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Tack, A. J. M.

Publications and source records attributed to Tack, A. J. M..

13 recordsLinked to original sources

Global homeostatic forces shape the composition of a hyperdiverse tropical insect fauna

Despite comprising the bulk of terrestrial biodiversity, we know surprisingly little about insect faunas, particularly in the tropics. Here, we characterize the insect fauna of Madagascar, a global biodiversity hotspot, based on extensive DNA metabarcoding of Malaise trap and leaf litter samples. We estimate that the fauna comprises at least 250,000 species, only 5% of which are currently recorded. The ecological and taxonomic composition is surprisingly similar to that of temperate forests. We show that this is likely caused by global homeostatic forces shaping net diversification rates after colonization of Madagascar rather than by the composition of colonizing lineages. Features differing from temperate forests include the dearth of parasitoids and richness of beetles. Understanding the forces shaping these patterns is key in sustainable management of tropical insect faunas.

evolutionary biology↗

Accuracy of occurrence and abundance estimates from insect metabarcoding

1. DNA metabarcoding--high-throughput sequencing of barcode regions from bulk samples--has become a key tool for insect biodiversity assessment. Yet, how methodological choices affect the accuracy of metabarcoding data remains insufficiently explored. In this paper, we ask: (1) How does the lysis method (non-destructive lysis vs. destructive homogenization) affect community recovery? (2) How comprehensively does metabarcoding capture species richness? (3) To what extent can spike-ins improve abundance estimates? (4) How accurately can species abundances be estimated? 2. We evaluated the accuracy of insect metabarcoding using 4,749 bulk samples from a large-scale biodiversity survey subjected to mild lysis. Of these samples, 856 were also homogenized, allowing a systematic comparison of the effect of alternative treatments. To potentially improve abundance estimates, we added six biological spike-ins (i.e., foreign insects) to all samples, and two synthetic spike-ins (artificial DNA fragments) to the homogenization treatment. In addition, we established the contents of 15 samples by individually barcoding all specimens, enabling direct assessment of occurrence and abundance estimates. 3. Our results revealed consistent differences between destructive and non-destructive treatments. While both methods reliably detected the majority of species, small and soft-bodied taxa were more often recovered after mild lysis than after homogenization, while the reverse was true for heavily sclerotized, hairy, and large taxa. Using biological spike-ins for calibration reduced the variance in read numbers per specimen considerably, especially in homogenized samples, while synthetic spike-ins were less effective. In a Bayesian analysis, where species data were matched to the best-fitting spike-in calibration curve, accurate abundance estimates (+/-1 individual) were obtained for 72.9% of species occurrences. 4. Our results show that it is possible to obtain reasonably accurate abundance estimates from metabarcoding data, and that mild lysis and homogenization result in different taxon-specific biases in terms of occurrence data, with neither method outperforming the other. Accuracy is improved by homogenization rather than mild lysis of samples, and by the use of biological rather than synthetic spike-ins. Together, these findings provide a major step towards robust, quantitative biodiversity monitoring using DNA-metabarcoding.

zoology↗

Plant sexual and asexual contributions to the seed microbiome

The seed microbiome plays a key role in the assembly of the plant microbiome, which has major impacts on plant functioning. Nonetheless, little is known about the origin of the seed microbiome. We investigated the relative contributions of two hypothesized transmission routes: sexual inheritance (via reproductive organs) and asexual inheritance (via the plant vascular system). To do that, we sampled shoot endophytes both before bloom and at seed maturity stages, apple flower ovaries and pollen sacs, and mature seeds from field-grown apple trees (Malus domestica BO_SCPLOWORKHC_SCPLOW. cv Gala Galaxy Selecta). We showed that bacterial richness, diversity and composition differ among tissue types, with shoots before bloom harboring a higher diversity than ovary and pollen. Source tracking revealed that both sexual (30.3%) and asexual (23.8%) pathways contributed to seed microbiome assembly, with shoots at seed maturity being the dominant source. Notably, a large proportion (49.5%) of the seed microbiome originated from unknown sources. Lastly, the transmission pathways significantly differed among bacterial genera, with Pseudomonas primarily linked to shoots, Rhizobacter to pollen and Burkholderia to the ovary. Insights into seed microbiome origin offers new opportunities to enhance seed health and crop productivity through microbiome-assisted breeding.

ecology↗

Open-land-derived agroforestry and effects of abandonment of management of the main crop on ecosystem services and woody plant diversity

