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bioRxiv2017

Estimating sampling completeness of interactions in quantitative bipartite ecological networks: incorporating variation in species specialisation

BackgroundThe analysis of ecological networks can be affected by sampling effort, potentially leading to bias. Ecological network structure is often summarised by descriptive metrics but these metrics can vary according to the proportion of the total interactions that have been observed. Therefore, to know the likely degree of bias, it is valuable to estimate the total number of interactions in a network, and so calculate the proportion of interactions that have been observed (sampling completeness of interactions). Existing approaches to estimate sampling completeness of interactions use the Chao family of asymptotic species richness estimators to predict the total number of interactions, but do not fully utilise information about the relative specialisation of species within the network.\n\nResultsHere, we propose a modification of previously-used methods, that places equal weight on each interaction (whether or not it has been observed), rather than on each species. Our approach is therefore equivalent to weighting the interaction sampling completeness of each species in the network according to its relative specialisation. We demonstrate that, for the subset of species that are observed and when assuming that species richness estimators accurately project the number of unobserved interactions per observed species, our approach is mathematically more accurate. Our approach can be universally applied to any quantitative, bipartite network.\n\nWe propose two methods to estimation using our approach, using abundance-based and incidence-based species richness estimators respectively, and give recommendations when each should be applied. We discuss the effect of unobserved species and the potential use of a threshold of minimum abundance for species inclusion. Finally, we consider these advances in the context of some of the main issues surrounding estimation of interaction sampling completeness in network ecology.\n\nConclusionsWe recommend that future studies of bipartite networks utilise our approach and methods to estimate the sampling completeness of interactions, to assist with the quantitative and comparative analysis and interpretation of network properties.

ecology↗
bioRxiv2017

Whole genome data reveal the complex history of a diverse ecological community

How widespread ecological communities assemble remains a key question in ecology. Trophic interactions between widespread species may reflect a shared population history, or ecological sorting of local pools of species with very different population histories. Which scenario applies is central to the stability of trophic associations, and the potential for coevolution between species. Here we show how alternative community assembly hypotheses can be discriminated using whole genome data for component species, and provide a novel likelihood framework that overcomes current limitations in formal comparison of multispecies histories. We illustrate our approach by inferring the assembly history of a Western Palaearctic community of insect herbivores and parasitoid natural enemies, trophic groups that together comprise 50% of terrestrial species. We reject models of co-dispersal from a shared origin, and of delayed enemy pursuit of their herbivore hosts, arguing against herbivore attainment of enemy-free space. The community-wide distribution of species expansion times is also incompatible with a random, neutral model of assembly. Instead, we reveal a complex assembly history of single- and multi-species range expansions through the Pleistocene from different directions and over a range of timescales. Our results suggest substantial turnover in species associations, and argue against tight coevolution in this system. The approach we illustrate is widely applicable to natural communities of non-model species, and makes it possible to reveal the historical backdrop against which selection acts.

ecology↗
bioRxiv2018

Disturbance macroecology: integrating disturbance ecology and macroecology in different-age post-fire stands of a closed-cone pine forest as a case study

Macroecological studies have generally restricted their scope to relatively steady-state systems, and as a result, how biodiversity and abundance metrics are expected to scale in disturbance-dependent ecosystems is unknown. We examine macroecological patterns in a fire-dependent forest of Bishop pine (Pinus muricata). We target two different-aged stands in a stand-replacing fire regime, one a characteristically mature stand with a diverse understory, and one more recently disturbed by a stand-replacing fire (17 years prior to measurement). We compare the stands using macroecological metrics of species richness, abundance and spatial distributions that are predicted by the Maximum Entropy Theory of Ecology (METE), an information-entropy based theory that has proven highly successful in predicting macroecological metrics across a wide variety of systems and taxa. Ecological patterns in the mature stand more closely match METE predictions than do data from the recently disturbed stand. This suggests METEs predictions are more robust in late-successional, slowly changing, or steady-state systems than those in rapid flux with respect to species composition, abundances, and organisms sizes. Our findings highlight the need for a macroecological theory that incorporates natural disturbance and other ecological perturbations into its predictive capabilities, because most natural systems are not in a steady state.

