More stories

  • in

    Crystalline iron oxides stimulate methanogenic benzoate degradation in marine sediment-derived enrichment cultures

    1.
    Arndt S, Jørgensen BB, LaRowe DE, Middelburg J, Pancost R, Regnier P. Quantifying the degradation of organic matter in marine sediments: a review and synthesis. Earth Sci Rev. 2013;123:53–86.
    CAS  Article  Google Scholar 
    2.
    Froelich PN, Klinkhammer GP, Bender ML, Luedtke NA, Heath GR, Cullen D, et al. Early oxidation of organic matter in pelagic sediments of the eastern equatorial Atlantic: suboxic diagenesis. Geochim Cosmochim Acta. 1979;43:1075–90.
    CAS  Article  Google Scholar 

    3.
    Calvert S. Oceanographic controls on the accumulation of organic matter in marine sediments. Geol Soc Spec Publ. 1987;26:137–51.
    Article  Google Scholar 

    4.
    De Leeuw J, Largeau C. A review of macromolecular organic compounds that comprise living organisms and their role in kerogen, coal, and petroleum formation. Org Geochem. 1993;11:23–72.

    5.
    Mackenzie FT, Lerman A, Andersson AJ. Past and present of sediment and carbon biogeochemical cycling models. Biogeosciences. 2004;1:11–32.
    CAS  Article  Google Scholar 

    6.
    Oni OE, Miyatake T, Kasten S, Richter-Heitmann T, Fischer D, Wagenknecht L, et al. Distinct microbial populations are tightly linked to the profile of dissolved iron in the methanic sediments of the Helgoland Mud Area, North Sea. Front Microbiol. 2015;6:365.
    PubMed Central  PubMed  Google Scholar 

    7.
    Egger M, Hagens M, Sapart CJ, Dijkstra N, van Helmond NA, Mogollón JM, et al. Iron oxide reduction in methane-rich deep Baltic Sea sediments. Geochim Cosmochim Acta. 2017;207:256–76.
    CAS  Article  Google Scholar 

    8.
    Riedinger N, Pfeifer K, Kasten S, Garming JFL, Vogt C, Hensen C. Diagenetic alteration of magnetic signals by anaerobic oxidation of methane related to a change in sedimentation rate. Geochim Cosmoch Acta. 2005;69:4117–26.
    CAS  Article  Google Scholar 

    9.
    Riedinger N, Formolo MJ, Lyons TW, Henkel S, Beck A, Kasten S. An inorganic geochemical argument for coupled anaerobic oxidation of methane and iron reduction in marine sediments. Geobiology. 2014;12:172–81.
    CAS  Article  Google Scholar 

    10.
    März C, Hoffmann J, Bleil U, De Lange G, Kasten S. Diagenetic changes of magnetic and geochemical signals by anaerobic methane oxidation in sediments of the Zambezi deep-sea fan (SW Indian Ocean). Mar Geol. 2008;255:118–30.
    Article  CAS  Google Scholar 

    11.
    Hensen C, Zabel M, Pfeifer K, Schwenk T, Kasten S, Riedinger N, et al. Control of sulfate pore-water profiles by sedimentary events and the significance of anaerobic oxidation of methane for the burial of sulfur in marine sediments. Geochim Cosmochim Acta. 2003;67:2631–47.
    CAS  Article  Google Scholar 

    12.
    Flood RD, Piper DJW, Klaus A, Party SS. Initial Reports. Proc. Ocean Drill. Progam. 1995;155. https://doi.org/10.2973/odp.proc.ir.155.1995.

    13.
    Kasten S, Freudenthal T, Gingele FX, Schulz HD. Simultaneous formation of iron-rich layers at different redox boundaries in sediments of the Amazon deep-sea fan. Geochim Cosmochim Acta. 1998;62:2253–64.
    CAS  Article  Google Scholar 

    14.
    Meyers SR. Production and preservation of organic matter: the significance of iron. Paleoceanography. 2007;22:PA4211.

    15.
    Barber A, Brandes J, Leri A, Lalonde K, Balind K, Wirick S, et al. Preservation of organic matter in marine sediments by inner-sphere interactions with reactive iron. Sci Rep. 2017;7:1–10.
    CAS  Article  Google Scholar 

    16.
    Lalonde K, Mucci A, Ouellet A, Gélinas Y. Preservation of organic matter in sediments promoted by iron. Nature. 2012;483:198–200.
    CAS  Article  Google Scholar 

    17.
    Middelburg JJ. A simple rate model for organic matter decomposition in marine sediments. Geochim Cosmochim Acta. 1989;53:1577–81.
    CAS  Article  Google Scholar 

    18.
    Biddle JF, Lipp JS, Lever MA, Lloyd KG, Sørensen KB, Anderson R, et al. Heterotrophic Archaea dominate sedimentary subsurface ecosystems off Peru. Proc Natl Acad Sci USA. 2006;103:3846–51.
    CAS  Article  Google Scholar 

    19.
    Aromokeye DA, Kulkarni AC, Elvert M, Wegener G, Henkel S, Coffinet S, et al. Rates and microbial players of iron-driven anaerobic oxidation of methane in methanic marine sediments. Front Microbiol. 2020;10:3041.
    PubMed Central  Article  PubMed  Google Scholar 

    20.
    Lovley DR, Phillips EJ. Organic matter mineralization with reduction of ferric iron in anaerobic sediments. Appl Environ Microbiol. 1986;51:683–9.
    CAS  PubMed Central  Article  PubMed  Google Scholar 

    21.
    Lovley DR, Coates JD, Blunt-Harris EL, Phillips EJ, Woodward JC. Humic substances as electron acceptors for microbial respiration. Nature. 1996;382:445–8.
    CAS  Article  Google Scholar 

    22.
    Lovley D. Dissimilatory Fe (III)-and Mn (IV)-reducing prokaryotes, In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The Prokaryotes. Springer: Berlin Heidelberg; 2006, Vol. 2, p. 635–58.

    23.
    Lovley DR, Phillips EJ. Novel mode of microbial energy metabolism: organic carbon oxidation coupled to dissimilatory reduction of iron or manganese. Appl Environ Microbiol. 1988;54:1472–80.
    CAS  PubMed Central  Article  PubMed  Google Scholar 

    24.
    Kato S, Hashimoto K, Watanabe K. Methanogenesis facilitated by electric syntrophy via (semi) conductive iron‐oxide minerals. Environ Microbiol. 2012;14:1646–54.
    CAS  Article  Google Scholar 

    25.
    Jiang S, Park S, Yoon Y, Lee J-H, Wu W-M, Phuoc Dan N, et al. Methanogenesis facilitated by geobiochemical iron cycle in a novel syntrophic methanogenic microbial community. Environ Sci Technol. 2013;47:10078–84.
    CAS  Article  Google Scholar 

    26.
    Aromokeye DA, Richter-Heitmann T, Oni O, Emmanuel, Kulkarni A, Yin X, et al. Temperature controls crystalline iron oxide utilization by microbial communities in methanic ferruginous marine sediment incubations. Front Microbiol. 2018;9:2574.
    PubMed Central  Article  PubMed  Google Scholar 

    27.
    Zhuang L, Tang J, Wang Y, Hu M, Zhou S. Conductive iron oxide minerals accelerate syntrophic cooperation in methanogenic benzoate degradation. J Hazard Mater. 2015;293:37–45.
    CAS  Article  Google Scholar 

    28.
    Hebbeln D, Scheurle C, Lamy F. Depositional history of the Helgoland Mud Area, German Bight, North Sea. Geo Mar Lett. 2003;23:81–90.
    Article  Google Scholar 

    29.
    Oni OE, Schmidt F, Miyatake T, Kasten S, Witt M, Hinrichs K-U, et al. Microbial communities and organic matter composition in surface and subsurface sediments of the Helgoland Mud Area, North Sea. Front Microbiol. 2015;6:1290.
    PubMed Central  PubMed  Google Scholar 

    30.
    Gan S, Schmidt F, Heuer VB, Goldhammer T, Witt M, Hinrichs K-U. Impacts of redox conditions on dissolved organic matter (DOM) quality in marine sediments off the River Rhône, Western Mediterranean Sea. Geochim Cosmochim Acta. 2020;276:151–69.
    CAS  Article  Google Scholar 

    31.
    Carmona M, Zamarro MT, Blázquez B, Durante-Rodríguez G, Juárez JF, Valderrama JA, et al. Anaerobic catabolism of aromatic compounds: a genetic and genomic view. Microbiol Mol Biol Rev. 2009;73:71–133.
    CAS  PubMed Central  Article  PubMed  Google Scholar 

    32.
    Fuchs G, Boll M, Heider J. Microbial degradation of aromatic compounds—from one strategy to four. Nat Rev Microbiol. 2011;9:803–16.
    CAS  Article  Google Scholar 

    33.
    Gibson J, Harwood SC. Metabolic diversity in aromatic compound utilization by anaerobic microbes. Annu Rev Microbiol. 2002;56:345–69.
    CAS  Article  Google Scholar 

    34.
    Hopkins BT, McInerney MJ, Warikoo V. Evidence for anaerobic syntrophic benzoate degradation threshold and isolation of the syntrophic benzoate degrader. Appl Environ Microbiol. 1995;61:526.
    CAS  PubMed Central  Article  PubMed  Google Scholar 

    35.
    Schink B. Energetics of syntrophic cooperation in methanogenic degradation. Microbiol Mol Biol Rev. 1997;61:262–80.
    CAS  PubMed Central  Article  PubMed  Google Scholar 

    36.
    Schöcke L, Schink B. Energetics of methanogenic benzoate degradation by Syntrophus gentianae in syntrophic coculture. Microbiology. 1997;143:2345–51.
    Article  Google Scholar 

    37.
    Widdel F, Kohring G-W, Mayer F. Studies on dissimilatory sulfate-reducing bacteria that decompose fatty acids III. Characterization of the filamentous gliding Desulfonema limicola gen. nov. sp. nov., and Desulfonema magnum sp. nov. Arch Microbiol. 1983;134:286–94.
    CAS  Article  Google Scholar 

    38.
    Widdel F. Anaerober Abbau von Fettsäuren und Benzoesäure durch neu isolierte Arten sulfat-reduzierender Bakterien [PhD Thesis]. Göttingen, Germany: Georg-August-Universität zu Göttingen; 1980.

    39.
    Widdel F, Pfennig N. Studies on dissimilatory sulfate-reducing bacteria that decompose fatty acids. Arch Microbiol. 1981;129:395–400.
    CAS  Article  Google Scholar 

    40.
    Viollier E, Inglett P, Hunter K, Roychoudhury A, Van, Cappellen P. The ferrozine method revisited: Fe(II)/Fe(III) determination in natural waters. Appl Geochem. 2000;15:785–90.
    CAS  Article  Google Scholar 

    41.
    Heuer VB, Pohlman JW, Torres ME, Elvert M, Hinrichs K-U. The stable carbon isotope biogeochemistry of acetate and other dissolved carbon species in deep subseafloor sediments at the northern Cascadia Margin. Geochim Cosmochim Acta. 2009;73:3323–36.
    CAS  Article  Google Scholar 

    42.
    Lin Y-S, Heuer VB, Goldhammer T, Kellermann MY, Zabel M, Hinrichs K-U. Towards constraining H2 concentration in subseafloor sediment: a proposal for combined analysis by two distinct approaches. Geochim Cosmochim Acta. 2012;77:186–201.
    CAS  Article  Google Scholar 

    43.
    Lueders T, Manefield M, Friedrich MW. Enhanced sensitivity of DNA‐and rRNA‐based stable isotope probing by fractionation and quantitative analysis of isopycnic centrifugation gradients. Environ Microbiol. 2004;6:73–8.
    CAS  Article  Google Scholar 

    44.
    Amann R, Fuchs BM, Behrens S. The identification of microorganisms by fluorescence in situ hybridisation. Curr Opin Biotechnol. 2001;12:231–6.
    CAS  Article  Google Scholar 

    45.
    Poulton SW, Krom MD, Raiswell R. A revised scheme for the reactivity of iron (oxyhydr)oxide minerals towards dissolved sulfide. Geochim Cosmochim Acta. 2004;68:3703–15.
    CAS  Article  Google Scholar 

    46.
    Herndon EM, Yang Z, Bargar J, Janot N, Regier TZ, Graham DE, et al. Geochemical drivers of organic matter decomposition in arctic tundra soils. Biogeochemistry. 2015;126:397–414.
    CAS  Article  Google Scholar 

    47.
    Yang Z, Wullschleger SD, Liang L, Graham DE, Gu B. Effects of warming on the degradation and production of low-molecular-weight labile organic carbon in an Arctic tundra soil. Soil Biol Biochem. 2016;95:202–11.
    CAS  Article  Google Scholar 

    48.
    Yang Z, Shi X, Wang C, Wang L, Guo R. Magnetite nanoparticles facilitate methane production from ethanol via acting as electron acceptors. Sci Rep. 2015;5;16118. https://doi.org/10.1038/srep16118.