Tropical forests are biodiversity hotspots threatened by deforestation and fragmentation. One strategy to restore tropical forest is to establish agroforestry on open land. However, we lack insights into the social and ecological dynamics of open-land-derived agroforests, and specifically the reasons for and consequences of abandonment. We combined semi-quantitative interviews with biodiversity surveys to examine the reasons for abandonment and the consequences for ecosystem services, disservices, and the woody plant community in the Atlantic Forest region. Reasons for abandonment were primarily related to agroecology. Ecosystem services, disservices, and woody plant diversity had not (yet) differentiated after the abandonment of management. Strengthening agronomic support to farmers is essential to maintain and expand open-land-derived agroforestry. Notably, as abandoned agroforests were not converted back to open land, partly due to legal restrictions, they continued to provide ecosystem services and contributed to the restoration of native tree cover across the landscape.

ecology↗

Fermentative yeast diversity at the northern range limit of their oak tree hosts

Fermentative yeasts play important roles in both ecological and industrial processes but their distribution and abundance in natural environments is not well understood. We investigated the diversity of yeast species associated with oak trees (Quercus spp.) in the northern range limit of oak in Sweden, and identified climatic and ecological conditions governing their distribution. We isolated yeasts from oak bark collected from 28 forests and identified them to the species level using metabarcoding. Most communities were dominated by species in the Saccharomycetaceae family, especially by species of Saccharomyces, Kluyveromyces, and Pichia. Each of these genera showed a distinct latitudinal and longitudinal distribution, and both temperature and precipitation metrics predicted significant variation in their abundance. Consistent with this, laboratory assays revealed significant effects of temperature on the growth of strains collected from different longitudes and latitudes. We further found that older trees harbour more diverse and more balanced microbial communities with more evenly distributed species abundances, and that communities across trees were more similar when sharing a common dominant genus. This work provides a baseline for future studies on the impact of climate change on the microbial biodiversity of temperate forests in northern latitudes, and contributes to a growing collection of fermentative yeasts isolated from the wild with potential for biotechnological applications.

microbiology↗

HAPP: High-Accuracy Pipeline for Processing deep metabarcoding data

We introduce HAPP, a high-accuracy pipeline for processing deep metabarcoding data, leveraging data richness to enhance the signal-to-noise-ratio. Starting with denoised amplicon sequence variants, the pipeline consists of four steps: (1) additional chimera removal, using UCHIME and a strict sample-based approach; (2) taxonomic annotation, combining k-mer matching (SINTAX) to a reference library with phylogenetic placement (EPA-NG) on a reference tree; (3) OTU clustering using SWARM, an open-source algorithm with precision and recall comparable to RESL used in circumscribing BOLD BINs; and (4) noise filtering (NUMTs and sequencing errors), using a new algorithm introduced here, NEEAT, which combines "echo" signals across samples with detection of unusual evolutionary signatures among clusters with similar DNA sequences. HAPP computations are parallelized across taxa, making analyses tractable on very large datasets. The performance of HAPP was validated through extensive benchmarks, involving CO1 data from BOLD and Malaise trap data, demonstrating significant improvements over the state of the art.

bioinformatics↗

High-throughput biodiversity surveying sheds new light on the brightest of insect taxa

Sampling of species-rich taxa followed by DNA metabarcoding is quickly becoming a popular high-throughput method for biodiversity inventories. Unfortunately, we know little about its accuracy and efficiency, as the results mostly pertain to poorly-known organism groups in underexplored environments or regions of the world. Here we ask what an extensive sampling effort based on Malaise trapping and metabarcoding can tell us about the lepidopteran fauna of Sweden - one of the best-understood insect taxa in one of the most-surveyed countries of the world. Specifically, we deployed 197 Malaise traps for a single year across Sweden in a systematic sampling design, then metabarcoded the resulting 4,749 bulk samples, and compared the results to existing data sources. We detected more than half (1,535) of the 2,990 lepidopteran species ever recorded as occurring in Sweden, and 323 species not reported during the sampling period by other data providers. Full-length barcoding of individual specimens confirmed three new species for the country and extensive range extensions for two species. It also corroborated eight genetically distinct COI variants that may represent new species to science, one of which has since been described. Most of the new records are for small and inconspicuous species and poorly surveyed regions, suggesting that they represent previously overlooked components of the fauna. Our findings, corroborated by independent metagenomic analyses, show that DNA metabarcoding can be a highly efficient and accurate method of biodiversity sampling, to the extent that it can generate significant new discoveries even for the most well-known of insect faunas.