ecology↗
bioRxiv2018

Towards an Ecological Trait-data Standard

O_LITrait-based approaches are widespread throughout ecological research, offering great potential for trait data to deliver general and mechanistic conclusions. Accordingly,a wealth of trait data is available for many organism groups, but, due to a lack of standardisation, these data come in heterogeneous formats.\nC_LIO_LIWe review current initiatives and infrastructures for standardising trait data and discuss the importance of standardisation for trait data hosted in distributed open-access repositories.\nC_LIO_LIIn order to facilitate the standardisation and harmonisation of distributed trait datasets, we propose a general and simple vocabulary as well as a simple data structure for storing and sharing ecological trait data.\nC_LIO_LIAdditionally, we provide an R-package that enables the transformation of any tabular dataset into the proposed format. This also allows trait datasets from heterogeneous sources to be harmonised and merged, thus facilitating data compilation for any particular research focus.\nC_LIO_LIWith these decentralised tools for trait-data harmonisation, we intend to facilitate the exchange and analysis of trait data within ecological research and enable global syntheses of traits across a wide range of taxa and ecosystems.\nC_LI

ecology↗
bioRxiv2018

Implementation of the Water Framework Directive: Lessons learned and future perspectives for an ecologically meaningful classification of the status of Greek lakes, Mediterranean region

The enactment of the Water Framework Directive (WFD) initiated scientific efforts to develop reliable methods for comparing prevailing lake conditions against reference (or non-impaired) states, using the state of a set biological elements. Drawing a distinction between impaired and natural conditions can be a challenging exercise, as it stipulates the robust delineation of reference conditions along with the establishment of threshold values for key environmental variables used as proxies for the degree of system impairment. Another important aspect is to ensure that water quality assessment is comparable among the different Member States. In this context, the present paper offers a constructive critique of the practices followed during the WFD implementation in Greece by pinpointing methodological weaknesses and knowledge gaps that undermine our ability to classify the ecological status of Greek lakes. One of the pillars of WDF is a valid lake typology that sets ecological standards transcending geographic regions and national boundaries. The national typology of Greek lakes has failed to take into account essential components (e.g. surface area, altitude, salinity). WFD compliance assessments based on descriptions of phytoplankton communities are oversimplified and as such should be revisited. Exclusion of most chroococcal species from the analysis of cyanobacteria biovolume in Greek lakes and most reservoirs in the Mediterranean Geographical Intercalibration Group (Greece, Spain, Portugal and Cyprus) is not consistent with the distribution of those taxa in lakes. Similarly, the total biovolume reference values and the indices used in their classification schemes reflect misunderstandings of WFD core principles. This hampers the comparability of ecological status across Europe and leads to quality standards that are too relaxed to provide an efficient target especially for the protection and management of Greek/transboundary lakes such as Lake Megali Prespa, one of the oldest lakes in Europe.

ecology↗
bioRxiv2018

Superior dispersal ability leads to persistent ecological dominance by Candida pseudoglaebosa in the Sarracenia purpurea fungal metacommunity

A large number of descriptive surveys document changes in microbial communities over time, but direct evidence for the ecological processes mediating succession or causing ecological dominance remains rare. Differential dispersal may be a key mechanism. We surveyed microbial diversity within a metacommunity of pitchers of the model carnivorous plant Sarracenia purpurea and discovered the yeast Candida pseudoglaebosa as ecologically dominant. Its frequency in the metacommunity increased over the growing season, and it was not replaced by other taxa. We next measured its competitive ability in a manipulative laboratory experiment and tracked its dispersal over time in nature. Despite its dominance, C. pseudoglaebosa is not a superior competitor. Instead, it is a superior disperser: it arrives in pitchers earlier, and disperses into more pitchers, than other taxa. Differential dispersal across the spatially structured metacommunity of individual pitchers emerges as a key driver of the continuous dominance of C. pseudoglaebosa during succession.

ecology↗
bioRxiv2018

Climate as a driver of adaptive variations in ecological strategies in Arabidopsis thaliana