    49.
    McInerney MJ, Struchtemeyer CG, Sieber J, Mouttaki H, Stams AJ, Schink B, et al. Physiology, ecology, phylogeny, and genomics of microorganisms capable of syntrophic metabolism. Ann N Y Acad Sci. 2008;1125:58–72.
    CAS  Article  Google Scholar 

    50.
    Sieber J, McInerney M, Plugge C, Schink B, Gunsalus R. Methanogenesis: syntrophic metabolism. In: Timmis KN (ed), Handbook of hydrocarbon and lipid microbiology. Springer: Berlin, Heidelberg; 2010. p. 337–55.

    51.
    Vandieken V, Mußmann M, Niemann H, Jørgensen BB. Desulfuromonas svalbardensis sp. nov. and Desulfuromusa ferrireducens sp. nov., psychrophilic, Fe(III)-reducing bacteria isolated from Arctic sediments, Svalbard. Int J Syst Evol Microbiol. 2006;56:1133–9.
    CAS  Article  Google Scholar 

    52.
    Jones DL, Edwards AC. Influence of sorption on the biological utilization of two simple carbon substrates. Soil Biol Biochem. 1998;30:1895–902.
    CAS  Article  Google Scholar 

    53.
    Bray MS, Wu J, Reed BC, Kretz CB, Belli KM, Simister RL, et al. Shifting microbial communities sustain multiyear iron reduction and methanogenesis in ferruginous sediment incubations. Geobiology. 2017;15:678–89.
    CAS  Article  Google Scholar 

    54.
    Dolfing J, Tiedje JM. Acetate inhibition of methanogenic, syntrophic benzoate degradation. Appl Environ Microbiol. 1988;54:1871–3.
    CAS  PubMed Central  Article  PubMed  Google Scholar 

    55.
    Warikoo V, McInerney MJ, Robinson JA, Suflita JM. Interspecies acetate transfer influences the extent of anaerobic benzoate degradation by syntrophic consortia. Appl Environ Microbiol. 1996;62:26–32.
    CAS  PubMed Central  Article  PubMed  Google Scholar 

    56.
    Elshahed MS, McInerney MJ. Benzoate Fermentation by the anaerobic bacterium Syntrophus aciditrophicus in the absence of hydrogen-using microorganisms. Appl Environ Microbiol. 2001;67:5520–5.
    CAS  PubMed Central  Article  PubMed  Google Scholar 

    57.
    Watanabe M, Kojima H, Fukui M. Review of Desulfotomaculum species and proposal of the genera Desulfallas gen. nov., Desulfofundulus gen. nov., Desulfofarcimen gen. nov. and Desulfohalotomaculum gen. nov. Int J Syst Evol Microbiol. 2018;68:2891–9.
    CAS  Article  Google Scholar 

    58.
    Harwood CS, Burchhardt G, Herrmann H, Fuchs G. Anaerobic metabolism of aromatic compounds via the benzoyl-CoA pathway. FEMS Microbiol Rev. 1998;22:439–58.
    CAS  Article  Google Scholar 

    59.
    Rabus R, Boll M, Heider J, Meckenstock RU, Buckel W, Einsle O, et al. Anaerobic microbial degradation of hydrocarbons: from enzymatic reactions to the environment. J Mol Microbiol Biotechnol. 2016;26:5–28.
    CAS  Google Scholar 

    60.
    Podosokorskaya OA, Kadnikov VV, Gavrilov SN, Mardanov AV, Merkel AY, Karnachuk OV, et al. Characterization of Melioribacter roseus gen. nov., sp. nov., a novel facultatively anaerobic thermophilic cellulolytic bacterium from the class Ignavibacteria, and a proposal of a novel bacterial phylum Ignavibacteriae. Environ Microbiol. 2013;15:1759–71.
    CAS  Article  Google Scholar 

    61.
    Kadnikov VV, Mardanov AV, Podosokorskaya OA, Gavrilov SN, Kublanov IV, Beletsky AV, et al. Genomic analysis of Melioribacter roseus, facultatively anaerobic organotrophic bacterium representing a novel deep lineage within Bacteriodetes/Chlorobi group. PLoS ONE 8:e53047. https://doi.org/10.1371/journal.pone.0053047.

    62.
    Zavarzina DG, Sokolova TG, Tourova TP, Chernyh NA, Kostrikina NA, Bonch-Osmolovskaya EA. Thermincola ferriacetica sp. nov., a new anaerobic, thermophilic, facultatively chemolithoautotrophic bacterium capable of dissimilatory Fe(III) reduction. Extremophiles. 2007;11:1–7.
    CAS  Article  Google Scholar 

    63.
    Wrighton KC, Agbo P, Warnecke F, Weber KA, Brodie EL, DeSantis TZ, et al. A novel ecological role of the Firmicutes identified in thermophilic microbial fuel cells. ISME J. 2008;2:1146–56.
    CAS  Article  Google Scholar 

    64.
    Byrne-Bailey KG, Wrighton KC, Melnyk RA, Agbo P, Hazen TC, Coates JD. Complete genome sequence of the electricity-producing “Thermincola potens” strain JR. J Bacteriol. 2010;192:4078–9.
    CAS  PubMed Central  Article  PubMed  Google Scholar 

    65.
    Wrighton KC. Following electron flow: from a gram-positive community to mechanisms of electron transfer. Berkeley, CA, USA: UC Berkeley; 2010.

    66.
    Poser A, Lohmayer R, Vogt C, Knoeller K, Planer-Friedrich B, Sorokin D, et al. Disproportionation of elemental sulfur by haloalkaliphilic bacteria from soda lakes. Extremophiles. 2013;17:1003–12.
    CAS  Article  Google Scholar 

    67.
    Sorokin DY, Tourova TP, Mußmann M, Muyzer G. Dethiobacter alkaliphilus gen. nov. sp. nov., and Desulfurivibrio alkaliphilus gen. nov. sp. nov.: two novel representatives of reductive sulfur cycle from soda lakes. Extremophiles. 2008;12:431–9.
    CAS  Article  Google Scholar 

    68.
    Zhuang L, Tang Z, Ma J, Yu Z, Wang Y, Tang J. Enhanced anaerobic biodegradation of benzoate under sulfate-reducing conditions with conductive iron-oxides in sediment of Pearl River Estuary. Front Microbiol. 2019;10:374.
    PubMed Central  Article  PubMed  Google Scholar 

    69.
    Kamagata Y, Kitagawa N, Tasaki M, Nakamura K, Mikami E. Degradation of benzoate by an anaerobic consortium and some properties of a hydrogenotrophic methanogen and sulfate-reducing bacterium in the consortium. J Ferment Bioeng. 1992;73:213–8.
    CAS  Article  Google Scholar 

    70.
    Junghare M, Schink B. Desulfoprunum benzoelyticum gen. nov., sp. nov., a gram-negative benzoate-degrading sulfate-reducing bacterium isolated from the wastewater treatment plant. Int J Syst Evol Microbiol. 2015;65:77–84.
    CAS  Article  Google Scholar 

    71.
    Oren A. The order Halanaerobiales, and the families Halanaerobiaceae and Halobacteroidaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F, editors. The prokaryotes: firmicutes and tenericutes. Berlin, Heidelberg: Springer Berlin Heidelberg; 2014. p. 153–77.

    72.
    Hatamoto M, Imachi H, Yashiro Y, Ohashi A, Harada H. Detection of active butyrate-degrading microorganisms in methanogenic sludges by RNA-based stable isotope probing. Appl Environ Microbiol. 2008;74:3610–4.
    CAS  PubMed Central  Article  PubMed  Google Scholar 

    73.
    Nobu MK, Narihiro T, Liu M, Kuroda K, Mei R, Liu WT. Thermodynamically diverse syntrophic aromatic compound catabolism. Environ Microbiol. 2017;19:4576–86.
    CAS  Article  Google Scholar 

    74.
    Lentini CJ, Wankel SD, Hansel CM. Enriched iron(III)-reducing bacterial communities are shaped by carbon substrate and iron oxide mineralogy. Front Microbiol. 2012;3:404.
    PubMed Central  Article  PubMed  Google Scholar 

    75.
    Newsome L, Lopez Adams R, Downie HF, Moore KL, Lloyd JR. NanoSIMS imaging of extracellular electron transport processes during microbial iron(III) reduction. FEMS Microbiol Ecol. 2018;94:fiy104.

    76.
    Wang H, Byrne JM, Liu P, Liu J, Dong X, Lu Y. Redox cycling of Fe(II) and Fe(III) in magnetite accelerates aceticlastic methanogenesis by Methanosarcina mazei. Environ Microbiol Rep. 2020;12:97–109.
    CAS  Article  Google Scholar 

    77.
    Dodsworth JA, Blainey PC, Murugapiran SK, Swingley WD, Ross CA, Tringe SG, et al. Single-cell and metagenomic analyses indicate a fermentative and saccharolytic lifestyle for members of the OP9 lineage. Nat Commun. 2013;4:1854.
    PubMed Central  Article  CAS  PubMed  Google Scholar 

    78.
    Nobu MK, Dodsworth JA, Murugapiran SK, Rinke C, Gies EA, Webster G, et al. Phylogeny and physiology of candidate phylum ‘Atribacteria’(OP9/JS1) inferred from cultivation-independent genomics. ISME J. 2016;10:273–86.
    CAS  Article  Google Scholar 

    79.
    Algora C, Vasileiadis S, Wasmund K, Trevisan M, Krüger M, Puglisi E, et al. Manganese and iron as structuring parameters of microbial communities in Arctic marine sediments from the Baffin Bay. FEMS Microbiol Ecol. 2015;91:fiv056.
    Article  CAS  PubMed  PubMed Central  Google Scholar 

    80.
    Lehours A-C, Rabiet M, Morel-Desrosiers N, Morel J-P, Jouve L, Arbeille B, et al. Ferric iron reduction by fermentative strain BS2 isolated from an iron-rich anoxic environment (Lake Pavin, France). Geomicrobiol J. 2010;27:714–22.
    CAS  Article  Google Scholar 

    81.
    Liu D, Wang H, Dong H, Qiu X, Dong X, Cravotta CA. Mineral transformations associated with goethite reduction by Methanosarcina barkeri. Chem Geol. 2011;288:53–60.
    CAS  Article  Google Scholar 

    82.
    Sivan O, Shusta S, Valentine D. Methanogens rapidly transition from methane production to iron reduction. Geobiology. 2016;14:190–203.
    CAS  Article  Google Scholar 

    83.
    Whitman WB, Coleman DC, Wiebe WJ. Prokaryotes: the unseen majority. Proc Nat Acad Sci USA. 1998;95:6578–83.
    CAS  Article  Google Scholar 

    84.
    Aromokeye AD. Iron oxide driven methanogenesis and methanotrophy in methanic sediments of Helgoland Mud Area, North Sea. Bremen, Germany: Universität Bremen; 2018. More

  • in

    Bryophytes are predicted to lag behind future climate change despite their high dispersal capacities

    The methodological framework for simulating the dispersal of bryophytes under changing climate conditions is presented in Fig. 4. A grid of pixel-specific environmental conditions and dispersal kernels, combining information on species dispersal traits, local wind conditions, as well as landscape features affecting dispersal by wind, is generated and used as input in simulations of species dispersal in the landscape under changing climate conditions.
    Fig. 4: Overview of workflow implemented in the present study to integrate mechanistic dispersal kernels and correlative climatic suitability models in simulations of future wind-dispersed species distributions under climate change.

    Species distribution data (left) are combined with climatic variables to produce climatic suitability models that are calibrated under present and projected under future climatic conditions (Part 1) and used to build mechanistic dispersal models (Part 2). The latter combine species intrinsic features (spore settling velocity Vt and release height Z0) and extrinsic environmental features (mean horizontal wind speed Ū and canopy height h) to generate maps of spatially explicit dispersal kernels. Climatic suitability and dispersal kernel maps, updated at regular intervals, are finally combined to parameterize simulations of dynamic range shifts under changing climatic conditions (Part 3).