zoology↗

Biotic and abiotic drivers of ecosystem functioning differ between a temperate and a tropical region

Any single ecosystem will provide many ecosystem functions. Whether these functions tend to increase in concert or trade off against each other is a question of much current interest. Equally topical are the drivers behind ecosystem function rates. Yet, we lack large-scale systematic studies that investigate how abiotic factors can directly or indirectly -- via effects on biodiversity -- drive ecosystem functioning. In this study, we assessed the impact of climate, landscape and biotic community on ecosystem functioning and multifunctioning in the temperate and tropical zone, and investigated potential trade-offs among ecosystem functions in both zones. To achieve this, we measured a diverse set of insect-related ecosystem functions -- including herbivory, seed dispersal, predation, decomposition and pollination -- at 50 sites across Madagascar and 171 sites across Sweden, and characterized the insect community at each site using Malaise traps. We used structural equations models to infer causality of the effects of climate, landscape, and biodiversity on ecosystem functioning. For the temperate zone, we found that abiotic factors were more important than biotic factors in driving ecosystem functioning, while in the tropical zone, effects of biotic drivers were most pronounced. In terms of trade-offs among functions, in the temperate zone, only seed dispersal and predation were positively correlated, while all other functions were uncorrelated. By contrast, in the tropical zone, most ecosystem functions increased in concert, highlighting that tropical ecosystems can simultaneously provide a diverse set of functions. These correlated functions in Madagascar could for the most part be explained by similar responses to local climate, landscape, and biota. Our study suggests that the functioning of temperate and tropical ecosystems differs fundamentally in patterns and drivers. Without a better understanding of these differences, it will be impossible to correctly predict shifts in ecosystem functioning in response to environmental disturbances. To identify global patterns and drivers of ecosystem functioning, we will next need replicate sampling across biomes - as here achieved for two regions, thus paving the road and setting the baseline expectations.

ecology↗

Does urbanization lead to parallel demographic shifts across the world in a cosmopolitan plant?

Urbanization is occurring globally, leading to dramatic environmental changes that are altering the ecology and evolution of species. In particular, the expansion of human infrastructure and the loss and fragmentation of natural habitats in cities is predicted to increase genetic drift and reduce gene flow by reducing the size and connectivity of populations. Alternatively, the "urban facilitation model" suggests that some species will have greater gene flow into and within cities leading to higher diversity and lower differentiation in urban populations. These alternative hypotheses have not been contrasted across multiple cities. Here, we used the genomic data from the Global Urban Evolution project (GLUE), to study the effects of urbanization on non-adaptive evolutionary processes of white clover (Trifolium repens) at a global scale. We found that white clover populations presented high genetic diversity and no evidence of a reduction in Ne linked to urbanization. On the contrary, we found that urban populations were less likely to experience a recent decrease in effective population size than rural ones. In addition, we found little genetic structure among populations both globally and between urban and rural populations, which showed extensive gene flow between habitats. Interestingly, white clover displayed overall higher gene flow within urban areas than within rural habitats. Our study provides one of the largest comprehensive tests of demographic effects of urbanization and our results contrast the common perception that heavily altered and fragmented urban environments will reduce the effective population size and genetic diversity of populations and contribute to their isolation.

evolutionary biology↗

Optimizing insect metabarcoding using replicated mock communities

Metabarcoding (high-throughput sequencing of marker gene amplicons) has emerged as a promising and cost-effective method for characterizing insect community samples. Yet, the methodology varies greatly among studies and its performance has not been systematically evaluated to date. In particular, it is unclear how accurately metabarcoding can resolve species communities in terms of presence-absence, abundances, and biomass. Here we use mock community experiments and a simple probabilistic model to evaluate the performance of different metabarcoding protocols. Specifically, we ask four questions: (Q1) How consistent are the recovered community profiles across replicate mock communities?; (Q2) How does the choice of lysis buffer affect the recovery of the original community?; (Q3) How are community estimates affected by differing lysis times and homogenization?; and (Q4) Is it possible to obtain adequate species abundance estimates through the use of biological spike-ins? We show that estimates are quite variable across community replicates. In general, a mild lysis protocol is better at reconstructing species lists and approximate counts, while homogenization is better at retrieving biomass composition. Tiny insects are more likely to be detected in lysates, while some tough species require homogenization to be detected. Results are less consistent across biological replicates for lysates than for homogenates. Some species are associated with strong PCR amplification bias, which complicates the reconstruction of species counts. Yet, with adequate spike-in data, species abundance can be determined with roughly 40% standard error for homogenates, and with roughly 50% standard error for lysates, under ideal conditions. In the latter case, however, this often requires species-specific reference data, while spike-in data generalizes better across species for homogenates. We conclude that a non-destructive, mild lysis approach shows the highest promise for presence/absence description of the community, while also allowing future morphological or molecular work on the material. However, homogenization protocols perform better for characterizing community composition, in particular in terms of biomass.

