Published November 14, 2021 | Version v1
Journal article Open

Community metabarcoding reveals the relative role of environmental filtering and spatial processes in metacommunity dynamics of soil microarthropods across a mosaic of montane forests

Authors/Creators

  • 1. Department of Biological Sciences, University of Cyprus, Nicosia, Cyprus Instituto de Productos Naturales y Agrobiología (IPNA-CSIC), San Cristóbal de La Laguna, Tenerife, Canary Islands, Spain
  • 2. Department of Biological Sciences, University of Cyprus, Nicosia, Cyprus
  • 3. Instituto de Productos Naturales y Agrobiología (IPNA-CSIC), San Cristóbal de La Laguna, Tenerife, Canary Islands, Spain
  • 4. Department of Life Sciences, Natural History Museum, London, UK
  • 5. Institut de Biologie de l'ENS (IBENS), Ecole Normale Supérieure, CNRS, INSERM, Université PSL, Paris, France
  • 6. Department of Life Sciences, Natural History Museum, London, UK Department of Life Sciences, Silwood Park Campus, Imperial College London, Ascot, UK

Description

Disentangling the relative role of environmental filtering and spatial processes in driving metacommunity structure across mountainous regions remains challenging, as the way we quantify spatial connectivity in topographically and environmentally heterogeneous landscapes can influence our perception of which process predominates. More empirical data sets are required to account for taxon- and context-dependency, but relevant research in understudied areas is often compromised by the taxonomic impediment. Here we used haplotype-level community DNA metabarcoding, enabled by stringent filtering of amplicon sequence variants (ASVs), to characterize metacommunity structure of soil microarthropod assemblages across a mosaic of five forest habitats on the Troodos mountain range in Cyprus. We found similar β diversity patterns at ASV and species (OTU, operational taxonomic unit) levels, which pointed to a primary role of habitat filtering resulting in the existence of largely distinct metacommunities linked to different forest types. Within-habitat turnover was correlated to topoclimatic heterogeneity, again emphasizing the role of environmental filtering. However, when integrating landscape matrix information for the highly fragmented Quercus alnifolia habitat, we also detected a major role of spatial isolation determined by patch connectivity, indicating that stochastic and niche-based processes synergistically govern community assembly. Alpha diversity patterns varied between ASV and OTU levels, with OTU richness decreasing with elevation and ASV richness following a longitudinal gradient, potentially reflecting a decline of genetic diversity eastwards due to historical pressures. Our study demonstrates the utility of haplotype-level community metabarcoding for characterizing metacommunity structure of complex assemblages and improving our understanding of biodiversity dynamics across mountainous landscapes worldwide.

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Additional details

Funding

European Commission
iBioGen - Twinning for European excellence in Island Biodiversity Genomics 810729

References

  • Andrews, S. (2010). fastqc: a quality control tool for high throughput sequence data. Available at http://www.bioinformatics.babraham. ac.uk/projects/fastqc/
  • Andújar, C., Arribas, P., Gray, C., Bruce, C., Woodward, G., Yu, D. W., & Vogler, A. P. (2018). Metabarcoding of freshwater invertebrates to detect the effects of a pesticide spill. Molecular Ecology, 27(1), 146– 166. https://doi.org/10.1111/mec.14410
  • Andújar, C., Creedy, T. J., Arribas, P., López, H., Salces-Castellano, A., Pérez-Delgado, A. J., Vogler, A. P., & Emerson, B. C. (2021). Validated removal of nuclear pseudogenes and sequencing artefacts from mitochondrial metabarcode data. Molecular Ecology Resources, 21(6), 1772–1787. https://doi. org/10.1111/1755-0998.13337
  • Arribas, P., Andújar, C., Bidartondo, M. I., Bohmann, K., Coissac, É., Creer, S., deWaard, J. R., Elbrecht, V., Ficetola, G. F., Goberna, M., Kennedy, S., Krehenwinkel, H., Leese, F., Novotny, V., Ronquist, F., Yu, D. W., Zinger, L., Creedy, T. J., Meramveliotakis, E., … Emerson, B. C. (2021). Connecting high-throughput biodiversity inventories: Opportunities for a site-based genomic framework for global integration and synthesis. Molecular Ecology, 30(5), 1120–1135. https:// doi.org/10.1111/mec.15797
  • Arribas, P., Andújar, C., Hopkins, K., Shepherd, M., & Vogler, A. P. (2016). Metabarcoding and mitochondrial metagenomics of endogean arthropods to unveil the mesofauna of the soil. Methods in Ecology and Evolution, 7(9), 1071–1081. https://doi. org/10.1111/2041-210x.12557