Background and aimsThe CSR classification categorizes plant species between stress-tolerators, ruderals (R) and competitors (C). Initially proposed as a general framework to describe ecological strategies at the interspecific level, this scheme has recently been used to investigate the variation of strategies within species. For instance, ample variation along the S-R axis was found in Arabidopsis thaliana, with stress-tolerator accessions predominating in hot and dry regions.\n\nMethodsIn this study, the range of CSR strategies within A. thaliana was evaluated across 426 accessions originating from North Africa to Scandinavia. A position in the CSR strategy space was allocated for every accession based on three functional traits: leaf area, leaf dry matter content (LDMC) and specific leaf area (SLA). Results were related to climate at origin and compared to a previous study performed on the same species. Furthermore, the role of natural selection in phenotypic differentiation between lineages was investigated with Qst-Fst comparisons, using the large genetic information available for this species.\n\nKey resultsSubstantial variation in ecological strategies along the S-R axis was found in A. thaliana. By contrast with previous findings, stress-tolerator accessions predominated in cold climates, notably Scandinavia, where late flowering was associated with traits related to resource conservation such as high LDMC and low SLA. Because of trait plasticity, variations in CSR classification to growth conditions were also observed for the same genotypes.\n\nConclusionsThere is a latitudinal gradient of ecological strategies in A. thaliana as a result of within-species adaptation to climate. Our study also underlines the importance of growth conditions and of the methodology used for trait measurement, notably age versus stage measurement, to infer the strength and direction of trait-environment relationships. Taken together, this highlights the potential and limitations of the CSR classification to explain functional adaptation to the environment.

ecology↗
bioRxiv2018

The ecological drivers of variation in global language diversity

Language diversity is distributed unevenly over the globe. Why do some areas have so many different languages and other areas so few? Intriguingly, patterns of language diversity resemble biodiversity patterns, leading to suggestions that similar mechanisms may underlie both linguistic and biological diversification. Here we present the first global analysis of language diversity that identifies the relative importance of two key ecological mechanisms suggested to promote language diversification - isolation and ecological risk - after correcting for spatial autocorrelation and phylogenetic non-independence. We find significant effects of climate on language diversity consistent with the ecological risk hypothesis that areas of high year-round productivity lead to more languages by supporting human cultural groups with smaller distributions. Climate has a much stronger effect on language diversity than landscape features that might contribute to isolation of cultural groups, such as altitudinal variation, river density, or landscape roughness. The association between biodiversity and language diversity appears to be an incidental effect of their covariation with climate, rather than a causal link between the two. While climate and landscape provide strong explanatory signal for variation in language diversity, we identify a number of areas of high unexplained language diversity, with more languages than would be predicted from environmental features alone; notably New Guinea, the Himalayan foothills, West Africa, and Mesoamerica. Additional processes may be at play in generating higher than expected language diversity in these regions.

ecology↗
bioRxiv2018

Size-based ecological interactions drive food web responses to climate warming

Predicting the impacts of climate change on animal populations and communities requires understanding of feedbacks between direct physiological responses and indirect effects via ecological interactions. Food-dependent body growth and within-species size variation have major effects on dynamics of populations and communities through feedbacks between individual performance and population size structure. Moreover, evidence suggests a link between temperature and population size structure, but we lack an understanding of how this is mediated by species interactions when life history processes are food-dependent. Here, we use a dynamic stage-structured biomass model with food-, size- and temperature-dependent life history processes to assess how temperature affects coexistence, stability and size structure in a tri-trophic food chain. We show that predator biomass densities decline with warming either gradually or in the form of collapses, depending on which consumer life stage they predominantly feed on. Collapses occur when warming destabilizes the community and induces alternative stable states via Allee effects, which emerge when predators promote their own food source through predation. By contrast, warming at low temperatures stabilizes the community as limit cycles turn to fixed point dynamics, unless predators feed only on juveniles. Elevated costs of being large in warmer environments accelerate the decline in predator persistence and mean body size of the community. These results suggest that predator persistence in warmer climates may be lower than previously acknowledged when accounting for size- and food-dependence of life history processes, and that interactions within and between species can mediate the effects of warming on food web stability.\n\nSignificanceClimate warming is altering the dynamics and structure of aquatic ecosystems worldwide. Predicting food web reorganization under rising temperatures requires an understanding of physiological responses and ecological interactions of organisms, both of which depend on body size. We show that size variation within species, food-dependent growth and ecological interactions critically affect how food chains respond to warming. Specifically, warming can stabilize or destabilize food chains and expose predators to increased risk of sudden collapses, resulting in alternative stable food web states. Increasing temperatures can cause abrupt reductions in mean community body size, primarily due to loss of top predators. The potential loss of biodiversity and shifts in ecosystem stability are among the major challenges caused by a warming climate.