ecology↗

The impact of microclimate and soil on the ecology and evolution of an arctic plant

The arctic and alpine regions are predicted to experience one of the highest rates of climate change, and the arctic vegetation is expected to be especially sensitive to such changes. Understanding the ecological and evolutionary responses of arctic plant species to changes in climate is therefore a key objective. Geothermal areas, where temperature gradients naturally occur over small spatial scales, and without many of the confounding environmental factors present in latitudinal and other gradient studies, provide a natural experimental setting to examine the impact of temperature on the response of arctic-alpine plants to increasing temperatures. To test the ecological and evolutionary response of the circumpolar alpine bistort (Bistorta vivipara) to temperature, we collected plant material and soil from areas with low, intermediate, and high soil temperatures and grew them in all combinations at three different temperatures. At higher experimental soil temperatures, sprouting was earlier, and plants had more leaves. Sprouting was earlier in soil originating from intermediate temperature and plants had more leaves when grown in soil originating from low temperatures. We did not find evidence of local adaptation or genetic variation in reaction norms among plants originating from areas with low, intermediate, and high soil temperature. Our findings suggest that the alpine bistort has a strong plastic response to warming, but that differences in soil temperature have not resulted in genetic differentiation. The lack of an observed evolutionary response may, for example, be due to the absence of temperature-mediated selection on B. vivipara, or high levels of gene flow balancing differences in selection. When placed within the context of other studies, we conclude that arctic-alpine plant species often show strong plastic responses to spring warming, while evidence of evolutionary responses varies among species.

ecology↗

Spring phenology dominates over shade in affecting seedling performance and plant attack during the growing season

O_LIClimate change is affecting both the abiotic environment and the seasonal timing of life history events, with potentially major consequences for plant performance and plant-associated food webs. Despite this, we lack insights into how effects of plant phenology on plant performance and food webs depend on environmental conditions, and to what extent effects of phenology and the environment on plant performance are direct vs. mediated by changes in the plant-associated community. C_LIO_LIWe conducted a multifactorial field experiment to test for the effect of spring phenology and shade on Quercus robur seedling traits and performance, as well as attacks by specialist plant pathogens, insects and small mammals. C_LIO_LISpring phenology strongly affected seedling performance whereas shade only affected leaf thickness and chlorophyll. Likewise, spring phenology strongly affected herbivore and pathogen attack, whereas shade and its interaction with spring phenology only explained a minor part of the variation. Small mammals preferentially attacked later phenology seedlings, which strongly affected plant survival, while insect herbivores and pathogens did not mediate the effect of spring phenology and shade on plant performance. C_LIO_LISynthesis: This study highlights that the effect of spring phenology outweighs the effect of environmental context on plant performance and plant attack during the growing season. Interestingly, small mammal herbivores, and not diseases and insect herbivores, may play a key role in mediating the effect of spring phenology on plant performance. Together, these findings advance our understanding of the consequences of climate-induced changes in spring phenology and the abiotic environment on plant performance within a community context. C_LI

ecology↗

Can school children support ecological research? Lessons from the ‘Oak bodyguard’ citizen science project

Scientific knowledge in the field of ecology is increasingly enriched by data acquired by the general public participating in citizen science (CS) programs. Yet, doubts remain about the reliability of such data, in particular when acquired by school children. We built upon an ongoing CS program - Oak bodyguards - to assess the ability of European schoolchildren to accurately estimate the strength of biotic interactions in terrestrial ecosystems. We used standardized protocols to estimate predation rates on artificial caterpillars and insect herbivory on oak leaves and compared estimates made by school children, trained and untrained professional scientists (with no or limited expertise in predation or herbivory assessment). Compared to trained scientists, both schoolchildren and untrained professional scientists overestimated predation rates, but assessments made by the latter were more consistent. School children overestimated insect herbivory, as did untrained professional scientists. Thus, raw data acquired by school children participating in CS programs cannot be used and require several quality checks. However, such data are of no less value than data collected by untrained professional scientists and can be calibrated for bias.

scientific communication and education↗