  • Arribas, P., Andújar, C., Salces-Castellano, A., Emerson, B. C., & Vogler, A. P. (2021). The limited spatial scale of dispersal in soil arthropods revealed with whole-community haplotype-level metabarcoding. Molecular Ecology, 30(1), 48–61. https://doi.org/10.1111/ mec.15591
  • Bahram, M., Kohout, P., Anslan, S., Harend, H., Abarenkov, K., & Tedersoo, L. (2016). Stochastic distribution of small soil eukaryotes resulting from high dispersal and drift in a local environment. ISME Journal, 10(4), 885–896. https://doi.org/10.1038/ismej.2015.164
  • Bálint, M., Domisch, S., Engelhardt, C. H. M., Haase, P., Lehrian, S., Sauer, J., Theissinger, K., Pauls, S. U., & Nowak, C. (2011). Cryptic biodiversity loss linked to global climate change. Nature Climate Change, 1(6), 313–318. https://doi.org/10.1038/nclimate1191
  • Baselga, A. (2010). Partitioning the turnover and nestedness components of beta diversity. Global Ecology and Biogeography, 19(1), 134– 143. https://doi.org/10.1111/j.1466-8238.2009.00490.x
  • Baselga, A., Fujisawa, T., Crampton-Platt, A., Bergsten, J., Foster, P. G., Monaghan, M. T., & Vogler, A. P. (2013). Whole-community DNA barcoding reveals a spatio-temporal continuum of biodiversity at species and genetic levels. Nature Communications, 4, 1892. https:// doi.org/10.1038/ncomms2881
  • Baselga, A., Gómez-Rodríguez, C., & Vogler, A. P. (2015). Multihierarchical macroecology at species and genetic levels to discern neutral and non-neutral processes. Global Ecology and Biogeography, 24(8), 873–882. https://doi.org/10.1111/geb.12322
  • Baselga, A., & Orme, C. D. L. (2012). betapart: an r package for the study of beta diversity. Methods in Ecology and Evolution, 3(5), 808–812. https://doi.org/10.1111/j.2041-210X.2012.00224.x
  • Benito, X., Fritz, S. C., Steinitz-Kannan, M., Velez, M. I., & McGlue, M. M. (2018). Lake regionalization and diatom metacommunity structuring in tropical South America. Ecology and Evolution, 8(16), 7865– 7878. https://doi.org/10.1002/ece3.4305
  • Berg, B., & McClaugherty, C. (2008). Plant Litter. Decomposition, humus formation, carbon sequestration, 2nd ed. Springer-Verlag.
  • Berg, M. P. (2012). Patterns of biodiversity at fine and small spatial scales. In D. H. Wall, R. D. Bardgett, V. Behan-Pelletier, J. E. Herrick, T. H. Jones, K. Ritz, J. Six, D. R. Strong, & W. H. van der Putte (Eds.), Soil ecology and ecosystem services (pp. 136–152). Oxford University Press
  • Biswas, S. R., & Wagner, H. H. (2012). Landscape contrast: a solution to hidden assumptions in the metacommunity concept? Landscape Ecology, 27(5), 621–631. https://doi.org/10.1007/s1098 0-012-9732-5
  • Brodie, J. F., & Newmark, W. D. (2019). Heterogeneous matrix habitat drives species occurrences in complex, fragmented landscapes. American Naturalist, 193(5), 748–754. https://doi. org/10.1086/702589
  • Brown, B. L., Sokol, E. R., Skelton, J., & Tornwall, B. (2017). Making sense of metacommunities: dispelling the mythology of a metacommunity typology. Oecologia, 183(3), 643–652. https://doi.org/10.1007/ s00442-016-3792-1
  • Bush, A., Monk, W. A., Compson, Z. G., Peters, D. L., Porter, T. M., Shokralla, S., Wright, M. T. G., Hajibabaei, M., & Baird, D. J. (2020). DNA metabarcoding reveals metacommunity dynamics in a threatened boreal wetland wilderness. Proceedings of the National Academy of Sciences of the United States of America, 117(15), 8539– 8545. https://doi.org/10.1073/pnas.1918741117
  • Callahan, B. J., McMurdie, P. J., & Holmes, S. P. (2017). Exact sequence variants should replace operational taxonomic units in markergene data analysis. ISME Journal, 11(12), 2639–2643. https://doi. org/10.1038/ismej.2017.119
  • Callahan, B. J., McMurdie, P. J., Rosen, M. J., Han, A. W., Johnson, A. J. A., & Holmes, S. P. (2016). dada2: high-resolution sample inference from Illumina amplicon data. Nature Methods, 13(7), 581–583. https://doi.org/10.1038/nmeth.3869
  • Caruso, T., Schaefer, I., Monson, F., & Keith, A. M. (2019). Oribatid mites show how climate and latitudinal gradients in organic matter can drive large-scale biodiversity patterns of soil communities. Journal of Biogeography, 46(3), 611–620. https://doi.org/10.1111/jbi.13501
  • Caruso, T., Taormina, M., & Migliorini, M. (2012). Relative role of deterministic and stochastic determinants of soil animal community: a spatially explicit analysis of oribatid mites. Journal of Animal Ecology, 81(1), 214–221. https://doi.org/10.1111/j.1365-2656.2011.01886.x
  • Chase, J. M. (2005). Towards a really unified theory for metacommunities. Functional Ecology, 19(1), 182–186. https://doi. org/10.1111/j.0269-8463.2005.00937.x
  • Chase, J. M. (2014). Spatial scale resolves the niche versus neutral theory debate. Journal of Vegetation Science, 25(2), 319–322. https://doi. org/10.1111/jvs.12159
  • Chase, J. M., & Leibold, J. (2003). Ecological niches: linking classical and contemporary approaches. The University of Chicago Press.
  • Cicconardi, F., Fanciulli, P. P., & Emerson, B. C. (2013). Collembola, the biological species concept and the underestimation of global species richness. Molecular Ecology, 22(21), 5382–5396. https://doi. org/10.1111/mec.12472
  • Clappe, S., Dray, S., & Peres-Neto, P. R. (2018). Beyond neutrality: disentangling the effects of species sorting and spurious correlations in community analysis. Ecology, 99(8), 1737–1747. https://doi. org/10.1002/ecy.2376
  • Cottenie, K. (2005). Integrating environmental and spatial processes in ecological community dynamics. Ecology Letters, 8(11), 1175–1182. https://doi.org/10.1111/j.1461-0248.2005.00820.x
  • Coulson, S. I., Hodkinson, I. D., & Webb, N. R. (2003). Microscale distribution patterns in high Arctic soil microarthropod communities: the influence of plant species within the vegetation mosaic. Ecography, 26(6), 801–809. https://doi.org/10.1111/j.0906-7590.2003.03646.x
  • Creedy, T. J., Andújar, C., Meramveliotakis, E., Noguerales, V., Overcast, I., Papadopoulou, A., Morlon, H., Vogler, A. P., Emerson, B. C., & Arribas, P. (2021). Coming of age for COI metabarcoding of whole organism community DNA: towards bioinformatic harmonisation. Molecular Ecology Resources, in Press. https://doi. org/10.1111/1755-0998.13502
  • Creedy, T. J., Ng, W. S., & Vogler, A. P. (2019). Toward accurate specieslevel metabarcoding of arthropod communities from the tropical forest canopy. Ecology and Evolution, 9(6), 3105–3116. https://doi. org/10.1002/ece3.4839
  • Decaëns, T. (2010). Macroecological patterns in soil communities. Global Ecology and Biogeography, 19(3), 287–302. https://doi. org/10.1111/j.1466-8238.2009.00517.x
  • Delipetrou, P., Makhzoumi, J., Dimopoulos, P., & Georghiou, K. (2008). Cyprus. In I. N. Vogiatzakis, G. Pungetti, & A. M. Mannion (Eds.), Mediterranean islands landscapes. Natural and cultural approaches (pp. 170–203). Springer-Verlag.
  • Doblas-Miranda, E., Sánchez-Piñero, F., & González-Megías, A. (2009). Different microhabitats affect soil macroinvertebrate assemblages in a Mediterranean arid ecosystem. Applied Soil Ecology, 41(3), 329– 335. https://doi.org/10.1016/j.apsoil.2008.12.008
  • Dopheide, A., Tooman, L. K., Grosser, S., Agabiti, B., Rhode, B., Xie, D., Stevens, M. I., Nelson, N., Buckley, T. R., Drummond, A. J., & Newcomb, R. D. (2019). Estimating the biodiversity of terrestrial invertebrates on a forested island using DNA barcodes and metabarcoding data. Ecological Applications, 29(4), e01877. https://doi. org/10.1002/eap.1877
  • Dray, S., Bauman, D., Blanchet, G., Borcard, D., Clappe, S., Guenard, G., & Wagne, H. H. (2021). adespatial: multivariate multiscale spatial analysis. r package version 0.3-14. Available at https://CRAN.Rproject.org/package=adespatial
  • Edgar, R. (2016). UNOISE2: improved error-correction for Illumina 16S and ITS amplicon sequencing. BioRxiv, 081257, https://doi. org/10.1101/081257
  • Eissfeller, V., Langenbruch, C., Jacob, A., Maraun, M., & Scheu, S. (2013). Tree identity surpasses tree diversity in affecting the community structure of oribatid mites (Oribatida) of deciduous temperate forests. Soil Biology and Biochemistry, 63, 154–162. https://doi. org/10.1016/j.soilbio.2013.03.024
  • Elbrecht, V., Vamos, E. E., Steinke, D., & Leese, F. (2018). Estimating intraspecific genetic diversity from community DNA metabarcoding data. PeerJ, 6, e4644. https://doi.org/10.7717/peerj.4644
  • Eliades, N.-G., Aravanopoulos, F., & Christou, A. (2018). Mediterranean islands hosting marginal and peripheral forest tree populations: the case of Pinus brutia Ten in Cyprus. Forests, 9(9), 514. https://doi. org/10.3390/f9090514
  • Eliades, N.-G.-H., Gailing, O., Leinemann, L., Fady, B., & Finkeldey, R. (2011). High genetic diversity and significant population structure in Cedrus brevifolia Henry, a narrow endemic Mediterranean tree from Cyprus. Plant Systematics and Evolution, 294(3–4), 185–198. https://doi.org/10.1007/s00606-011-0453-z
  • Ferrenberg, S., Martinez, A. S., & Faist, A. M. (2016). Aboveground and belowground arthropods experience different relative influences of stochastic versus deterministic community assembly processes following disturbance. PeerJ, 4, e2545. https://doi.org/10.7717/ peerj.2545
  • Fick, S. E., & Hijmans, R. J. (2017). WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. International Journal of Climatology, 37(12), 4302–4315. https://doi.org/10.1002/ joc.5086
  • Firmiano, K. R., Cañedo-Argüelles, M., Gutiérrez-Canovas, C., Macedo, D. R., Linares, M. S., Bonada, N., & Callisto, M. (2021). Land use and local environment affect macroinvertebrate metacommunity organization in Neotropical stream networks. Journal of Biogeography, 48(3), 479–491. https://doi.org/10.1111/jbi.14020
  • Fletcher, R. J., Burrell, N. S., Reichert, B. E., Vasudev, D., & Austin, J. D. (2016). Divergent perspectives on landscape connectivity reveal consistent effects from genes to communities. Current Landscape Ecology Reports, 1, 67–79. https://doi.org/10.1007/s4082 3-016-0009-6
  • Florinsky, I. V. (2012). Influence of topography on soil properties. In I. V. Florinsky (Ed.), Digital terrain analysis in soil science and geology, 2nd ed. (pp. 265–270). Academic Press-Elsevier
  • Fukami, T. (2015). Historical contingency in community assembly: integrating niches, species pools, and priority effects. Annual Review of Ecology, Evolution, and Systematics, 46(1), 1–23. https://doi. org/10.1146/annurev-ecolsys-110411-160340
  • Gálvez-Reyes, N., Arribas, P., Andújar, C., Emerson, B. C., Piñero, D., & Mastretta-Yanes, A. (2021). Local-scale dispersal constraints promote spatial structure and arthropod diversity within a tropical sky-island. Molecular Ecology, in Press. https://doi.org/10.1111/mec.16195
  • Gan, H., Zak, D. R., & Hunter, M. D. (2019). Scale dependency of dispersal limitation, environmental filtering and biotic interactions determine the diversity and composition of oribatid mite communities. Pedobiologia, 74, 43–53. https://doi.org/10.1016/j. pedobi.2019.03.002
  • Gao, M., Liu, D., Lin, L., & Wu, D. (2016). The small-scale structure of a soil mite metacommunity. European Journal of Soil Biology, 74, 69– 75. https://doi.org/10.1016/j.ejsobi.2016.03.004
  • Gómez-Rodríguez, C., & Baselga, A. (2018). Variation among European beetle taxa in patterns of distance decay of similarity suggests a major role of dispersal processes. Ecography, 41(11), 1825–1834. https://doi.org/10.1111/ecog.03693
  • Graf, R. F., Kramer-Schadt, S., Fernández, N., & Grimm, V. (2007). What you see is where you go? Modeling dispersal in mountainous landscapes. Landscape Ecology, 22(6), 853–866. https://doi. org/10.1007/s10980-006-9073-3
  • Graham, C. H., Carnaval, A. C., Cadena, C. D., Zamudio, K. R., Roberts, T. E., Parra, J. L., McCain, C. M., Bowie, R. C. K., Moritz, C., Baines, S. B., Schneider, C. J., VanDerWal, J., Rahbek, C., Kozak, K. H., & Sanders, N. J. (2014). The origin and maintenance of montane diversity: integrating evolutionary and ecological processes. Ecography, 37(8), 711–719. https://doi.org/10.1111/ecog.00578
  • Gravel, D., Canham, C. D., Beaudet, M., & Messier, C. (2006). Reconciling niche and neutrality: the continuum hypothesis. Ecology Letters, 9(4), 399–409. https://doi.org/10.1111/j.1461-0248.2006.00884.x
  • Grear, J. S., & Schmitz, O. J. (2005). Effects of grouping behavior and predators on the spatial distribution of a forest floor arthropod. Ecology, 86(4), 960–971. https://doi.org/10.1890/04-1509
  • Hartfelder, J., Reynolds, C., Stanton, R. A., Sibiya, M., Monadjem, A., McCleery, R. A., & Fletcher, R. J. J. (2020). The allometry of movement predicts the connectivity of communities. Proceedings of the National Academy of Sciences of the United States of America, 117(36), 22274–22280. https://doi.org/10.1073/ pnas.2001614117
  • Hawkins, B. A., Field, R., Cornell, H. V., Currie, D. J., Guégan, J.-F., Kaufman, D. M., Kerr, J. T., Mittelbach, G. G., Oberdorff, T., O'Brien, E. M., Porter, E. E., & Turner, J. R. G. (2003). Energy, water, and broad-scale geographic patterns of species richness. Ecology, 84(12), 3105–3117. https://doi.org/10.1890/03-8006
  • He, S., Chen, K., Soininen, J., Heino, J., Ding, N., & Wang, B. (2020). Elements of metacommunity structure of diatoms and macroinvertebrates within stream networks differing in environmental heterogeneity. Journal of Biogeography, 47(8), 1755–1764. https://doi. org/10.1111/jbi.13859
  • Hillel, D. (2008). Soil in the environment. Crucible of terrestrial life. Academic Press-Elsevier.
  • Hleap, J. S., Littlefair, J. E., Steinke, D., Hebert, P. D. N., & Cristescu, M. E. (2021). Assessment of current taxonomic assignments strategies for metabarcoding eukaryotes. Molecular Ecology Resources, 21(7), 2190–2203. https://doi.org/10.1111/1755-0998.13407
  • Hoiss, B., Krauss, J., Potts, S. G., Roberts, S., & Steffan-Dewenter, I. (2012). Altitude acts as an environmental filter on phylogenetic composition, traits and diversity in bee communities. Proceedings of the Royal Society B-Biological Sciences, 279(1746), 4447–4456. https://doi.org/10.1098/rspb.2012.1581
  • How, R. A., Cowan, M. A., Teale, R. J., & Schmitt, L. H. (2020). Environmental correlates of reptile variation on the Houtman Abrolhos archipelago, eastern Indian Ocean. Journal of Biogeography, 47(9), 2017– 2028. https://doi.org/10.1111/jbi.13881
  • Hubbell, S. P. (2001). The unified neutral theory of species abundance and diversity. Princeton University Press
  • Huson, D. H., Beier, S., Flade, I., Gorska, A., El-Hadidi, M., Mitra, S., Ruscheweyh, H.-J., & Tappu, R. (2016). MEGAN Community Edition - Interactive Exploration and Analysis of Large-Scale Microbiome Sequencing Data. PLOS Computational Biology, 12(6), e1004957. https://doi.org/10.1371/journal.pcbi.1004957
  • Hutchinson, G. E. (1959). Homage to Santa-Rosalia or why are there so many kinds of animals. American Naturalist, 93(870), 145–159. https://doi.org/10.1086/282070
  • Ingimarsdóttir, M., Caruso, T., Ripa, J., Magnusdottir, O. B., Migliorini, M., & Hedlund, K. (2012). Primary assembly of soil communities: disentangling the effect of dispersal and local environment. Oecologia, 170(3), 745–754. https://doi.org/10.1007/s0044 2-012-2334-8
  • Jamoneau, A., Chabrerie, O., Closset-Kopp, D., & Decocq, G. (2012). Fragmentation alters beta-diversity patterns of habitat specialists within forest metacommunities. Ecography, 35(2), 124–133. https:// doi.org/10.1111/j.1600-0587.2011.06900.x
  • Jombart, T. (2008). adegenet: a r package for the multivariate analysis of genetic markers. Bioinformatics, 24(11), 1403–1405. https://doi. org/10.1093/bioinformatics/btn129
  • Joos, L., Beirinckx, S., Haegeman, A., Debode, J., Vandecasteele, B., Baeyen, S., Goormachtig, S., Clement, L., & De Tender, C. (2020). Daring to be differential: metabarcoding analysis of soil and plantrelated microbial communities using amplicon sequence variants and operational taxonomical units. BMC Genomics, 21(1), 733. https://doi.org/10.1186/s12864-020-07126-4
  • Jupke, J. F., & Schäfer, R. B. (2020). Should ecologists prefer model- over distance-based multivariate methods? Ecology and Evolution, 10(5), 2417–2435. https://doi.org/10.1002/ece3.6059
  • Jurburg, S. D., Keil, P., Singh, B. K., & Chase, J. M. (2021). All together now: limitations and recommendations for the simultaneous analysis of all eukaryotic soil sequences. Molecular Ecology Resources, 21(6), 1759–1771. https://doi.org/10.1111/1755-0998.13401
  • Katoh, K., & Standley, D. M. (2013). mafft - Multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30(4), 772–780. https://doi. org/10.1093/molbev/mst010
  • Kindt, R., & Coe, R. (2005). Tree diversity analysis. A manual and software for common statistical methods for ecological and biodiversity studies. World Agroforestry Centre (ICRAF). Available at https://www. worldagroforestry.org/output/tree-diversity-analysis
  • Legendre, P., & Anderson, M. J. (1999). Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments. Ecological Monographs, 69(1), 1–24. https://doi. org/10.1890/0012-9615(1999)069<0001:DBRATM>2.0.CO;2
  • Legendre, P., & De Caceres, M. (2013). Beta diversity as the variance of community data: dissimilarity coefficients and partitioning. Ecology Letters, 16(8), 951–963. https://doi.org/10.1111/ele.12141
  • Leibold, M. A., Holyoak, M., Mouquet, N., Amarasekare, P., Chase, J. M., Hoopes, M. F., Holt, R. D., Shurin, J. B., Law, R., Tilman, D., Loreau, M., & Gonzalez, A. (2004). The metacommunity concept: a framework for multi-scale community ecology. Ecology Letters, 7(7), 601– 613. https://doi.org/10.1111/j.1461-0248.2004.00608.x
  • Leingärtner, A., Krauss, J., & Steffan-Dewenter, I. (2014). Species richness and trait composition of butterfly assemblages change along an altitudinal gradient. Oecologia, 175(2), 613–623. https://doi. org/10.1007/s00442-014-2917-7
  • Lindo, Z., & Winchester, N. N. (2009). Spatial and environmental factors contributing to patterns in arboreal and terrestrial oribatid mite diversity across spatial scales. Oecologia, 160(4), 817–825. https:// doi.org/10.1007/s00442-009-1348-3
  • Liu, C., Dudley, K. L., Xu, Z.-H., & Economo, E. P. (2018). Mountain metacommunities: climate and spatial connectivity shape ant diversity in a complex landscape. Ecography, 41(1), 101–112. https://doi. org/10.1111/ecog.03067
  • Logue, J. B., Mouquet, N., Peter, H., & Hillebrand, H. (2011). Empirical approaches to metacommunities: a review and comparison with theory. Trends in Ecology and Evolution, 26(9), 482–491. https://doi. org/10.1016/j.tree.2011.04.009
  • Lopez, J. V., Yuhki, N., Masuda, R., Modi, W., & O'Brien, S. J. (1994). NUMT, a recent transfer and tandem amplification of mitochondrialDNA to the nuclear genome of the domestic cat. Journal of Molecular Evolution, 39(2), 174–190. https://doi.org/10.1007/ BF00163806
  • Marrec, R., Le Roux, V., Martin, L., Lenoir, J., Brunet, J., Cousins, S. A. O., De Smedt, P., Deconchat, M., Diekmann, M., Ehrmann, S., GalletMoron, E., Giffard, B., Liira, J., Lindgren, J., Valdes, A., Verheyen, K., Wulf, M., & Decocq, G. (2021). Multiscale drivers of carabid beetle (Coleoptera: Carabidae) assemblages in small European woodlandsGlobal Ecology and Biogeography, 30(1), 165–182. https://doi. org/10.1111/geb.13208
  • Martin, G. K., Beisner, B. E., Chain, F. J. J., Cristescu, M. E., del Giorgio, P. A., & Derry, A. M. (2021). Freshwater zooplankton metapopulations and metacommunities respond differently to environmental and spatial variation. Ecology, 102(1), e03224. https://doi.org/10.1002/ ecy.3224
  • Martin, M. (2011). cutadapt removes adapter sequences from highthroughput sequencing reads. EMBnet.journal, 17, 10–12. https:// doi.org/10.14806/ej.17.1.200
  • Martinez Arbizu, P. (2020). pairwiseAdonis: pairwise multilevel comparison using adonis. r package version 0.4. Available at: https://github. com/pmartinezarbizu/pairwiseAdonis
  • McRae, B. H. (2006). Isolation by resistance. Evolution, 60(8), 1551–1561. https://doi.org/10.1111/j.0014-3820.2006.tb00500.x
  • McRae, B. H., & Beier, P. (2007). Circuit theory predicts gene flow in plant and animal populations. Proceedings of the National Academy of Sciences of the United States of America, 104(50), 19885–19890. https://doi.org/10.1073/pnas.0706568104
  • McRae, B. H., Dickson, B. G., Keitt, T. H., & Shah, V. B. (2008). Using circuit theory to model connectivity in ecology, evolution, and conservation. Ecology, 89(10), 2712–2724. https://doi. org/10.1890/07-1861.1
  • Medail, F., & Quezel, P. (1997). Hot-spots analysis for conservation of plant biodiversity in the Mediterranean basin. Annals of the Missouri Botanical Garden, 84(1), 112–127. https://doi.org/10.2307/2399957
  • Meynard, C. N., Lavergne, S., Boulangeat, I., Garraud, L., Van Es, J., Mouquet, N., & Thuiller, W. (2013). Disentangling the drivers of metacommunity structure across spatial scales. Journal of Biogeography, 40(8), 1560–1571. https://doi.org/10.1111/jbi.12116
  • Nekola, J. C., & White, P. S. (1999). The distance decay of similarity in biogeography and ecology. Journal of Biogeography, 26(4), 867–878. https://doi.org/10.1046/j.1365-2699.1999.00305.x
  • Nielsen, U. (2019). Soil fauna assemblages: global to local scales (Ecology, Biodiversity and Conservation). Cambridge University Press.
  • Oksanen, J., Blanchet, F. G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D. & Wagner, H. (2020). vegan: community ecology package. r package version 2.5-7. Available at https://CRAN.R-project.org/packa ge=vegan
  • Ortego, J., Gugger, P. F., & Sork, V. L. (2015). Climatically stable landscapes predict patterns of genetic structure and admixture in the Californian canyon live oak. Journal of Biogeography, 42(2), 328– 338. https://doi.org/10.1111/jbi.12419
  • Overcast, I., Emerson, B. C., & Hickerson, M. J. (2019). An integrated model of population genetics and community ecology. Journal of Biogeography, 46(4), 816–829. https://doi.org/10.1111/jbi.13541
  • Overcast, I., Ruffley, M., Rosindell, J., Harmon, L., Borges, P. A. V., Emerson, B. C., Etienne, R. S., Gillespie, R., Krehenwinkel, H., Mahler, D. L., Massol, F., Parent, C. E., Patiño, J., Peter, B., Week, B., Wagner, C., Hickerson, M. J., & Rominger, A. (2021). A unified model of species abundance, genetic diversity, and functional diversity reveals the mechanisms structuring ecological communities. Molecular Ecology Resources, 21(8), 2782–2800. https://doi. org/10.1111/1755-0998.13514
  • Papadopoulou, A., Anastasiou, I., Spagopoulou, F., Stalimerou, M., Terzopoulou, S., Legakis, A., & Vogler, A. P. (2011). Testing the species–genetic diversity correlation in the Aegean Archipelago: toward a haplotype-based macroecology? The American Naturalist, 178(2), 241–255. https://doi.org/10.1086/660828
  • Paradis, E., & Schliep, K. (2019). ape 5.0: an environment for modern phylogenetics and evolutionary analyses in r. Bioinformatics, 35(3), 526–528. https://doi.org/10.1093/bioinformatics/bty633
  • Peres-Neto, P. R., & Jackson, D. A. (2001). How well do multivariate data sets match? The advantages of a Procrustean superimposition approach over the Mantel test. Oecologia, 129(2), 169–178. https:// doi.org/10.1007/s004420100720
  • Peters, M. K., Hemp, A., Appelhans, T., Behler, C., Classen, A., Detsch, F., Ensslin, A., Ferger, S. W., Frederiksen, S. B., Gebert, F., Haas, M., Helbig-Bonitz, M., Hemp, C., Kindeketa, W. J., Mwangomo, E., Ngereza, C., Otte, I., Röder, J., Rutten, G., … Steffan-Dewenter, I. (2016). Predictors of elevational biodiversity gradients change from single taxa to the multi-taxa community level. Nature Communications, 7, 13736. https://doi.org/10.1038/ncomms13736
  • Porter, T. M., & Hajibabaei, M. (2020). Putting COI metabarcoding in context: the utility of exact sequence variants (ESVs) in biodiversity analysis. Frontiers in Ecology and Evolution, 8, 248. https://doi. org/10.3389/fevo.2020.00248
  • R Core Team (2020). r: a language and environment for statistical computing. R Foundation for Statistical Computing. https://www.r-proje ct.org/
  • Rahbek, C. (1995). The elevational gradient of species richness - a uniform pattern. Ecography, 18(2), 200–205. https://doi.org/10.1111/ j.1600-0587.1995.tb00341.x
  • Rahbek, C., Borregaard, M. K., Colwell, R. K., Dalsgaard, B. O., Holt, B. G., Morueta-Holme, N., Nogues-Bravo, D., Whittaker, R. J., & Fjeldså, J. (2019). Humboldt's enigma: what causes global patterns of mountain biodiversity? Science, 365(6458), 1108–1113. https:// doi.org/10.1126/science.aax0149
  • Reisch, C., & Schmid, C. (2019). Species and genetic diversity are not congruent in fragmented dry grasslands. Ecology and Evolution, 9(1), 664–671. https://doi.org/10.1002/ece3.4791
  • Resasco, J., & Fletcher, R. J. (2021). Accounting for connectivity alters the apparent roles of spatial and environmental processes on metacommunity assembly. Landscape Ecology, 36(4), 1089–1099. https:// doi.org/10.1007/s10980-021-01203-z
  • Rognes, T., Flouri, T., Nichols, B., Quince, C., & Mahe, F. (2016). vsearch: a versatile open source tool for metagenomics. PeerJ, 4, e2584. https://doi.org/10.7717/peerj.2584
  • Rota, N., Canedoli, C., Ferre, C., Ficetola, G. F., Guerrieri, A., & PadoaSchioppa, E. (2020). Evaluation of soil biodiversity in alpine habitats through eDNA metabarcoding and relationships with environmental features. Forests, 11(7), 738. https://doi.org/10.3390/f1107 0738
  • Schliep, K. P. (2011). phangorn: phylogenetic analysis in r. Bioinformatics, 27(4), 592–593. https://doi.org/10.1093/bioinformatics/btq706
  • Schuppenhauer, M. M., Lehmitz, R., & Xylander, W. E. R. (2019). Slowmoving soil organisms on a water highway: aquatic dispersal and survival potential of Oribatida and Collembola in running water. Movement Ecology, 7, 20. https://doi.org/10.1186/s4046 2-019-0165-5
  • Shokralla, S., Porter, T. M., Gibson, J. F., Dobosz, R., Janzen, D. H., Hallwachs, W., Golding, G. B., & Hajibabaei, M. (2015). Massively parallel multiplex DNA sequencing for specimen identification using an Illumina MiSeq platform. Scientific Reports, 5, 9687. https:// doi.org/10.1038/srep09687
  • Soininen, J. (2014). A quantitative analysis of species sorting across organisms and ecosystems. Ecology, 95(12), 3284–3292. https://doi. org/10.1890/13-2228.1
  • Steinbauer, M. J., Grytnes, J.-A., Jurasinski, G., Kulonen, A., Lenoir, J., Pauli, H., Rixen, C., Winkler, M., Bardy-Durchhalter, M., Barni, E., Bjorkman, A. D., Breiner, F. T., Burg, S., Czortek, P., Dawes, M. A., Delimat, A., Dullinger, S., Erschbamer, B., Felde, V. A., … Wipf, S. (2018). Accelerated increase in plant species richness on mountain summits is linked to warming. Nature, 556(7700), 231–234. https:// doi.org/10.1038/s41586-018-0005-6
  • Thakur, M. P., Phillips, H. R. P., Brose, U., De Vries, F. T., Lavelle, P., Loreau, M., Mathieu, J., Mulder, C., Van der Putten, W. H., Rillig, M. C., Wardle, D. A., Bach, E. M., Bartz, M. L. C., Bennett, J. M., Briones, M. J. I., Brown, G., Decaëns, T., Eisenhauer, N., Ferlian, O., … Cameron, E. K. (2020). Towards an integrative understanding of soil biodiversity. Biological Reviews, 95(2), 350–364. https://doi. org/10.1111/brv.12567
  • Title, P. O., & Bemmels, J. B. (2018). ENVIREM: an expanded set of bioclimatic and topographic variables increases flexibility and improves performance of ecological niche modeling. Ecography, 41(2), 291– 307. https://doi.org/10.1111/ecog.02880
  • Tonkin, J. D., Altermatt, F., Finn, D. S., Heino, J., Olden, J. D., Pauls, S. U., & Lytle, D. A. (2018). The role of dispersal in river network metacommunities: patterns, processes, and pathways. Freshwater Biology, 63(1), 141–163. https://doi.org/10.1111/fwb.13037
  • Tonkin, J. D., Shah, R. D. T., Shah, D. N., Hoppeler, F., Jaehnig, S. C., & Pauls, S. U. (2017). Metacommunity structuring in Himalayan streams over large elevational gradients: the role of dispersal routes and niche characteristics. Journal of Biogeography, 44(1), 62– 74. https://doi.org/10.1111/jbi.12895
  • Tonkin, J. D., Stoll, S., Jähnig, S. C., & Haase, P. (2016). Contrasting metacommunity structure and beta diversity in an aquatic-floodplain system. Oikos, 125(5), 686–697. https://doi.org/10.1111/oik.02717
  • Türke, M., Lange, M., & Eisenhauer, N. (2018). Gut shuttle service: endozoochory of dispersal-limited soil fauna by gastropods. Oecologia, 186(3), 655–664. https://doi.org/10.1007/s0044 2-018-4058-x
  • Vellend, M. (2010). Conceptual synthesis in community ecology. Quarterly Review of Biology, 85(2), 183–206. https://doi.org/10.1086/652373
  • Vellend, M., Srivastava, D. S., Anderson, K. M., Brown, C. D., Jankowski, J. E., Kleynhans, E. J., Kraft, N. J. B., Letaw, A. D., Macdonald, A. A. M., Maclean, J. E., Myers-Smith, I. H., Norris, A. R., & Xue, X. (2014). Assessing the relative importance of neutral stochasticity in ecological communities. Oikos, 123(12), 1420–1430. https://doi. org/10.1111/oik.01493
  • Viana, D. S., & Chase, J. M. (2019). Spatial scale modulates the inference of metacommunity assembly processes. Ecology, 100(2), e02576. https://doi.org/10.1002/ecy.2576
  • Vittinghoff, E., Glidden, D. V., Shiboski, S. C., & McCulloch, C. E. (2012). Regression methods in biostatistics: linear, logistic, survival, and repeated measures models, 2nd ed. Springer-Verlag.
  • Vogiatzakis, I. N., Mannion, A. M., & Sarris, D. (2016). Mediterranean island biodiversity and climate change: the last 10,000 years and the future. Biodiversity and Conservation, 25(13), 2597–2627. https:// doi.org/10.1007/s10531-016-1204-9
  • Walsh, C., & Mac Nally, R. (2003). hier.part: hierarchical partitioning. r package version 1.0-6. Available at https://CRAN.R-project.org/ package=hier.part
  • Wang, I. J. (2013). Examining the full effects of landscape heterogeneity on spatial genetic variation: a multiple matrix regression approach for quantifying geographic and ecological isolation. Evolution, 67(12), 3403–3411. https://doi.org/10.1111/evo.12134
  • Wang, I. J. (2020). Topographic path analysis for modelling dispersal and functional connectivity: calculating topographic distances using the topoDistance r package. Methods in Ecology and Evolution, 11(2), 265–272. https://doi.org/10.1111/2041-210x.13317
  • Wang, J., Legendre, P., Soininen, J., Yeh, C.-F., Graham, E., Stegen, J., Casamayor, E. O., Zhou, J., Shen, J. I., & Pan, F. (2020). Temperature drives local contributions to beta diversity in mountain streams: stochastic and deterministic processes. Global Ecology and Biogeography, 29(3), 420–432. https://doi.org/10.1111/geb.13035
  • Wang, Y., Naumann, U., Wright, S. T., & Warton, D. I. (2012). mvabund - an r package for model-based analysis of multivariate abundance data. Methods in Ecology and Evolution, 3(3), 471–474. https://doi. org/10.1111/j.2041-210X.2012.00190.x
  • Watling, J. I., Nowakowski, A. J., Donnelly, M. A., & Orrock, J. L. (2011). Meta-analysis reveals the importance of matrix composition for animals in fragmented habitat. Global Ecology and Biogeography, 20(2), 209–217. https://doi.org/10.1111/j.1466-8238.2010.00586.x
  • Young, M. R., Proctor, H. C., deWaard, J. R., & Hebert, P. D. N. (2019). DNA barcodes expose unexpected diversity in Canadian mites. Molecular Ecology, 28(24), 5347–5359. https://doi.org/10.1111/ mec.15292
  • Yu, D. W., Ji, Y., Emerson, B. C., Wang, X., Ye, C., Yang, C., & Ding, Z. (2012). Biodiversity soup: metabarcoding of arthropods for rapid biodiversity assessment and biomonitoring. Methods in Ecology and Evolution, 3(4), 613–623. https://doi.org/10.1111/j.2041-210X.2012.00198.x
  • Zhang, J., Kobert, K., Flouri, T., & Stamatakis, A. (2014). pear: a fast and accurate Illumina Paired-End reAd mergeR. Bioinformatics, 30(5), 614–620. https://doi.org/10.1093/bioinformatics/btt593
  • Zinger, L., Taberlet, P., Schimann, H., Bonin, A., Boyer, F., De Barba, M., Gaucher, P., Gielly, L., Giguet-Covex, C., Iribar, A., Réjou-Méchain, M., Rayé, G., Rioux, D., Schilling, V., Tymen, B., Viers, J., Zouiten, C., Thuiller, W., Coissac, E., & Chave, J. (2019). Body size determines soil community assembly in a tropical forest. Molecular Ecology, 28(3), 528–543. https://doi.org/10.1111/mec.14919
  • Zizka, V. M. A., Weiss, M., & Leese, F. (2020). Can metabarcoding resolve intraspecific genetic diversity changes to environmental stressors? A test case using river macrozoobenthos. Metabarcoding & Metagenomics, 4, 23–34. https://doi.org/10.3897/ mbmg.4.51925