ecology↗
bioRxiv2018

Relationship between ecological stoichiometry and community diversity of plant ecosystems in the upper reaches of the Tarim River, China

AimAlthough it is commonly proposed that nutrient cycling can impact plant community diversity, this relationship has not been fully examined in arid and semi-arid zones. Here, we expand on the framework for evaluating the relationship between biodiversity and ecological stoichiometry by scaling up from the level of the community.\n\nLocationThe upper reaches of the Tarim River (Northwest China, 80{degrees}10-84{degrees}36E, 0{degrees}25-41{degrees}10N).\n\nMethodsWe used multivariate analysis of variance to compare the stoichiometric characteristics and species diversity indices of sampled plant communities. We also measured carbon (C), nitrogen (N), and phosphorous (P) content of plants. We then assessed correlations between community stoichiometry and species diversity through structural equation models (SEM) and redundancy analysis (RDA).\n\nResultsWe found that the differences between stoichiometric characteristics and community diversity indices were highly significant. The Margalef index was strongly related to C and P content. The Simpsons index and Shannon-Weaner index were most strongly correlated with C content. Pielous index was closely related to C and N contents, and the C:N and C:P ratios were important at driving ecological dominance.\n\nMain ConclusionsOur study highlights the importance of ecological stoichiometry in driving community assembly and diversity within a desert ecosystems in northwestern China. The relationship between eclogical stoichiometry in the desert plant community had an effect on species diversity, and it was a good indicator of plant community diversity.

ecology↗
bioRxiv2014

Horizontal Transfers and Gene Losses in the phospholipid pathway of Bartonella reveal clues about early ecological niches

Bartonellae are mammalian pathogens vectored by blood-feeding arthropods. Although of increasing medical importance, little is known about their ecological past, and host associations are underexplored. Previous studies suggest an influence of horizontal gene transfers in ecological niche colonization by acquisition of host pathogenicity genes. We here expand these analyses to metabolic pathways of 28 Bartonella genomes, and experimentally explore the distribution of bartonellae in 21 species of blood-feeding arthropods. Across genomes, repeated gene losses and horizontal gains in the phospholipid pathway were found. The evolutionary timing of these patterns suggests functional consequences likely leading to an early intracellular lifestyle for stem bartonellae. Comparative phylogenomic analyses discover three independent lineage-specific reacquisitions of a core metabolic gene - NAD(P)H-dependent glycerol-3-phosphate dehydrogenase (gpsA) - from Gammaproteobacteria and Epsilonproteobacteria. Transferred genes are significantly closely related to invertebrate Arsenophonus-, and Serratia-like endosymbionts, and mammalian Helicobacter-like pathogens, supporting a cellular association with arthropods and mammals at the base of extant bartonellae. Our studies suggest that the horizontal re-aquisitions had a key impact on bartonellae lineage specific ecological and functional evolution.

Microbiology↗
bioRxiv2014

The emergence of network structure, complementarity and convergence from basic ecological and genetic processes

Plant-animal mutualistic networks are highly diverse and structured. This has been explained by coevolution through niche based processes. However, this explanation is only warranted if neutral processes (e.g. limited dispersal, genetic and ecological drift) cannot explain these patterns. Here we present a spatially explicit model based on explicit genetics and quantitative traits to study the connection between genome evolution, speciation and plant-animal network demography. We consider simple processes for the speciation dynamics of plant-animal mutualisms: ecological (dispersal, demography) and genetic processes (mutation, recombination, drift) and morphological constraints (matching of quantitative trait) for species interactions, particularly mating. We find the evolution of trait convergence and complementarity and topological features observed in real plant-animal mutualistic webs (i.e. nestedness and centrality). Furthermore, the morphological constraint for plant reproduction generates higher centrality among plant individuals (and species) than in animals, consistent with observations. We argue that simple processes are able to reproduce some well known ecological and evolutionary patterns of plant-animal mutualistic webs.