    Full size image

    Data sampling
    The European bryophyte flora includes 1817 native or naturalized species41. Because information on bryophyte species distribution is scarce and very heterogeneous, challenging the application of climatic suitability models42, we selected 10 species based upon their representativeness for each of the four main biogeographic elements (i.e., groups of species sharing similar distribution patterns), namely the Arctic-Alpine, Atlantic, Mediterranean, and wide-temperate elements (Supplementary Table 2). For each of these species, we downloaded data from the Global Biodiversity Information Facility (https://www.gbif.org). We excluded data collected before 1960, which represented, on average, 41 ± 12% of the data available, for two reasons. First, old records often lack sufficiently precise location information. Second, we wanted to avoid a potential mismatch between old observations and current climate conditions used for modeling. To complete these data and generate a dataset across the entire range of each species in Europe, we specifically performed a thorough literature review to document their occurrence from more than 600 sources. Only points that were separated by at least 0.1° from each other were subsequently retained for modeling (“ecospat.occ.desaggregation” function in Ecospat 3.143) to avoid sampling bias and reduce the risk of spatial autocorrelation. Altogether, the number of observations available for each species ranged between 55 and 34,035 (database available from Figshare, https://doi.org/10.6084/m9.figshare.8289650).
    Average spore diameter was recorded for each species from Zanatta et al.44 and references therein. Species unknown to produce sporophytes were assigned a spore size of 150 µm to take dispersal through larger asexual propagules into account. Spore settling velocities Vt and release height (0.03, 1 and 10 m, which roughly correspond to habitat preferences for ground-dwelling, saxicolous, and epiphytic species, respectively) were determined for each species (Supplementary Table 2) following Zanatta et al.44.
    Nineteen bioclimatic variables, averaged over the period from 1970 to 2000, were retrieved from WorldClim 1.4 at a resolution of 30 arc-seconds45. Although snow is an important driver of species distributions in Arctic regions46, the lack of sufficiently detailed information on snow precipitation across Europe prevented us from implementing this variable.
    Given the spatial grain of our study, the hypothesis that some species will persist in small microhabitats, where temperatures can be cooler and humidity higher than in the surrounding environment, cannot be rejected. Data at finer scales for both present and future conditions would therefore be desirable47. Recently developed methods to generate fine-grained climatic data taking into account microclimatic effects modulated by microtopographic variation in the terrain, vegetation cover and ground properties using energy balance equations cannot, however, yet be implemented across large spatial scales48.
    For future climate conditions, a wide range of GCMs have been described and their variation represents the largest source of uncertainty in future range prediction studies49. No criterion exists to evaluate GCMs, whose performance may vary among regions and variables50. Due to computational constrains associated with our migration simulations (see below), we followed Didersky et al.51. and selected two GCMs that reflected the highest and lowest levels of predicted changes due to climate change for two angiosperm species in Europe50, namely MPI-ESM-LR52 and HadGem2-ES53. For each GCM, we analyzed two climate change scenarios. These scenarios are expressed by the representative concentration pathways (RCPs), using values comparing the level of radiative forcing between the preindustrial era and 2100. The moderate scenario RCP4.5 assumes 650 ppm CO2 and 1.0–2.6 °C increase by 2100, and refers to AR4 guideline scenario B1 of IPCC AR4 guidelines. The pessimistic scenario RCP8.5 assumes 1350 ppm CO2 and 2.6–4.8 °C increase by 2100, and refers to A1F1 scenario of IPCC AR4 guidelines54. Climatic data for each GCM and each RCP were averaged for each of the four time periods considered, i.e., 2010–2020, 2020–2030, 2030–2040 and 2040–2050.
    Monthly average and daily maximum wind speeds measured at 10 m as well as predicted wind speeds for the same ten-year time periods between 2010 and 2050, were computed from EURO-CORDEX (https://euro-cordex.net). Canopy height data were obtained from the global scale mapping of canopy height and biomass at a 1-km spatial resolution55. Wind speed and canopy height were sampled for each pixel and each time-slice to generate kernel maps through time (see below).
    Deriving climatic suitability maps
    The correlation among the 19 bioclimatic variables was computed from 50,000 random points. To avoid multicollinearity, five bioclimatic variables with a Pearson correlation value of R 10 km from a potential source could be colonized by LDD. The maximum LDD distance was set to unlimited based on phylogeographic evidence39. Following Robledo-Arnuncio et al.31, we employed the results of previous Approximate Bayesian Computation methods for LDD inference from genetic structure data in bryophytes39,77 to define the range of LDD probability values, set to 0, 10−4, 10−3, 10−2 and 10−1.
    Migclim simulations
    We modeled the dispersal of a species under a climate change scenario over a period of 40 years, from 2010 to 2050. Starting with an initial distribution for the year 2010, the climatic suitability of cells was updated every 10 years to reflect the projected changes in climatic conditions under the considered climate change scenario. Since our simulations run over 40 years, we need four different climatic suitability maps. The wind layers were updated at the same 10 years intervals as the climatic data to produce series of spatially and temporally explicit kernel maps. We assume that our species disperse once a year, and hence, our simulations performed a total of 40 dispersal steps between 2010 and 2050. For each 10 years climatic period, pixels were identified as potentially suitable based on the binarized climatic suitability model projections. While climatic suitability thus drove colonization probability, a recent study raised the intriguing idea that spread rates at the migration front increase as climatic suitability decreases as a response to the need to seek for more suitable habitats78. In bryophytes, however, such a mechanism would be unlikely as inadequate resources and investment in environmental stress defence typically result in shifts from sexual to asexual reproduction79.
    For each species, we ran a sensitivity analysis by testing the impact of variation of the free parameters described above: two values of horizontal windspeed Ū (monthly average and daily maximum), three values of spore release height Z0 (0.03, 1 and 10 m), and four values of LDD probabilities (see above). For each parameter combination, 30 MigClim replicates were performed.
    We computed the ratio between the predicted loss of suitable area (fraction of initially suitable cells that became unsuitable by 2050) and the simulated effective colonization rate (fraction of newly suitable cells by 2050 that were effectively colonized) using two extreme values of the LDD probability range, that is, 0 and 0.1.
    To determine the time-lag of the colonization of newly suitable habitats, the analyses were run for 500 years, keeping the environmental parameters at their 2050 values.
    Reporting summary
    Further information on research design is available in the Nature Research Reporting Summary linked to this article. More

  • in

    Evidence for a cryptic parasitoid species reveals its suitability as a biological control agent

    Drosophila rearing
    The starting colony of D. suzukii was collected from wild Rubus sp. and Fragaria sp. fruits in various sites in Switzerland in 201523. The flies from the initial collection are described molecularly by Fraimout et al.43. The starting colony of D. melanogaster and D. simulans were obtained from laboratory colonies of INRA (Sophia-Antipolis, France) in 2015 and 2019, respectively. The general rearing of flies was done in plastic tubes (5 cm diameter, 10 cm height) containing approximately 10 g of artificial diet (Formula 4-24 medium, Carolina Biological SupplyCo., Burlington, NC), 40 ml of methyl-4-hydroxylbenzoate solution (1.43 g/L) to inhibit fungal growth, and a few grains of commercial instant dry yeast. The tubes were kept in growth chambers at 22 ± 2 °C, 60% ± 10% RH, and a 16 h photoperiod (hereafter called general rearing conditions). To collect eggs and resulting larvae on different nutritive media (i.e., fresh and decomposing fruits or artificial diet) for the below-described parasitoid rearing and experiments with parasitoids, some adult flies were kept in gauze cages (BugDorm-4F4545) at general rearing conditions. They were fed with sugar water provided on dental cotton rolls and dried instant yeast, additional water was provided on cellulose paper. The nutritive media were exposed to adult flies when needed.
    Parasitoid rearing
    The starting colonies of G. cf. brasiliensis were obtained during surveys in Asia from 2015–2017 and names to describe their origin are based on the collection sites described by Girod et al.19: Dali, Fumin, Kunming, Shiping, and Kunming—Xining temple (Xining in this study) in the Yunnan Province of China, as well as Hasuike (Nagano) and Tokyo—Naganuma park (actually on the territory of Hachioji but named Tokyo in this study) in Japan. The parasitoids were reared in the quarantine laboratory at CABI-Switzerland (Delémont, Switzerland) separated by origin in gauze cages (BugDorm-4F4545) to prevent them from interbreeding. The general rearing was done on D. suzukii larvae feeding on blueberries as described by Girod et al.19, with the difference that fruits were only exposed for 24 h to D. suzukii for oviposition. The environmental parameters of the quarantine chamber were the above-described general rearing conditions. Up to 50 adult wasps were kept in transparent plastic containers (9 cm diameter, 5 cm height) inside each gauze cage. An Eppendorf tube with a wet cellulose paper was added as a water source and the container was closed with a foam plug on which a drop of honey was placed as food source. Six fresh blueberries, which were placed 24 h before in the D. suzukii rearing cages to collect eggs, were added every 2–3 days to each container with adults to allow for parasitism of young fly larvae. After the exposure to the wasps, infested fruits were removed from the containers and kept in clear plastic tubes (5 cm diameter, 10 cm height) with a filter paper at the bottom to absorb leaking fruit juice. Every 2–3 days, the presence of newly hatched wasps was checked among rearing tubes and adult wasps were transferred to the oviposition containers.
    Molecular characterization
    The molecular characterization was performed on (1) individuals originating from the field (nine locations from five provinces in China and three locations from three prefectures of the Honshu island in Japan), (2) the derived laboratory strains and (3) individuals used for the experiments (Table S2). Two molecular markers were used, the mitochondrial coding gene Cytochrome Oxidase subunit 1 (COI) and the nuclear region Internal Transcripted Spacer 2 (ITS2). Both were previously used to characterize Ganaspis individuals from Eastern Asia22,23 and elsewhere.
    The DNA was extracted in a total of 30 µl using either the prepGEM Insect kit (Zygem) (3 h at 75 °C and 5 min at 95 °C), or the QuickExtract DNA Extraction Solution (n°QE09050, Lucigen) (15 min at 65 °C and 2 min at 98 °C). For both molecular markers (COI and ITS2), each individual PCR was realized in a total of 25 µl, including 12.5 µl of the Multiplex PCR Master Mix (Qiagen), 0.125 µl of each primer (100 µM), and 1 µl DNA. For COI, the primers LCO (5′-GGTCAACAAATCATAAAGATATTGG-3′) and HCO (5′-TAAACTTCAGGGTGACCAAAAAATCA-3′)44 were used for more than 400 individuals. PCR conditions consisted of (1) 15 min at 95 °C, (2) 35 cycles of 30 s at 94 °C, 90 s at 50 °C and 60 s at 72 °C, (3) 10 min at 72 °C. For ITS2, the primers ITS2-F (5′-TGTGAACTGCAGGACACATG-3′) and ITS2-R (5′-AATGCTTAAATTTAGGGGTA-3′)45 were used for a subset of representative individuals. PCR conditions consisted of (1) 15 min at 95 °C; (2) 40 cycles of 30 s at 94 °C, 90 s at 53 °C, and 60 s at 72 °C; and (3) 10 min at 72 °C. In both cases, the PCR was checked using a QIAxcel DNA Fast Analysis Kit on a QIAxcel Advanced System (Qiagen). Positive PCR products were then sequenced with the Sanger method in one direction with the HCO primer for COI and both directions for ITS2. Sequences were trimmed, assembled and aligned using ClustalW for COI and Muscle for ITS2 (Geneious, version 10.2.3). For COI, only haplotypes observed twice within the panel of high-quality sequences (length  > 520 bp and no undetermined nucleotide) were considered. These data were then enriched with 83 additional GenBank accessions, including in particular sequences from Nomano et al.22 and Giorgini et al.23. The whole dataset (our own haplotypes and GenBank accessions) was then analyzed on a common part of 519 bp included between the two marks, ATTGGDTCAA and TTAGCAGGTG (5′ → 3′ on the positive strand). Three criteria were then applied to summarize and clean the data including: (1) the conservation of repres entative, necessary and sufficient sequences from the three main sources22,23 (and this study); (2) the exclusion of sequence with undetermined nucleotide(s); (3) the exclusion of each sequence with a unique amino-acid sequence. A final dataset of 62 sequences (haplotypes from this study and GenBank accessions) remained after this process. Based on this dataset, three complementary approaches were used to investigate the molecular clustering: (1) a Neighbour Joining approach using the Tamura 3 parameters distance (the best evolutionary model according to the software MEGA10.1.746), using 500 replicates for bootstrapping; (2) a Maximum Likelihood approach using the evolutionary model HKY85 + I (the best model according to the software PhyML3.047); and (3) the constitution of a network using the Median Joining method (ε set to zero, PopArt48). The Kimura 2 parameters distance (often used in the frame of barcoding’s studies) was also used to investigate the pairwise distances within and between clusters (see Discussion). For ITS2, the identified haplotypes were directly compared to those available on GenBank and mapped into the COI Neighbor-Joining tree.
    Crossing experiments
    Ganaspis brasiliensis is arrhenotokous, unmated females produce only male progeny while mated females are able to produce both males (unfertilized eggs) and females (fertilized eggs). Thus, the proportion of female progeny can be used as an indicator of reproductive isolation. With regard to already acquired knowledge on Asian Ganaspis cf. brasiliensis19,22,25,30, we more precisely investigated here the reproductive (in)compatibilities between the two main molecular clusters (G1 and G3-4—see Results and Discussion) and, within the cluster G1, between two geographically distant populations (one Chinese and one Japanese). Thus, crossing experiments with individuals from three locations were done here: Tokyo, Hasuike and Kunming. For the latter, only individuals that were a posteriori affiliated to G1 through the molecular characterization described above were taken into account. For individuals from each location, parasitized Drosophila pupae from the general parasitoid rearing (see above) were identified under a microscope (parasitoid pupae can be seen through the translucent Drosophila pupal case) and kept individually in plastic vials containing moisturized plastic foams. Within 24 h after emergence, 1–2 males were placed with each virgin female during 24 h for mating. Females were then transferred to a plastic vial containing 10–30 first instar D. suzukii larvae feeding in fresh blueberries and drops of honey for the parasitoid’s nutrition. After 3 days, females were collected and kept in 95% ethanol for potential molecular analysis. The vials containing the potentially parasitized D. suzukii larvae in blueberries were kept until adult emergence under the general rearing conditions described above. Upon emergence of the F1 generation, adults were sexed based on antennal length (males have longer antennae than females24) and the percentage of female progeny was calculated for each parental female. To test the fertility of F1 females, they were allowed mating with males from the same origin for 24 h. Then, the above described oviposition procedure was repeated, and upon emergence, the F2 progeny was sexed and percentage of females was calculated. The number of parental females for each crossing varied from 9–24 (Table 1), depending on emergence during the experimental period.
    Affinity towards the targeted host and its nutritive media
    To study the specificity of G. cf. brasiliensis from the above mentioned seven different origins in Asia, three combinations of hosts and nutritive media were tested under no-choice conditions: (1) D. suzukii larvae feeding on blueberries, (2) D. suzukii larvae feeding on artificial diet, and (3) D. melanogaster larvae feeding on artificial diet. The blue formula of the above-mentioned artificial diet was used to facilitate counting of Drosophila eggs. Additionally, the diet was blended with about 25 g of fresh blueberries, as described by Girod et al.25. The artificial diet and fresh blueberries were exposed to the respective Drosophila species for 1–3 h, until 10–30 eggs were counted under a microscope, and incubated for 24 h at room temperature to allow eggs to hatch. Mated and naïve (i.e., never exposed to hosts for oviposition) 3–4 d old G. cf. brasiliensis females were then released individually into plastic tubes (2.7 cm diameter, 5.2 cm height) containing one of the three media. The tubes were closed with a moist foam lid containing a drop of honey to nourish the parasitoids. Females were removed from the tubes after 48 h and placed in 95% ethanol for genetic identification based on CO1, as described above. The tubes containing potentially parasitized Drosophila larvae were kept at the general rearing conditions and observed for fly and parasitoid emergence on a regular basis for 40 d. For each tube, the number of Drosophila flies and parasitoids were recorded. For each parasitoid origin, 20 replicates per host species-nutritive media combination were tested, for a total of 420 individual females.
    Influence of the nutritive media on the parasitism of non-target species
    A second no-choice test was done to investigate whether G. cf. brasiliensis’ host specificity is dependent on the nutritive medium of the host. To this end, four host species-nutritive medium combinations were tested: D. melanogaster or D. simulans larvae feeding on either blueberries or artificial diet. Because both Drosophila species do not have a serrated ovipositor and can therefore not oviposit through the skin of fresh fruits, slightly decomposed blueberries were cut in half and exposed to these species until 10–30 eggs were counted on each half. As in the first no-choice test, the artificial diet used in this experiment was the blue formula blended with about 25 g blueberries. The experiment was then conducted as described above for the first no-choice test, with the difference that 10 replicates for each host species-nutritive medium combination were used for parasitoids originating from Tokyo, Xining, and Hasuike only. This brought the total number of females for this experiment to 120.
    Preference for the targeted host and its habitats
    To investigate differences in preferences for the targeted host and its habitats among the different genetic groups of G. cf. brasiliensis, a three- and a four-choice bioassay were done. The bioassays took place in a cylindrical transparent plastic container (10 cm diameter, 5 cm height) with two holes of 2.5 cm diameter in the lid: one was covered with netting for ventilation and the other closed with a foam plug on which a drop of honey was placed to nourish the parasitoid. Inside each container, one 4–5 days old mated parasitoid female was placed, a plastic vial with wet cellulose paper as a water source, and small dishes (2.5 cm diameter, 1 cm height) containing the choices for oviposition in a random order. To avoid the influence of light and colors on the wasp’s directional choice, the choice arenas were placed inside a white plastic box (100 × 50 cm), leaving only one light source from above. After 24 h in the choice arena at the general rearing conditions, female parasitoids were kept in 95% ethanol to allow for further DNA analysis confirming the genetic group they belonged to. The dishes containing the different hosts and nutritive media were placed separately in rearing tubes (5 cm diameter, 10 cm height) containing a moist filter paper at the bottom and covered with a moist foam lid to avoid drying of the media. Three weeks after the beginning of the choice test, all adult Drosophila were removed from the rearing tubes and were counted. Until the eighth week after the choice test, emerging parasitoids were collected once a week, sexed, and counted.
    The three-choice bioassay was designed to determine if also when given the choice, G1 G. cf. brasiliensis are specific to fruits as the host’s nutritive medium, rather than to the host species, while G3-4 parasitoids are not specific to either. Therefore, the three host-species-nutritive medium combinations were (1) D. suzukii or (2) D. melanogaster larvae feeding on fresh blueberry, and (3) D. melanogaster larvae feeding on artificial diet. All media were prepared as described above for the no-choice experiments. In total, 68 female wasps were tested in the three-choice bioassay, 20 originating from Hasuike, 24 from Tokyo, and 24 from Xining.
    To determine if the habitat specificity of G1 and generality of G3-4 G. cf. brasiliensis also hold true when comparing fresh to decomposing fruits, a four-choice bioassay was designed. The host species-nutritive media combinations were (1) D. suzukii or (2) D. melanogaster larvae feeding on either (3) fresh or (4) decomposing blueberry. Infestation of fresh blueberries with fly larvae was done as described above. To decompose fruits, blueberries were exposed to room temperature in a plastic container for 7–10 days until growth of molt was visible. They were then exposed to D. suzukii and D. melanogaster for the collection of eggs as described for fresh fruits. In total, 27 and 22 females originating from Tokyo (G1) and Hasuike (G3-4) were tested, respectively, in the four-choice bioassay. For all choice tests, only results from females that produced at least one offspring were analyzed.
    Statistical analysis
    Apparent parasitism (AP) was calculated as the proportion of parasitoid offspring among the total number of insects that emerged from the nutritive medium (i.e. Drosophila sp. and parasitoids). The proportion of ovipositing females (POF) was calculated as the number of female parasitoids which produced at least one offspring (or which showed an oviposition response, in the case of the behavioral experiments) divided by the number of females tested. All data were analyzed using logistic regression followed by post-hoc comparisons of means with Tukey adjustments. Differences in proportions of females in the crossing experiment as well as AP and POF in the no-choice experiments was analyzed using quasibinomial distributions to account for overdispersion of the residuals (glm function of the ‘stats’ package in R49). For the no-choice experiment with parasitoids from different origins, AP was analyzed with the explanatory variables parasitoid origin, nutritive medium, and their interaction; and the POF developing on D. melanogaster feeding on artificial diet was analyzed with the parasitoid’s genetic group (G1 or G3-4) as explanatory variable. AP in the no-choice experiment with non-target species, the explanatory variables were parasitoid origin, host species, nutritive medium, and all possible interactions.
    Mixed effects logistic regressions (glmer function of the ‘lme4’ package in R50) were used to analyze AP in the choice tests. Analyses were done for each parasitoid origin separately because of convergence problems with more than one fixed effect. Therefore, nutritive medium was the sole fixed-effect explanatory variable for all analyses concerning the choice tests. In all cases, individual females were included as a random effect to account for correlation of parasitism between the media by the same female and an additional observation-level random effect was introduced to solve the problem of residual overdispersion. More

  • in

    Polyandry blocks gene drive in a wild house mouse population

    1.
    Burt, A. & Trivers, R. Genes in Conflict: The Biology of Selfish Genetic Elements (Belknap Press, Cambridge, 2006).
    2.
    Lindholm, A. K. et al. The ecology and evolutionary dynamics of meiotic drive. Trends Ecol. Evolution 31, 316–326 (2016).
    Google Scholar 

    3.
    Champer, J., Kim, I. K., Champer, S. E., Clark, A. G. & Messer, P. W. Performance analysis of novel toxin-antidote CRISPR gene drive systems. BMC Biol. 18, 1–17 (2020).
    Google Scholar 

    4.
    Godwin, J. et al. Rodent gene drives for conservation: opportunities and data needs. Proc. R. Soc. B 286, 20191606 (2019).
    PubMed  PubMed Central  Google Scholar 

    5.
    Champer, J., Buchman, A. & Akbari, O. S. Cheating evolution: engineering gene drives to manipulate the fate of wild populations. Nat. Rev. Genet. 17, 146 (2016).
    CAS  PubMed  PubMed Central  Google Scholar 

    6.
    Haig, D. & Bergstrom, C. Multiple mating, sperm competition and meiotic drive. J. Evol. Biol. 8, 265–282 (1995).
    Google Scholar 

    7.
    Manser, A., Lindholm, A. K., König, B. & Bagheri, H. C. Polyandry and the decrease of a selfish genetic element in a wild house mouse population. Evolution 65, 2435–2447 (2011).
    PubMed  PubMed Central  Google Scholar 

    8.
    Holman, L., Price, T. A., Wedell, N. & Kokko, H. Coevolutionary dynamics of polyandry and sex-linked meiotic drive. Evolution 69, 709–720 (2015).
    PubMed  PubMed Central  Google Scholar 

    9.
    Price, T. & Wedell, N. Selfish genetic elements and sexual selection: their impact on male fertility. Genetica 134, 99–111 (2008).
    PubMed  Google Scholar 

    10.
    Wedell, N. The dynamic relationship between polyandry and selfish genetic elements. Philos. Trans. R. Soc. Lond. Ser. B, Biol. Sci. 368, 1–10 (2013).
    Google Scholar 

    11.
    Sutter, A. & Lindholm, A. K. Detrimental effects of an autosomal selfish genetic element on sperm competitiveness in house mice. Proc. R. Soc. B 282, 20150974 (2015).
    Google Scholar 

    12.
    Manser, A., Lindholm, A. K., Simmons, L. W. & Firman, R. C. Sperm competition suppresses gene drive among experimentally evolving populations of house mice. Mol. Ecol. 20, 5784–5792 (2017).
    Google Scholar 

    13.
    Price, T., Hodgson, D., Lewis, Z., Hurst, G. & Wedell, N. Selfish genetic elements promote polyandry in a fly. Science 332, 1241–1243 (2008).
    ADS  Google Scholar 

    14.
    Price, T. et al. Sex ratio distorter reduces sperm competitive ability in an insect. Evolution 62, 1644–1652 (2008).
    PubMed  Google Scholar 

    15.
    Herrmann, B. G. & Bauer, H. The Mouse t-haplotype: a Selfish Chromosome—Genetics, Molecular Mechanism, and Evolution, Vol. 3, 297–314 (Cambridge University Press, Cambridge, 2012).

    16.
    Lindholm, A. K., Musolf, K., Weidt, A. & König, B. Mate choice for genetic compatibility in the house mouse. Ecol. Evolution 3, 1231–1247 (2013).
    Google Scholar 

    17.
    Dean, M., Ardlie, K. & Nachman, M. The frequency of multiple paternity suggests that sperm competition is common in house mice (Mus domesticus). Mol. Ecol. 15, 4141–4151 (2006).
    CAS  PubMed  PubMed Central  Google Scholar 

    18.
    Firman, R. & Simmons, L. Polyandry facilitates postcopulatory inbreeding avoidance in house mice. Evolution 62, 603–611 (2008).
    PubMed  Google Scholar 

    19.
    Thonhauser, K. E., Thoss, M., Musolf, K., Klaus, T. & Penn, D. J. Multiple paternity in wild house mice (Mus musculus musculus): effects on offspring genetic diversity and body mass. Ecol. Evolution 4, 200–209 (2013).
    Google Scholar 

    20.
    Auclair, Y., König, B. & Lindholm, A. K. Socially mediated polyandry: a new benefit of communal nesting in mammals. Behav. Ecol. 25, 1467–1473 (2014).
    PubMed  PubMed Central  Google Scholar 

    21.
    Rolland, C., Macdonald, D., de Fraipont, M. & Berdoy, M. Free female choice in house mice: leaving best for last. Behaviour 140, 1371–1388 (2003).
    Google Scholar 

    22.
    Thonhauser, K. E., Raveh, S., Hettyey, A., Beissmann, H. & Penn, D. J. Scent marking increases male reproductive success in wild house mice. Anim. Behav. 86, 1013–1021 (2013).
    PubMed  PubMed Central  Google Scholar 

    23.
    Thonhauser, K. E., Raveh, S. & Penn, D. J. Multiple paternity does not depend on male genetic diversity. Anim. Behav. 93, 135–141 (2014).
    PubMed  PubMed Central  Google Scholar 

    24.
    Bronson, F. The reproductive ecology of the house mouse. Q. Rev. Biol. 54, 265–299 (1979).
    CAS  PubMed  Google Scholar 

    25.
    Evans, J. P. & Simmons, L. W. The genetic basis of traits regulating sperm competition and polyandry: can selection favour the evolution of good-and sexy-sperm? Genetica 134, 5 (2008).
    PubMed  Google Scholar 

    26.
    McFarlane, E. S. et al. The heritability of multiple male mating in a promiscuous mammal. Biol. Lett. 7, 368–371 (2011).
    PubMed  Google Scholar 

    27.
    Reid, J. M., Arcese, P., Sardell, R. J. & Keller, L. F. Heritability of female extra-pair paternity rate in song sparrows (Melospiza melodia). Proc. R. Soc. B 278, 1114–1120 (2011).
    PubMed  Google Scholar 

    28.
    Sutter, A. & Lindholm, A. K. Meiotic drive changes sperm precedence patterns in house mice: potential for male alternative mating tactics? BMC Evolut. Biol. 16, 133 (2016).
    Google Scholar 

    29.
    Sutter, A. & Lindholm, A. K. The copulatory plug delays ejaculation by rival males and affects sperm competition outcome in house mice. J. Evol. Biol. 29, 1617–1630 (2016).
    CAS  PubMed  Google Scholar 

    30.
    Atlan, A., Joly, D., Capillon, C. & Montchamp-Moreau, C. Sex-ratio distorter of Drosophila simulans reduces male productivity and sperm competition ability. J. Evol. Biol. 17, 744 (2004).
    CAS  PubMed  PubMed Central  Google Scholar 

    31.
    Wilkinson, G., Johns, P., Kelleher, E., Muscedere, M. & Lorsong, A. Fitness effects of X chromosome drive in the stalk-eyed fly, Cyrtodiopsis dalmanni. J. Evol. Biol. 19, 1851–1860 (2006).
    CAS  PubMed  PubMed Central  Google Scholar 

    32.
    Angelard, C., Montchamp-Moreau, C. & Joly, D. Female-driven mechanisms, ejaculate size and quality contribute to the lower fertility of sex-ratio distorter males in Drosophila simulans. BMC Evol. Biol. 8, 1–12 (2008).
    PubMed  PubMed Central  Google Scholar 

    33.
    Dyer, K. A. & Hall, D. W. Fitness consequences of a non-recombining sex-ratio drive chromosome can explain its prevalence in the wild. Proc. R. Soc. B 286, 20192529 (2019).
    PubMed  PubMed Central  Google Scholar 

    34.
    Keais, G., Lu, S. & Perlman, S. Autosomal suppression and fitness costs of an old driving X chromosome in Drosophila testacea. J. Evol. Biol. 33, 619–628 (2020).

    35.
    Price, T. A., Lewis, Z., Smith, D. T., Hurst, G. D. & Wedell, N. Sex ratio drive promotes sexual conflict and sexual coevolution in the fly Drosophila pseudoobscura. Evolution 64, 1504–1509 (2010).
    PubMed  PubMed Central  Google Scholar 

    36.
    Runge, J.-N. & Lindholm, A. K. Carrying a selfish genetic element predicts increased migration propensity in free-living wild house mice. Proc. R. Soc. B 285, 20181333 (2018).
    PubMed  PubMed Central  Google Scholar 

    37.
    Meade, L., Finnegan, S., Kad, R., Fowler, K. & Pomiankowski, A. Adaptive maintenance of fertility in the face of meiotic drive. Am. Naturalist 195, 743–751 (2019).
    Google Scholar 

    38.
    Zeh, J. & Zeh, D. The evolution of polyandry II: post-copulatory defences against genetic incompatibility. Proc. R. Soc. B 264, 69–75 (1997).
    ADS  Google Scholar 

    39.
    Yasui, Y. A “good-sperm” model can explain the evolution of costly multiple mating by females. Am. Naturalist 149, 573–584 (1997).
    Google Scholar 

    40.
    Ferrari, M., Lindholm, A. K. & König, B. Fitness consequences of female alternative reproductive tactics in house mice (Mus musculus domesticus). Am. Naturalist 193, 106–124 (2019).
    Google Scholar 

    41.
    Ardlie, K. G. & Silver, L. M. Low frequency of t haplotypes in natural populations of house mice (Mus musculus domesticus). Evolution 52, 1185–1196 (1998).
    PubMed  Google Scholar 

    42.
    Ardlie, K. Putting the brake on drive: meiotic drive of t haplotype in natural populations of mice. Trends Genet. 14, 189–193 (1998).
    CAS  PubMed  Google Scholar 

    43.
    Young, S. A proposition on the population dynamics of the sterile t alleles in the house mouse. Evolution 21, 190–192 (1967).
    CAS  PubMed  Google Scholar 

    44.
    Petras, M. & Topping, J. The maintenance of polymorphisms at two loci in house mouse (Mus musculus) populations. Genome 25, 190–201 (1983).
    CAS  Google Scholar 

    45.
    Bull, J. Lethal gene drive selects inbreeding. Evolution 1, 1–16 (2017).

    46.
    van Boven, M. & Weissing, F. J. Segretation distortion in a deme-structured population: opposing demands of gene, individual and group selection. J. Evol. Biol. 12, 80–93 (1999).
    Google Scholar 

    47.
    Nunney, L. The role of deme size, reproductive patterns, and dispersal in the dynamics of t-lethal haplotypes. Evolution 47, 1342–1359 (1993).
    PubMed  Google Scholar 

    48.
    Lenington, S. The t complex: a story of genes, behavior, and populations. Adv. Study Behav. 20, 51–86 (1991).
    Google Scholar 

    49.
    Sutter, A. & Lindholm, A. K. No evidence for female discrimination against male house mice carrying a selfish genetic element. Curr. Zool. 62, zow063 (2016).
    Google Scholar 

    50.
    Manser, A., König, B. & Lindholm, A. Female house mice avoid fertilization by t haplotype incompatible males in a mate choice experiment. J. Evol. Biol. 28, 54–64 (2015).
    CAS  PubMed  Google Scholar 

    51.
    Manser, A., Lindholm, A. K. & Weissing, F. J. The evolution of costly mate choice against segregation distorters. Evolution 71, 2817–2828 (2017).

    52.
    Price, T., Verspoor, R. & Wedell, N. Ancient gene drives: an evolutionary paradox. Proc. R. Soc. B 286, 20192267 (2019).
    CAS  PubMed  Google Scholar 

    53.
    Galizi, R. et al. A synthetic sex ratio distortion system for the control of the human malaria mosquito. Nat. Commun. 5, 3977 (2014).
    ADS  CAS  PubMed  PubMed Central  Google Scholar 

    54.
    Galizi, R. et al. A CRISPR-Cas9 sex-ratio distortion system for genetic control. Sci. Rep. 6, 31139 (2016).
    ADS  CAS  PubMed  PubMed Central  Google Scholar 

    55.
    Piaggio, A. J. et al. Is it time for synthetic biodiversity conservation? Trends Ecol. Evolution 32, 97–107 (2017).
    Google Scholar 

    56.
    Leitschuh, C. M. et al. Developing gene drive technologies to eradicate invasive rodents from islands. J Responsible Innov. 5, S121–138 (2017).

    57.
    Manser, A. et al. Controlling invasive rodents via synthetic gene drive and the role of polyandry. Proc. R. Soc. B 286, 20190852 (2019).
    PubMed  Google Scholar 

    58.
    Howald, G. et al. Invasive rodent eradication on islands. Conserv. Biol. 21, 1258–1268 (2007).
    PubMed  Google Scholar 

    59.
    Prowse, T. A., Adikusuma, F., Cassey, P., Thomas, P. & Ross, J. V. A Y-chromosome shredding gene drive for controlling pest vertebrate populations. Elife 8, e41873 (2019).
    PubMed  PubMed Central  Google Scholar 

    60.
    König, B. & Lindholm, A. The Complex Social Environment of Female House Mice (Mus domesticus), 114–134 (Cambridge University Press, Cambridge, 2012).

    61.
    Berry, R., Tattersall, F. & Hurst, J. Genus Mus (The Mammal Society Southampton, 2008).

    62.
    Kalinowski, S. T., Taper, M. L. & Marshall, T. C. Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol. Ecol. 16, 1099–1106 (2007).
    Google Scholar 

    63.
    Brambell, F. The influence of lactation on the implantation of the mammalian embryo. Am. J. Obstet. Gynecol. 33, 942–953 (1937).
    Google Scholar 

    64.
    Schimenti, J. & Hammer, M. Rapid identification of mouse t haplotype by PCR polymorphism (PCRP). Mouse Genome 108 (1990).

    65.
    Wilson, A. J. et al. An ecologist’s guide to the animal model. J. Anim. Ecol. 79, 13–26 (2010).
    PubMed  Google Scholar 

    66.
    Hadfield, J. D. et al. MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J. Stat. Softw. 33, 1–22 (2010).
    Google Scholar 

    67.
    Bruck, D. Male segregation ratio advantage as a factor in maintaining lethal alleles in wild populations of house mice. Proc. Natl Acad. Sci. USA 43, 152–158 (1957).
    ADS  CAS  PubMed  Google Scholar  More

  • in

    Get Africa’s Great Green Wall back on track

    Forest land surrounding Ethiopia’s churches are important islands of biodiversity. The government has pledged to restore 15 million hectares of degraded and deforested land by 2030.Credit: Kieran Dodds/Panos

    The Great Green Wall of Africa, a plan to restore a 7,000-kilometre-long stretch of degraded land from Senegal in West Africa to Djibouti in the east, is a bold and ambitious idea intended to help combat drought and desertification, which currently affect around 45% of Africa’s land area. Proposed 13 years ago by two of the continent’s elder statesmen, Nigeria’s then president Olusegun Obasanjo and Senegal’s former president Abdoulaye Wade, it is even more important now, given the threat from climate change and the reliance of the continent’s people on agriculture for their livelihoods.
    But, so far, the project has struggled to reach key goals. Less than one-fifth of the designated land area has been restored or rehabilitated. The African Union’s top decision makers don’t see the green wall as a priority, and inter-national donors seem reluctant to commit further funding. Researchers, governments and international agencies must work together better to rehabilitate this crucial scheme.
    The project’s focus has widened from its founders’ vision because there are more ways to restore degraded land than by reforestation, such as creating communal gardens and nature reserves. But the addition of these and other measures has made the green wall more complex. It has required different ministries in individual countries to work together. That is always difficult, but it becomes even more so when two further variables are added: the African Union and the international donor community. These and other observations are confirmed in an independent assessment of the project, commissioned by the project’s partners and published in September by the United Nations Convention to Combat Desertification (UNCCD).
    The assessment report tries to look on the bright side. It says that 11 countries along the green wall have re-habilitated nearly 4 million hectares of land and created 350,000 jobs in the process. It also confirms that a broader group of 21 African countries is committed to restoring and rehabilitating 100 million hectares of land by 2030, creating 10 million green jobs. But it doesn’t sugar-coat the fact that governments and donors will need to find between US$3.6 billion and $4.3 billion every year for the next decade if the 100-million-hectare target is to be achieved. That will be a tall order — the report calls it a “quantum leap” — considering that the project raised around $2 billion in its first decade. But it is not impossible — and there are several key ways in which researchers can contribute.
    The UNCCD report provides headline information on each country’s progress — such as the numbers of plants and seedlings produced; the area of land reforested; and the numbers of people trained and jobs created. Most of these data were provided by each country. The next step should be for independent researchers — for example, members of IPBES (the Intergovernmental Science–Policy Platform on Biodiversity and Ecosystem Services) — to assess these data and publish their own reviews, to help all sides have more confidence in the data and in the monitoring process.
    Funding is always a challenge in such projects. But although it might seem feasible that the 55 member states of the African Union and their inter-national partners could raise the required amounts, nations have already committed funding to inter-national initiatives with similar goals to those of the green wall. African countries, for example, are signatories to the Aichi Bio-diversity Targets, which include a goal to reduce habitat loss and degradation. Countries have also signed up to the UN Sustainable Development Goals, which include a target of combating desertification and restoring degraded land and soil. And they are also members of the UNCCD, which has pledged to reach what it is calling “land degradation neutrality” by 2030.
    The UNCCD report suggests a single trust fund could be the answer. That would work if countries and international agencies agree to pool their resources and create harmonized reporting requirements. Researchers could help here by developing a method for measuring whether countries are succeeding in meeting their green-wall goals, as well as providing a common accounting framework.
    The need to restore and rehabilitate land is urgent. People in the affected countries are among the world’s poorest. The overwhelming majority earn their living from agriculture or livestock production. Climate change is projected to lift average temperatures by 3–6 °C by the end of the century, compared with a late-twentieth-century baseline. More extremes of weather are expected, and these, in turn, will reduce crop yields.
    The green-wall project needs international agencies to cooperate better, it needs researchers to help, and it needs the present generation of the continent’s leaders to step up and take on a more visible role in championing it, just as its two founding presidents did. More

  • in

    Assessing ecological uncertainty and simulation model sensitivity to evaluate an invasive plant species’ potential impacts to the landscape

    1.
    Sofaer, H. R., Jarnevich, C. S. & Pearse, I. S. The relationship between invader abundance and impact. Ecosphere 9, e02415. https://doi.org/10.1002/ecs2.2415 (2018).
    Article  Google Scholar 
    2.
    Parker, I. M. et al. Impact: Toward a framework for understanding the ecological effects of invaders. Biol. Invasions 1, 3–19. https://doi.org/10.1023/a:1010034312781 (1999).
    Article  Google Scholar 

    3.
    Fusco, E. J., Finn, J. T., Balch, J. K., Nagy, R. C. & Bradley, B. A. Invasive grasses increase fire occurrence and frequency across US ecoregions. Proc. Natl. Acad. Sci. 116, 23594–23599. https://doi.org/10.1073/pnas.1908253116 (2019).
    ADS  CAS  Article  PubMed  Google Scholar 

    4.
    Hellmann, J. J., Byers, J. E., Bierwagen, B. G. & Dukes, J. S. Five potential consequences of climate change for invasive species. Conserv. Biol. 22, 534–543. https://doi.org/10.1111/j.1523-1739.2008.00951.x (2008).
    Article  PubMed  Google Scholar 

    5.
    Clark, J. S. et al. Ecological forecasts: An emerging imperative. Science 293, 657–660. https://doi.org/10.1126/science.293.5530.657 (2001).
    CAS  Article  PubMed  Google Scholar 

    6.
    Andrew, M. E. & Ustin, S. L. The role of environmental context in mapping invasive plants with hyperspectral image data. Remote Sens. Environ. 112, 4301–4317. https://doi.org/10.1016/j.rse.2008.07.016 (2008).
    ADS  Article  Google Scholar 

    7.
    Chesson, P. et al. Resource pulses, species interactions, and diversity maintenance in arid and semi-arid environments. Oecologia 141, 236–253. https://doi.org/10.1007/s00442-004-1551-1 (2004).
    ADS  Article  PubMed  Google Scholar 

    8.
    Theoharides, K. A. & Dukes, J. S. Plant invasion across space and time: Factors affecting nonindigenous species success during four stages of invasion. New Phytol. 176, 256–273. https://doi.org/10.1111/j.1469-8137.2007.02207.x (2007).
    Article  PubMed  Google Scholar 

    9.
    Daniel, C., Frid, L., Sleeter, B. & Fortin, M.-J. State-and-transition simulation models: A framework for forecasting landscape change. Methods Ecol. Evol. 7, 1413–1423. https://doi.org/10.1111/2041-210x.12597 (2016).
    Article  Google Scholar 

    10.
    Frid, L. & Wilmshurst, J. F. Decision analysis to evaluate control strategies for crested wheatgrass (Agropyron cristatum) in Grasslands National Park of Canada. Invasive Plant Sci. Manag. 2, 324–336 (2009).
    Article  Google Scholar 

    11.
    Jarnevich, C. S., Holcombe, T. R., Cullinane Thomas, C., Frid, L. & Olsson, A. Simulating long-term effectiveness and efficiency of management scenarios for an invasive grass. AIMS Environ. Sci. 2, 427–447, https://doi.org/10.3934/environsci.2015.2.427 (2015).

    12.
    Frid, L. et al. Using state and transition modeling to account for imperfect knowledge in invasive species management. Invasive Plant Sci. Manag. 6, 36–47 (2013).
    Article  Google Scholar 

    13.
    Grechi, I. et al. A decision framework for management of conflicting production and biodiversity goals for a commercially valuable invasive species. Agric. Syst. 125, 1–11. https://doi.org/10.1016/j.agsy.2013.11.005 (2014).
    Article  Google Scholar 

    14.
    Miller, B. W., Symstad, A. J., Frid, L., Fisichelli, N. A. & Schuurman, G. W. Co-producing simulation models to inform resource management: A case study from southwest South Dakota. Ecosphere 8, e02020, https://doi.org/10.1002/ecs2.2020 (2017).

    15.
    Cullinane Thomas, C., Sofaer, H. R., Cline, S. & Jarnevich, C. S. Integrating landscape simulation models with economic and decision tools for invasive species control. Manag. Biol. Invasions 10, 6–22 (2019).

    16.
    Marshall, V. M., Lewis, M. M. & Ostendorf, B. Buffel grass (Cenchrus ciliaris) as an invader and threat to biodiversity in arid environments: A review. J. Arid Environ. 78, 1–12. https://doi.org/10.1016/j.jaridenv.2011.11.005 (2012).
    ADS  Article  Google Scholar 

    17.
    Jarnevich, C. S., Young, N. E., Talbert, M. & Talbert, C. Forecasting an invasive species’ distribution with global distribution data, local data, and physiological information. Ecosphere 9, e02279. https://doi.org/10.1002/ecs2.2279 (2018).
    Article  Google Scholar 

    18.
    Martin, T. et al. Buffel grass and climate change: A framework for projecting invasive species distributions when data are scarce. Biol. Invasions 17, 3197–3210. https://doi.org/10.1007/s10530-015-0945-9 (2015).
    Article  Google Scholar 

    19.
    de Albuquerque, F. S., Macías-Rodríguez, M. Á., Búrquez, A. & Astudillo-Scalia, Y. Climate change and the potential expansion of buffelgrass (Cenchrus ciliaris L., Poaceae) in biotic communities of Southwest United States and northern Mexico. Biol. Invasions 21, 3335–3347, https://doi.org/10.1007/s10530-019-02050-5 (2019).

    20.
    Castellanos, A. E., Celaya-Michel, H., Rodríguez, J. C. & Wilcox, B. P. Ecohydrological changes in semiarid ecosystems transformed from shrubland to buffelgrass savanna. Ecohydrology 9, 1663–1674. https://doi.org/10.1002/eco.1756 (2016).
    Article  Google Scholar 

    21.
    McDonald, C. J. & McPherson, G. R. Fire behavior characteristics of buffelgrass-fueled fires and native plant community composition in invaded patches. J. Arid Environ. 75, 1147–1154. https://doi.org/10.1016/j.jaridenv.2011.04.024 (2011).
    ADS  Article  Google Scholar 

    22.
    McDonald, C. J. & McPherson, G. R. Creating hotter fires in the Sonoran Desert: Buffelgrass produces copious fuels and high fire temperatures. Fire Ecol. 9, 26–39 (2013).
    Article  Google Scholar 

    23.
    Bracamonte, J. A., Tinoco-Ojanguren, C., Sanchez Coronado, M. E. & Molina-Freaner, F. Germination requirements and the influence of buffelgrass invasion on a population of Mammillaria grahamii in the Sonoran Desert. J Arid Environ. 137, 50–59, https://doi.org/10.1016/j.jaridenv.2016.11.003 (2017).

    24.
    Lyons, K. G., Maldonado-Leal, B. G. & Owen, G. Community and ecosystem effects of buffelgrass (Pennisetum ciliare) and nitrogen deposition in the Sonoran Desert. Invasive Plant Sci. Manag. 6, 65–78. https://doi.org/10.1614/ipsm-d-11-00071.1 (2013).
    CAS  Article  Google Scholar 

    25.
    Olsson, A. D., Betancourt, J., McClaran, M. P. & Marsh, S. E. Sonoran Desert Ecosystem transformation by a C4 grass without the grass/fire cycle. Divers. Distrib. 18, 10–21. https://doi.org/10.1111/j.1472-4642.2011.00825.x (2012).
    Article  Google Scholar 

    26.
    Miller, G., Friedel, M., Adam, P. & Chewings, V. Ecological impacts of buffel grass (Cenchrus ciliaris L.) invasion in central Australia—Does field evidence support a fire-invasion feedback? Rangeland J. 32, 353–365, https://doi.org/10.1071/rj09076 (2010).

    27.
    Fensham, R. J., Wang, J. & Kilgour, C. The relative impacts of grazing, fire and invasion by buffel grass (Cenchrus ciliaris) on the floristic composition of a rangeland savanna ecosystem. Rangeland J. 37, 227–237. https://doi.org/10.1071/RJ14097 (2015).
    Article  Google Scholar 

    28.
    Schlesinger, C., White, S. & Muldoon, S. Spatial pattern and severity of fire in areas with and without buffel grass (Cenchrus ciliaris) and effects on native vegetation in central Australia. Austral. Ecol. 38, 831–840. https://doi.org/10.1111/aec.12039 (2013).
    Article  Google Scholar 

    29.
    Jarnevich, C. S. et al. Developing an expert elicited simulation model to evaluate invasive species and fire management alternatives. Ecosphere 10, e02730. https://doi.org/10.1002/ecs2.2730 (2019).
    Article  Google Scholar 

    30.
    Esque, T. C., Schwartz, M. W., Lissow, J. A., Haines, D. F. & Garnett, M. C. Buffelgrass fuel loads in Saguaro National Park, Arizona, increase fire danger and threaten native species. Park Sci. 24, 33–37,56 (2007).

    31.
    Wallace, C. S. et al. Mapping presence and predicting phenological status of invasive buffelgrass in Southern Arizona using MODIS, climate and citizen science observation data. Remote Sens. 8, 524 (2016).
    ADS  Article  Google Scholar 

    32.
    Martin-R, M. H., Cox, J. R. & Ibarra-F, F. Climatic effects on buffelgrass productivity in the Sonoran Desert. J. Range Manag. 48, 60–63 (1995).
    Article  Google Scholar 

    33.
    Stillman, S. et al. Spatiotemporal variability of summer precipitation in Southeastern Arizona. J. Hydrometeorol. 14, 1944–1951. https://doi.org/10.1175/jhm-d-13-017.1 (2013).
    ADS  Article  Google Scholar 

    34.
    Arias, P. A., Fu, R. & Mo, K. C. Decadal variation of rainfall seasonality in the North American monsoon region and its potential causes. J. Clim. 25, 4258–4274. https://doi.org/10.1175/jcli-d-11-00140.1 (2012).
    ADS  Article  Google Scholar 

    35.
    R Core Team. R: A Language and Environment for Statistical Computing. (Foundation for Statistical Computing. Vienna, https://www.R-project.org/. Version 3.4.3., 2017).

    36.
    Finney, M. A. FARSITE: Fire area simulator-model development and evaluation. in Research Paper RMRS-RP-4, Ogden, UT: U.S. Department of Agriculture, Forest Service, Rocky Mountain Research Station. (2004).

    37.
    Sofaer, H. R. et al. The development and delivery of species distribution models to inform decision-making. Bioscience 69, 544–557. https://doi.org/10.1093/biosci/biz045 (2019).
    Article  Google Scholar 

    38.
    Chevan, A. & Sutherland, M. Hierarchical partitioning. Am. Stat. 45, 90–96. https://doi.org/10.1080/00031305.1991.10475776 (1991).
    Article  Google Scholar 

    39.
    Wickham, H. tidyverse: Easily Install and Load the ‘Tidyverse’. R package version 1.2.1. https://CRAN.R-project.org/package=tidyverse. (2017).

    40.
    Hijmans, R. J. raster: Geographic Data Analysis and Modeling. R package version 2.5-2. https://CRAN.R-project.org/package=raster. (2015).

    41.
    Walsh, C. & MacNally, R. hier.part: Hierarchical Partitioning. R package version 1.0-4. https://CRAN.R-project.org/package=hier.part. (2013).

    42.
    Jarnevich, C. J., Cullinane Thomas, C. M. & Young, N. E. State-and-Transition Simulation Models of Buffelgrass in Saguaro National Park (2014–2044) to explore ecological uncertainties: U.S. Geological Survey data release. https://doi.org/10.5066/P9IZKB25.

    43.
    Daniel, C. J., Ter-Mikaelian, M. T., Wotton, B. M., Rayfield, B. & Fortin, M.-J. Incorporating uncertainty into forest management planning: Timber harvest, wildfire and climate change in the boreal forest. For Ecol Manag 400, 542–554. https://doi.org/10.1016/j.foreco.2017.06.039 (2017).
    Article  Google Scholar 

    44.
    Ford, P. L., Reeves, M. C. & Frid, L. A tool for projecting Rangeland vegetation response to management and climate. Rangelands 41, 49–60. https://doi.org/10.1016/j.rala.2018.10.010 (2019).
    Article  Google Scholar 

    45.
    Olsson, A. D., Betancourt, J. L., Crimmins, M. A. & Marsh, S. E. Constancy of local spread rates for buffelgrass (Pennisetum ciliare L.) in the Arizona Upland of the Sonoran Desert. J Arid Environ 87, 136–143, https://doi.org/10.1016/j.jaridenv.2012.06.005 (2012).

    46.
    Weston, J. D., McClaran, M. P., Whittle, R. K., Black, C. W. & Fehmi, J. S. Satellite patches, patch expansion, and doubling time as decision metrics for invasion control: Pennisetum ciliare expansion in southwestern Arizona. Invasive Plant Sci. Manag. 12, 36–42 (2019).
    Article  Google Scholar 

    47.
    Cox, J. R. et al. The influence of climate and soils on the distribution of four African grasses. J Range Manag 41, 127–139. https://doi.org/10.2307/3898948 (1988).
    Article  Google Scholar 

    48.
    de la Barrera, E. & Castellanos, A. E. High temperature effects on gas exchange for the invasive buffel grass (Pennisetum ciliare [L.] Link). Weed Biol Manag 7, 128–131, https://doi.org/10.1111/j.1445-6664.2007.00248.x (2007).

    49.
    Reichmann, L. G., Sala, O. E. & Peters, D. P. C. Precipitation legacies in desert grassland primary production occur through previous-year tiller density. Ecology 94, 435–443. https://doi.org/10.1890/12-1237.1 (2013).
    Article  PubMed  Google Scholar 

    50.
    Colorado-Ruiz, G., Cavazos, T., Salinas, J. A., De Grau, P. & Ayala, R. Climate change projections from Coupled Model Intercomparison Project phase 5 multi-model weighted ensembles for Mexico, the North American monsoon, and the mid-summer drought region. Int. J. Climatol. 38, 5699–5716. https://doi.org/10.1002/joc.5773 (2018).
    Article  Google Scholar 

    51.
    Pascale, S. et al. Weakening of the North American monsoon with global warming. Nat. Clim. Change 7, 806, https://doi.org/10.1038/nclimate3412, https://www.nature.com/articles/nclimate3412#supplementary-information (2017).

    52.
    Pascale, S., Kapnick, S. B., Bordoni, S. & Delworth, T. L. The influence of CO2 FORCING on North American monsoon moisture surges. J. Clim. 31, 7949–7968 (2018).
    ADS  Article  Google Scholar 

    53.
    Pascale, S., Carvalho, L. M. V., Adams, D. K., Castro, C. L. & Cavalcanti, I. F. A. Current and future variations of the monsoons of the Americas in a warming climate. Curr. Clim. Change Rep. 5, 125–144. https://doi.org/10.1007/s40641-019-00135-w (2019).
    Article  Google Scholar 

    54.
    Abatzoglou, J. T. & Kolden, C. A. Climate change in Western US Deserts: Potential for increased wildfire and invasive annual grasses. Rangeland Ecol. Manag. 64, 471–478. https://doi.org/10.2111/rem-d-09-00151.1 (2011).
    Article  Google Scholar 

    55.
    Poulin, J., Sakai, A. K., Weller, S. G. & Nguyen, T. Phenotypic plasticity, precipitation, and invasiveness in the fire-promoting grass Pennisetum setaceum (Poaceae). Am J Bot 94, 533–541. https://doi.org/10.3732/ajb.94.4.533 (2007).
    Article  PubMed  Google Scholar 

    56.
    Goergen, E. & Daehler, C. C. Factors affecting seedling recruitment in an invasive grass (Pennisetum setaceum) and a native grass (Heteropogon contortus) in the Hawaiian Islands. Plant Ecol 161, 147–156. https://doi.org/10.1023/a:1020368719136 (2002).
    Article  Google Scholar 

    57.
    Eschtruth, A. K. & Battles, J. J. Assessing the relative importance of disturbance, herbivory, diversity, and propagule pressure in exotic plant invasion. Ecol Monogr 79, 265–280. https://doi.org/10.1890/08-0221.1 (2009).
    Article  Google Scholar 

    58.
    Klinger, R. & Brooks, M. Alternative pathways to landscape transformation: Invasive grasses, burn severity and fire frequency in arid ecosystems. J Ecol 105, 1521–1533. https://doi.org/10.1111/1365-2745.12863 (2017).
    Article  Google Scholar 

    59.
    Brooks, M. L. et al. Effects of invasive alien plants on fire regimes. Bioscience 54, 677–688 (2004).
    Article  Google Scholar 

    60.
    D’Antonio, C. M. & Vitousek, P. M. Biological invasions by exotic grasses, the grass/fire cycle, and global change. Annu Rev Ecol Syst 23, 63–87 (1992).
    Article  Google Scholar 

    61.
    Barnosky, A. D. et al. Approaching a state shift in Earth’s biosphere. Nature 486, 52. https://doi.org/10.1038/nature11018 (2012).
    ADS  CAS  Article  PubMed  Google Scholar  More

  • in

    Investigating the impact of captivity and domestication on limb bone cortical morphology: an experimental approach using a wild boar model

    1.
    Magny, M. Aux racines de l’Anthropocène: une crise écologique reflet d’une crise de l’homme (2019).
    2.
    Turcotte, M. M., Araki, H., Karp, D. S., Poveda, K. & Whitehead, S. R. The eco-evolutionary impacts of domestication and agricultural practices on wild species. Philos. Trans. R. Soc. B Biol. Sci. 372, 20160033 (2017).
    Article  Google Scholar 

    3.
    Vigne, J.-D. The origins of animal domestication and husbandry: A major change in the history of humanity and the biosphere. C. R. Biol. 334, 171–181 (2011).
    Article  Google Scholar 

    4.
    Vigne, J.-D. Early domestication and farming: What should we know or do for a better understanding?. Anthropozoologica 50, 123–150 (2015).
    Article  Google Scholar 

    5.
    Zeder, M. A. Archaeological approaches to documenting animal domestication. Doc. Domest. New Genet. Archaeol. Paradig. 666, 171–180 (2006).
    Google Scholar 

    6.
    Darwin, C. The Variation of Animals and Plants Under Domestication (John Murray, Albermale, 1868).
    Google Scholar 

    7.
    Belyaev, D. K., Plyusnina, I. Z. & Trut, L. N. Domestication in the silver fox (Vulpes fulvus Desm): Changes in physiological boundaries of the sensitive period of primary socialization. Appl. Anim. Behav. Sci. 13, 359–370 (1985).
    Article  Google Scholar 

    8.
    Belyaev, D. K. et al. Destabilizing selection as a factor in domestication. J. Hered. 70, 301–308 (1979).
    CAS  Article  Google Scholar 

    9.
    Trut, L. N. Early canid domestication: The farm-fox experiment: Foxes bred for tamability in a 40-year experiment exhibit remarkable transformations that suggest an interplay between behavioral genetics and development. Am. Sci. 87, 160–169 (1999).
    Article  Google Scholar 

    10.
    Trut, L., Oskina, I. & Kharlamova, A. Animal evolution during domestication: The domesticated fox as a model. BioEssays 31, 349–360 (2009).
    Article  Google Scholar 

    11.
    Wilkins, A. S., Wrangham, R. W. & Fitch, W. T. The ‘Domestication Syndrome’ in mammals: A unified explanation based on neural crest cell behavior and genetics. Genetics 197, 795–808 (2014).
    Article  Google Scholar 

    12.
    Frantz, L. A. et al. Evidence of long-term gene flow and selection during domestication from analyses of Eurasian wild and domestic pig genomes. Nat. Genet. 47, 1141–1148 (2015).
    CAS  Article  Google Scholar 

    13.
    Marshall, F. B., Dobney, K., Denham, T. & Capriles, J. M. Evaluating the roles of directed breeding and gene flow in animal domestication. Proc. Natl. Acad. Sci. 111, 6153–6158 (2014).
    ADS  CAS  Article  Google Scholar 

    14.
    Lord, K. A., Larson, G., Coppinger, R. P. & Karlsson, E. K. The history of farm foxes undermines the animal domestication syndrome. Trends. Ecol. Evol. 35, 125 (2019).
    Article  Google Scholar 

    15.
    Clutton-Brock, J. The process of domestication. Mammal Rev. 22, 79–85 (1992).
    Article  Google Scholar 

    16.
    Clutton-Brock, J. Domesticated Animals from Early Times (British Museum (Natural History) and William Heinemann Ltd., London, 1981).
    Google Scholar 

    17.
    Schlichting, C. D. & Pigliucci, M. Phenotypic Evolution: A Reaction Norm Perspective (Sinauer Associates Incorporated, New York, 1998).
    Google Scholar 

    18.
    Pigliucci, M., Murren, C. J. & Schlichting, C. D. Phenotypic plasticity and evolution by genetic assimilation. J. Exp. Biol. 209, 2362–2367 (2006).
    Article  Google Scholar 

    19.
    Ehrlich, P. J. & Lanyon, L. E. mechanical strain and bone cell function: A review. Osteoporos. Int. 13, 688–700 (2002).
    CAS  Article  Google Scholar 

    20.
    Pearson, O. M. & Lieberman, D. E. The aging of Wolff’s “law”: Ontogeny and responses to mechanical loading in cortical bone. Am. J. Phys. Anthropol. 125, 63–99 (2004).
    Article  Google Scholar 

    21.
    Pöllath, N., Schafberg, R. & Peters, J. Astragalar morphology: Approaching the cultural trajectories of wild and domestic sheep applying Geometric Morphometrics. J. Archaeol. Sci. Rep. 23, 810–821 (2019).
    Google Scholar 

    22.
    Drew, I. M., Perkins, D. Jr. & Daly, P. Prehistoric domestication of animals: Effects on bone structure. Science 171, 280–282 (1971).
    ADS  CAS  Article  Google Scholar 

    23.
    Mainland, I., Schutkowski, H. & Thomson, A. F. Macro-and micromorphological features of lifestyle differences in pigs and wild boar. Anthropozoologica 42, 89–106 (2007).
    Google Scholar 

    24.
    Scheidt, A., Wölfer, J. & Nyakatura, J. A. The evolution of femoral cross-sectional properties in sciuromorph rodents: Influence of body mass and locomotor ecology. J. Morphol. 280, 1156–1169 (2019).
    PubMed  Google Scholar 

    25.
    Kilbourne, B. M. & Hutchinson, J. R. Morphological diversification of biomechanical traits: mustelid locomotor specializations and the macroevolution of long bone cross-sectional morphology. BMC Evol. Biol. 19, 1–16 (2019).
    Article  Google Scholar 

    26.
    Parsi-Pour, P. & Kilbourne, B. M. Functional morphology and morphological diversification of hind limb cross-sectional traits in mustelid mammals. Integr. Org. Biol. 2, obz032 (2020).
    Article  Google Scholar 

    27.
    Houssaye, A. & Botton-Divet, L. From land to water: Evolutionary changes in long bone microanatomy of otters (Mammalia: Mustelidae). Biol. J. Linn. Soc. 125, 240–249 (2018).
    Article  Google Scholar 

    28.
    Ruff, C. B. Biomechanical analyses of archaeological human skeletons. Biol. Anthropol. Hum. Skelet. Second Ed. 2, 183–206 (2007).
    Google Scholar 

    29.
    Henderson, C. Subsistence strategy changes: The evidence of entheseal changes. HOMO J. Comp. Hum. Biol. 64, 491–508 (2013).
    CAS  Article  Google Scholar 

    30.
    Jurmain, R., Cardoso, F. A., Henderson, C. & Villotte, S. Bioarchaeology’s Holy Grail: The reconstruction of activity. Companion Paleopathol. 666, 531–552 (2011).
    Google Scholar 

    31.
    Niinimäki, S. The relationship between musculoskeletal stress markers and biomechanical properties of the humeral diaphysis. Am. J. Phys. Anthropol. 147, 618–628 (2012).
    Article  Google Scholar 

    32.
    Villotte, S. & Knüsel, C. J. Understanding entheseal changes: Definition and life course changes. Int. J. Osteoarchaeol. 23, 135–146 (2013).
    Article  Google Scholar 

    33.
    Bayle, P. et al. Three-dimensional imaging and quantitative characterization of human fossil remains. Examples from the NESPOS database. Pleistocene Databases Acquis. Storing Shar. Mettmann Wiss. Schriften Neanderthal Mus. 4, 29–46 (2011).
    Google Scholar 

    34.
    Bondioli, L. et al. Morphometric maps of long bone shafts and dental roots for imaging topographic thickness variation. Am. J. Phys. Anthropol. 142, 328–334 (2010).
    Google Scholar 

    35.
    Bondioli, L. et al. Technical note: Morphometric maps of long bone shafts and dental roots for imaging topographic thickness variation. Am. J. Phys. Anthropol. 142, 328–334 (2010).
    Google Scholar 

    36.
    Cazenave, M. et al. Inner structural organization of the distal humerus in Paranthropus and Homo. C.R. Palevol 16, 521–532 (2017).
    Article  Google Scholar 

    37.
    Morimoto, N., De León, M. S. P. & Zollikofer, C. P. Exploring femoral diaphyseal shape variation in wild and captive chimpanzees by means of morphometric mapping: A test of Wolff’s law. Anat. Rec. Adv. Integr. Anat. Evol. Biol. 294, 589–609 (2011).
    Article  Google Scholar 

    38.
    Puymerail, L. The functionally-related signatures characterizing the endostructural organisation of the femoral shaft in modern humans and chimpanzee. C.R. Palevol 12, 223–231 (2013).
    Article  Google Scholar 

    39.
    Puymerail, L. et al. Structural analysis of the Kresna 11 Homo erectus femoral shaft (Sangiran, Java). J. Hum. Evol. 63, 741–749 (2012).
    Article  Google Scholar 

    40.
    Rabey, K. N. et al. Locomotor activity influences muscle architecture and bone growth but not muscle attachment site morphology. J. Hum. Evol. 78, 91–102 (2015).
    Article  Google Scholar 

    41.
    Wallace, I. J., Winchester, J. M., Su, A., Boyer, D. M. & Konow, N. Physical activity alters limb bone structure but not entheseal morphology. J. Hum. Evol. 107, 14–18 (2017).
    Article  Google Scholar 

    42.
    Zumwalt, A. A new method for quantifying the complexity of muscle attachment sites. Anat. Rec. Part B New Anat. Off. Publ. Am. Assoc. Anat. 286, 21–28 (2005).
    Google Scholar 

    43.
    Karakostis, F. A., Wallace, I. J., Konow, N. & Harvati, K. Experimental evidence that physical activity affects the multivariate associations among muscle attachments (entheses). J. Exp. Biol. 222, jeb213058 (2019).
    Article  Google Scholar 

    44.
    Hecker, H. M. Domestication revisited: Its implications for faunal analysis. J. Field Archaeol. 9, 217–236 (1982).
    Google Scholar 

    45.
    Lyman, R. L. & Lyman, C. Vertebrate Taphonomy (Cambridge University Press, Cambridge, 1994).
    Google Scholar 

    46.
    Zhou, X. L., Xu, Y. C., Yang, S. H., Hua, Y. & Stott, P. Effectiveness of femur bone indexes to segregate wild from captive minks, mustela vison, and forensic implications for small mammals. J. Forensic Sci. 60, 72–75 (2015).
    Article  Google Scholar 

    47.
    Barone, R. Anatomie comparée des mammifères domestiques, Vol. 3 (Vigot, Paris, 1976).
    Google Scholar 

    48.
    Wood, S. N. Thin plate regression splines. J. R Stat. Soc. Ser. B Stat. Methodol. 65, 95–114 (2003).
    MathSciNet  MATH  Article  Google Scholar 

    49.
    Wood, S. N. Generalized Additive Models: An Introduction with R (CRC Press, Boca Raton, 2017).
    Google Scholar 

    50.
    Grant, A. The use of tooth wear as a guide to the age of domestic ungulates. In Ageing and Sexing Animal Bones from Archaeological Sites (eds Wilson, B. et al.) 91–108 (B.A.R, New York, 1982).
    Google Scholar 

    51.
    Horard-Herbin, M.-P. Le village celtique des Arènes à Levroux. L’élevage et les productions animales dans l’économie de la fin du second âge du Fer-Levroux 4. vol. 12 (Fédération pour l’édition de la Revue archéologique du Centre de la France, Paris, 1997).

    52.
    Koolstra, J. H., van Eijden, T. M. G. J., Weijs, W. A. & Naeije, M. A three-dimensional mathematical model of the human masticatory system predicting maximum possible bite forces. J. Biomech. 21, 563–576 (1988).
    CAS  Article  Google Scholar 

    53.
    Bookstein, F. L. Morphometric Tools for Landmark Data (Cambridge University Press, New York, 1991).
    Google Scholar 

    54.
    Rohlf, F. J. & Corti, M. Use of two-block partial least-squares to study covariation in shape. Syst. Biol. 49, 740–753 (2000).
    CAS  Article  Google Scholar 

    55.
    Mitteroecker, P. & Bookstein, F. Linear discrimination, ordination, and the visualization of selection gradients in modern morphometrics. Evol. Biol. 38, 100–114 (2011).
    Article  Google Scholar 

    56.
    Adams, D. C. & Otárola-Castillo, E. geomorph: An R package for the collection and analysis of geometric morphometric shape data. Methods Ecol. Evol. 4, 393–399 (2013).
    Article  Google Scholar 

    57.
    Schlager, S. Chapter 9—Morpho and Rvcg—shape analysis in R: R-packages for geometric morphometrics, shape analysis and surface manipulations. In Statistical Shape and Deformation Analysis (eds Zheng, G. et al.) 217-256 (Academic Press, London, 2017). https://doi.org/10.1016/B978-0-12-810493-4.00011-0.
    Google Scholar 

    58.
    Carter, D. R., Van der Meulen, M. C. H. & Beaupré, G. S. Mechanical factors in bone growth and development. Bone 18, S5–S10 (1996).
    Article  Google Scholar 

    59.
    Gosman, J. H., Stout, S. D. & Larsen, C. S. Skeletal biology over the life span: A view from the surfaces. Am. J. Phys. Anthropol. 146, 86–98 (2011).
    Article  Google Scholar 

    60.
    van Der Meulen, M. C., Beaupre, G. S. & Carter, D. R. Mechanobiologic influences in long bone cross-sectional growth. Bone 14, 635–642 (1993).
    Article  Google Scholar 

    61.
    O’Regan, H. J. & Kitchener, A. C. The effects of captivity on the morphology of captive, domesticated and feral mammals. Mammal Rev. 35, 215–230 (2005).
    Article  Google Scholar 

    62.
    Kimura, T. & Hamada, Y. Growth of wild and laboratory born chimpanzees. Primates 37, 237–251 (1996).
    Article  Google Scholar 

    63.
    Armitage, P. L. Jawbone of a South American monkey from Brooks Wharf, City of London (London Archaeologist Association, London, 1983).
    Google Scholar 

    64.
    Felson, D. T., Zhang, Y., Hannan, M. T. & Anderson, J. J. Effects of weight and body mass index on bone mineral density in men and women: The Framingham study. J. Bone Miner. Res Off. J. Am. Soc. Bone Miner. Res. 8, 567–573 (1993).
    CAS  Article  Google Scholar 

    65.
    Ravn, P. et al. Low body mass index is an important risk factor for low bone mass and increased bone loss in early postmenopausal women Early Postmenopausal Intervention Cohort (EPIC) study group. J. Bone Miner. Res Off. J. Am. Soc. Bone Miner. Res. 14, 1622–1627 (1999).
    CAS  Article  Google Scholar 

    66.
    Niinimäki, S. & Salmi, A.-K. Entheseal changes in free-ranging versus zoo reindeer—Observing activity status of reindeer. Int. J. Osteoarchaeol. 26, 314–323 (2016).
    Article  Google Scholar 

    67.
    Harbers, H. et al. The mark of captivity: Plastic responses in the ankle bone of a wild ungulate (Sus scrofa). R. Soc. Open Sci. 7, 192039 (2020).
    ADS  Article  Google Scholar 

    68.
    Michopoulou, E., Nikita, E. & Valakos, E. D. Evaluating the efficiency of different recording protocols for entheseal changes in regards to expressing activity patterns using archival data and cross-sectional geometric properties. Am. J. Phys. Anthropol. 158, 557–568 (2015).
    Article  Google Scholar 

    69.
    Milella, M., Giovanna Belcastro, M., Zollikofer, C. P. & Mariotti, V. The effect of age, sex, and physical activity on entheseal morphology in a contemporary Italian skeletal collection. Am. J. Phys. Anthropol. 148, 379–388 (2012).
    Article  Google Scholar 

    70.
    Seeman, E. Bone quality: The material and structural basis of bone strength. J. Bone Miner. Metab. 26, 1–8 (2008).
    Article  Google Scholar 

    71.
    Wilkinson, S. et al. Signatures of diversifying selection in European pig breeds. PLOS Genet. 9, e1003453 (2013).
    CAS  Article  Google Scholar 

    72.
    Pelletier, F. & Coltman, D. W. Will human influences on evolutionary dynamics in the wild pervade the Anthropocene?. BMC Biol. 16, 7 (2018).
    Article  Google Scholar 

    73.
    O’Higgins, P. et al. Combining geometric morphometrics and functional simulation: An emerging toolkit for virtual functional analyses. J. Anat. 218, 3–15 (2011).
    Article  Google Scholar  More

  • in

    Spatial distribution of stygobitic crustacean harpacticoids at the boundaries of groundwater habitat types in Europe

    1.
    Griebler, C., Avramov, M. & Hose, G. Groundwater Ecosystems and Their Services: Current Status and Potential Risks. In Atlas of Ecosystem Services (eds Schröter, M. et al.) 197–203 (Springer, Berlin, 2019).
    Google Scholar 
    2.
    Di Lorenzo, T., Cifoni, M., Lombardo, P., Fiasca, B. & Galassi, D. M. P. Ammonium threshold values for groundwater quality in the EU may not protect groundwater fauna: evidence from an alluvial aquifer in Italy. Hydrobiologia 743, 139–150 (2015).
    Article  CAS  Google Scholar 

    3.
    Banks, E., Simmons, C., Love, A. & Shand, P. Assessing spatial and temporal connectivity between surface water and groundwater in a regional catchment: Implications for regional scale water quantity and quality. J. Hydrol. 404, 30–49 (2011).
    ADS  CAS  Article  Google Scholar 

    4.
    Di Lorenzo, T., Stoch, F. & Galassi, D. M. P. Incorporating the hyporheic zone within the river discontinuum: longitudinal patterns of subsurface copepod assemblages in an Alpine stream. Limnologica 43, 288–296 (2013).
    Article  CAS  Google Scholar 

    5.
    Hose, G. C. & Stumpp, C. Architects of the underworld: bioturbation by groundwater invertebrates influences aquifer hydraulic properties. Aquat. Sci. 81, 20 (2019).
    Article  Google Scholar 

    6.
    Di Lorenzo, T. & Galassi, D. M. P. Effect of temperature rising on the stygobitic crustacean species Diacyclops belgicus: Does global warming affect groundwater populations?. Water 9, 951 (2017).
    ADS  Article  CAS  Google Scholar 

    7.
    Strona, G. et al. AQUALIFE software: a new tool for a standardized ecological assessment of groundwater dependent ecosystems. Water 11, 2574 (2019).
    Article  Google Scholar 

    8.
    Mammola, S. et al. Scientists’ warning on the conservation of subterranean ecosystems. Bioscience 69, 641–650 (2019).
    Article  Google Scholar 

    9.
    Castellarini, F., Malard, F., Dole-Olivier, M.-J. & Gibert, J. