Merging DNA metabarcoding and ecological network analysis to understand and build resilient terrestrial ecosystems

Abstract

Summary1. Significant advances in both mathematical and molecular approaches in ecology offer unprecedented opportunities to describe and understand ecosystem functioning. Ecological networks describe interactions between species, the underlying structure of communities and the function and stability of ecosystems. They provide the ability to assess the robustness of complex ecological communities to species loss, as well as a novel way of guiding restoration. However, empirically quantifying the interactions between entire communities remains a significant challenge. 2. Concomitantly, advances in DNA sequencing technologies are resolving previously intractable questions in functional and taxonomic biodiversity and provide enormous potential to determine hitherto difficult to observe species interactions. Combining DNA metabarcoding approaches with ecological network analysis presents important new opportunities for understanding large-scale ecological and evolutionary processes, as well as providing powerful tools for building ecosystems that are resilient to environmental change. 3. We propose a novel 'nested tagging' metabarcoding approach for the rapid construction of large, phylogenetically structured species-interaction networks. Taking tree-insect-parasitoid ecological networks as an illustration, we show how measures of network robustness, constructed using DNA metabarcoding, can be used to determine the consequences of tree species loss within forests, and forest habitat loss within wider landscapes. By determining which species and habitats are important to network integrity, we propose new directions for forest management. 4. Merging metabarcoding with ecological network analysis provides a revolutionary opportunity to construct some of the largest, phylogenetically structured species-interaction networks to date, providing new ways to: (i) monitor biodiversity and ecosystem functioning; (ii) assess the robustness of interacting communities to species loss; and (iii) build ecosystems that are more resilient to environmental change.

The use of DNA barcodes in food web construction—terrestrial and aquatic ecologists unite!

“…These entries cover the technical challenges and bioinformatics decisions involved in turning from DNA barcoding single individuals to metabarcoding biological communities (Cristescu 2014;Clare et al 2016), the rise of modern molecular dietary analysis (Symondson 2002;Furlong 2015), recommendations for best practices in diet analyses (King et al 2008), and comparisons of specific molecular techniques for reconstructing trophic interactions (Razgour et al 2011;Pompanon et al 2012;Clare 2014;Toju 2015;Evans et al 2016). Rather than repeating what has been said better before, we thus bypass these steps and explicitly focus on a fundamental, conceptual issue: how barcode-based techniques in a broad sense can be applied to improve our understanding of how food webs are actually structured-to resolve both the nodes of the web and the links between them.…”

“…Pocock et al 2012;Wirta et al 2015b). Where the first such "network of ecological networks" have been forced to use different methods to quantifying different interactions (Pocock et al 2012;Sauve et al 2016), DNA barcodes do offer universal tools adaptable to "all" types of interactions (e.g., Clare et al 2014a;Bell et al 2016;Evans et al 2016).…”

“…2D), we may turn to the strategic, hierarchical tagging of compound samples. This will allow the efficient reconstruction of interaction structures across large ecological communities with several trophic levels (Evans et al 2016). With sequencing power currently increasing as fast or faster than computing power (Carlson 2011), the challenge is not in how much interaction data we can generate, but how we can keep track of samples of "who interacted with whom where" and process this information.…”

“…Where previous approaches have inferred a phylogenetic signal in interaction structure by combining interaction webs with phylogeny inferred from external sources, molecular information will allow the reconstruction of phylogenies from the samples themselves (Elias et al 2013;Evans et al 2016). Here, genomic approaches will add manifold to the information content as compared to classic DNA barcodes only (Papadopoulou et al 2015;Andújar et al 2015;Linard et al 2015)-again building a natural extension from previous studies advancing from one to multiple (Nyman et al 2007(Nyman et al , 2015Kress et al 2009Kress et al , 2015 gene regions.…”

Detecting host–parasitoid interactions in an invasive Lepidopteran using nested tagging DNA metabarcoding

“…In this study, we have two interlinked objectives as follows: (i) to present a simplified version of nested metabarcoding methods for determining OPM–parasitoid interactions using a single PCR locus for a large number of samples, including improvements to control cross‐contamination; and (ii) demonstrate the utility of nested metabarcoding for detecting species interactions by determining the parasitoid identities and rates for one recently established population of OPM in the United Kingdom using a reproducible pipeline for creating host–parasitoid networks (metaBEAT 0.97.7 https://github.com/HullUni-bioinformatics/metaBEAT) with a downloadable working environment conveniently packaged in Docker (Merkel, ) and GitHub (GitHub Inc.). By combining these objectives, we discuss how the ability to link metadata to individuals opens many new avenues for research including the ability to create larger more highly resolved ecological networks for habitat management and restoration (Evans et al., ).…”