Evolutionary Biology↗
bioRxiv2014

Connecting people and ideas from around the world: global innovation platforms for next-generation ecology and beyond

We present a case for using global community innovation platforms (GCIPs), an approach to improve innovation and knowledge exchange in international scientific communities through a common and open online infrastructure. We highlight the value of GCIPs by focusing on recent efforts targeting the ecological sciences, where GCIPs are of high relevance given the urgent need for interdisciplinary, geographical, and cross-sector collaboration to cope with growing challenges to the environment as well as the scientific community itself. Amidst the emergence of new international institutions, organizations, and dedicated meetings, GCIPs provide a stable international infrastructure for rapid and long-term coordination that can be accessed by any individual. The accessibility can be particularly important for researchers early in their careers. Recent examples of early career GCIPs complement an array of existing options for early career scientists to improve skill sets, increase academic and social impact, and broaden career opportunities. In particular, we provide a number of examples of existing early career initiatives that incorporate elements from the GCIPs approach, and highlight an in-depth case study from the ecological sciences: the International Network of Next-Generation Ecologists (INNGE), initiated in 2010 with support from the International Association for Ecology and 18 member institutions from six continents.

Preprint↗
bioRxiv2015

Ecological and evolutionary adaptations shape the gut microbiome of BaAka African rainforest hunter-gatherers

The gut microbiome provides access to otherwise unavailable metabolic and immune functions, likely affecting mammalian fitness and evolution. To investigate how this microbial ecosystem impacts evolutionary adaptation of humans to particular habitats, we explore the gut microbiome and metabolome of the BaAka rainforest hunter-gatherers from Central Africa. The data demonstrate that the BaAka harbor a colonic ecosystem dominated by Prevotellaceae and other taxa likely related to an increased capacity to metabolize plant structural polysaccharides, phenolics, and lipids. A comparative analysis shows that the BaAka gut microbiome shares similar patterns with that of the Hadza, another hunter-gatherer population from Tanzania. Nevertheless, the BaAka harbor significantly higher bacterial diversity and pathogen load compared to the Hadza, as well as other Western populations. We show that the traits unique to the BaAka microbiome and metabolome likely reflect adaptations to hunter-gatherer lifestyles and particular subsistence patterns. We hypothesize that the observed increase in microbial diversity and potential pathogenicity in the BaAka microbiome has been facilitated by evolutionary adaptations in immunity genes, resulting in a more tolerant immune system.\n\nSignificanceHuman ecological adaptation requires changes at the genomic level. However, the gut microbiome, the collection of microbes inhabiting the gastrointestinal tract and their functions, also responds significantly to ecological challenge. To determine how the gut microbiome responds to evolutionary adaptations in the host, we profiled gut bacterial communities of the BaAka, rainforest hunter-gatherers from Central Africa. The gut microbiome of the BaAka shows adaptations to metabolize foods rich in fiber, tannins and fats. Similarly, higher bacterial diversity and abundance of pathogenic bacteria, compared to other hunter-gatherers and western populations, suggest that the BaAka immune system evolved to coexist with increased pathogen threats. Accordingly, these results show how the gut microbiome contributes to human ecological plasticity, impacting host adaptation and evolution.

Microbiology↗
bioRxiv2016

Viral coinfection is shaped by bacterial ecology and virus-virus interactions across diverse microbial taxa and environments

Infection of more than one virus in a host, coinfection, is common across taxa and environments. Viral coinfection can enable genetic exchange, alter the dynamics of infections, and change the course of viral evolution. Yet, a systematic test of the factors explaining variation in viral coinfection across different taxa and environments awaits completion. Here I employ three microbial data sets of virus-host interactions covering cross-infectivity, culture coinfection, and single-cell coinfection (total: 6,564 microbial hosts, 13,103 viruses) to provide a broad, comprehensive picture of the ecological and biological factors shaping viral coinfection. I found evidence that ecology and virus-virus interactions are recurrent factors shaping coinfection patterns. Host ecology was a consistent and strong predictor of coinfection across all three datasets: cross-infectivity, culture coinfection, and single-cell coinfection. Host phylogeny or taxonomy was a less consistent predictor, being weak or absent in the cross-infectivity and single-cell coinfection models, yet it was the strongest predictor in the culture coinfection model. Virus-virus interactions strongly affected coinfection. In the largest test of superinfection exclusion to date, prophage sequences reduced culture coinfection by other prophages, with a weaker effect on extrachromosomal virus coinfection. At the single-cell level, prophage sequences eliminated coinfection. Virus-virus interactions also increased culture coinfection with ssDNA-dsDNA coinfections >2x more likely than ssDNA-only coinfections. The presence of CRISPR spacers was associated with a ~50% reduction in single-cell coinfection in a marine bacteria, despite the absence of exact spacer matches in any active infection. Collectively, these results suggest the environment bacteria inhabit and the interactions among surrounding viruses are two factors consistently shaping viral coinfection patterns. These findings highlight the role of virus-virus interactions in coinfection with implications for phage therapy, microbiome dynamics, and viral infection treatments.

