights from a key ecological indicator group

Oil palm expansion threatens biodiverse ecosystems across the tropics. However, palm oil is a widely used and profitable crop, so identifying strategies that mitigate the impact of oil palm expansion on biodiversity is important. Riparian reserves (strips of forest along rivers) are protected in many countries for hydrological reasons and also support species that would not otherwise persist in oil palm. However, management guidelines for riparian zones have been informed by relatively few ecological studies. We assessed how the structural features and landscape context of riparian reserves in Sabah, Malaysia affected dung beetle communities. We also tested the use of flight intercept traps to study movement of dung beetles along linear forest corridors. Overall, dung beetle abundance in riparian reserves was 54% lower than in logged forest areas, but all species observed in the logged forest were found in at least one riparian reserve site and both species richness and diversity increased with reserve width. Distance from a large block of continuous forest affected dung beetle community composition but not species richness, abundance, or functional diversity. The amount of forest cover in the surrounding landscape improved the retention of species within riparian reserves, and increases in vegetation complexity corresponded with higher functional richness and functional dispersion. The flight intercept traps did not indicate that there is net movement of individuals out of logged forest areas into the riparian reserves. The species richness of 30 m reserves (the suggested requirement of reserves in Sabah) was only 10% lower than in logged forest, but our data indicate that riparian reserves of at least 50 - 80 m are needed for species richness and diversity to equal that in nearby logged forest. These findings, particularly if they apply more widely to forest-dependent taxa, should be taken into account when setting policy and sustainability guidelines for oil palm plantations, both in areas undergoing conversion from forest and in existing oil palm plantations where forest restoration is required.

ecology

The application of zeta diversity as a continuous measure of compositional change in ecology

Zeta diversity provides the average number of shared species across n sites (or shared operational taxonomic units (OTUs) across n cases). It quantifies the variation in species composition of multiple assemblages in space and time to capture the contribution of the full suite of narrow, intermediate and wide-ranging species to biotic heterogeneity. Zeta diversity was proposed for measuring compositional turnover in plant and animal assemblages, but is equally relevant for application to any biological system that can be characterised by a row by column incidence matrix. Here we illustrate the application of zeta diversity to explore compositional change in empirical data, and how observed patterns may be interpreted. We use 10 datasets from a broad range of scales and levels of biological organisation - from DNA molecules to microbes, plants and birds - including one of the original data sets used by R.H. Whittaker in the 1960s to express compositional change and distance decay using beta diversity. The applications show (i) how different sampling schemes used during the calculation of zeta diversity may be appropriate for different data types and ecological questions, (ii) how higher orders of zeta may in some cases better detect shifts, transitions or periodicity, and importantly (iii) the relative roles of rare versus common species in driving patterns of compositional change. By exploring the application of zeta diversity across this broad range of contexts, our goal is to demonstrate its value as a tool for understanding continuous biodiversity turnover and as a metric for filling the empirical gap that exists on spatial or temporal change in compositional diversity.

ecology

The cost of enforcing marine protected areas to achieve ecological targets

Protected areas are the primary management tool for conserving ecosystems, yet their intended outcomes may often be compromised by poaching. Consequently, many protected areas are ineffective paper parks that contribute little towards conserving ecosystems. Poaching can be prevented through enforcement and engaging with community members so they support protected areas. It is not clear how much needs to be spent on enforcement and engagement to ensure they are frequent enough to be effective at conserving biodiversity. We develop models of enforcement against illegal fishing in marine protected areas. We apply the models to data on fishing rates and fish biomass from a marine protected area in Raja Ampat, Indonesia and explore how frequent enforcement patrols need to be to achieve targets for coral reef fish biomass. Achieving pristine levels of reef fish biomass required almost year-round enforcement of the protected area. Surveillance of the protected area may also be enhanced if local fishers who support the reserve report on poaching. The opportunity for local fishing boats to participate in surveillance was too small for it to have much benefit for total reef fish biomass, which increases slowly. However, specific functional groups of fish have much higher population growth rates and their biomass was predicted to increase markedly with community surveillance. We conclude that budgets for park management must balance the cost of conducting frequent patrols against supporting alternative activities, like education to build community support. Optimized budgets will be much more likely to achieve ecological targets for recovering fish biomasses and will contribute to fiscal sustainability of protected areas.

ecology

On the proportional abundance of species: Integrating population genetics and community ecology

The frequency of genes in interconnected populations and of species in interconnected communities are affected by similar processes, such as birth, death and immigration. The equilibrium distribution of gene frequencies in structured populations is known since the 1930s, under Wrights metapopulation model known as the island model. The equivalent distribution for the species frequency (i.e. the species proportional abundance distribution (SPAD), at the metacommunity level, however, is unknown. In this contribution, we develop a stochastic model to analytically account for this distribution (SPAD). We show that the same as for genes SPAD follows a beta distribution, which provides a good description of empirical data and applies across a continuum of scales. This stochastic model, based upon a diffusion approximation, provides an alternative to neutral models for the species abundance distribution (SAD), which focus on number of individuals instead of proportions, and demonstrate that the relative frequency of genes in local populations and of species within communities follow the same probability law. We hope our contribution will help stimulate the mathematical and conceptual integration of theories in genetics and ecology.

ecology

Ecological Change Points: The strength of density dependence and the loss of history

Change points in the dynamics of animal abundances have extensively been recorded in historical time series records. Little attention has been paid to the theoretical dynamic consequences of such change-points. Here we propose a change-point model of stochastic population dynamics. This investigation embodies a shift of attention from the problem of detecting when a change will occur, to another non-trivial puzzle: using ecological theory to understand and predict the post-breakpoint behavior of the population dynamics. The proposed model and the explicit expressions derived here predict and quantify how density dependence modulates the influence of the pre-breakpoint parameters into the post-breakpoint dynamics. Time series transitioning from one stationary distribution to another contain information about where the process was before the change-point, where is it heading and how long it will take to transition, and here this information is explicitly stated. Importantly, our results provide a direct connection of the strength of density dependence with theoretical properties of dynamic systems, such as the concept of resilience. Finally, we illustrate how to harness such information through maximum likelihood estimation for state-space models, and test the model robustness to widely different forms of compensatory dynamics. The model can be used to estimate important quantities in the theory and practice of population recovery.

ecology