Microbiology↗
bioRxiv2016

Adaptive divergence in brain composition between ecologically distinct incipient species

During ecological speciation diverging populations are exposed to contrasting sensory and spatial information that present new behavioral and perceptive challenges. Here, we investigate how brain composition evolves during the early stages of speciation. The incipient species pair, Heliconius erato cyrbia and H. himera, have parapatric ranges across an environmental and altitudinal gradient. Despite continuing gene-flow, these species have divergent ecological, behavioral and physiological traits. We demonstrate that these incipient species also differ significantly in brain composition, especially in the size of sensory structures. H. erato has larger visual components whilst H. himera invests more heavily in olfaction. These differences are not explained by environmentally-induced plasticity, but reflect non-allometric shifts in brain structure. Our results suggest the adaptive evolution of brain structure and function play an important role in facilitating the emergence of ecologically distinct species, and imply that plasticity alone may be insufficient to meet the demands of novel environments.

Evolutionary Biology↗
bioRxiv2016

Ecology, molecules and colour: Multivariate species delimitation and conservation of Harlequin poison frogs

AO_SCPLOWBSTRACTC_SCPLOWWe propose a iterative protocol for delimiting species under the generalized lineage concept (GLC) based on the multivariate clustering of morphological, ecological, and genetic data. Our rationale is that the resulting groups should correspond to evolutionarily independent metapopulation lineages because they reflect the common signal of different secondary defining properties (ecological and genetic distinctiveness, morphological diagnosability, etc.), implying the existence of barriers preventing or limiting gene exchange. We applied this method to study a group of highly endangered poison frogs, the Oophaga histrionica complex. In our study case, we use next generation targeted amplicon sequencing to obtain a robust genetic dataset that we then combined with patterns of morphological and ecological divergence. Our analyses revealed the existence of at least five different species in the histrionica complex (three of them new to science) occurring in very small isolated populations outside any protected areas. More broadly, our study exemplifies how transcriptome-based reduction of genomic complexity and multivariate statistical techniques can be integrated to successfully identify species and their boundaries.\n\nIO_SCPLOWNC_SCPLOWO_SCPCAP C_SCPCAPO_SCPLOWMEMORIAMC_SCPLOW\"I propose that each species has a distinctive life history, which include a series of stages that correspond to some of the named species concepts\"\n\nRichard G. Harrison\n\n1945-2016

Evolutionary Biology↗
bioRxiv2016

The cryptic origins of evolutionary novelty: 1,000-fold-faster trophic diversification rates without increased ecological opportunity or hybrid swarm

Ecological opportunity is frequently proposed as the sole ingredient for adaptive radiation into novel niches. Alternatively, genome-wide hybridization resulting from hybrid swarm may be the trigger. However, these hypotheses have been difficult to test due to the rarity of comparable control environments lacking adaptive radiations. Here I exploit such a pattern in microendemic radiations of Caribbean pupfishes. I show that a sympatric three-species radiation on San Salvador Island, Bahamas diversified 1,445 times faster than neighboring islands in jaw length due to evolution of a novel scale-eating adaptive zone from a generalist ancestral niche. I then sampled 22 generalist populations on seven neighboring islands and measured morphological diversity, stomach content diversity, dietary isotopic diversity, genetic diversity, lake/island areas, macroalgae richness, and Caribbean-wide patterns of gene flow. None of these standard metrics of ecological opportunity or gene flow were associated with adaptive radiation, except for slight increases in macroalgae richness. Thus, exceptional trophic diversification is highly localized despite myriad generalist populations in comparable environmental and genetic backgrounds. This study provides a strong counterexample to the ecological/hybrid-swarm theories of adaptive radiation and suggests that diversification of novel specialists on a sparse fitness landscape is constrained by more than ecological opportunity and gene flow.

Evolutionary Biology↗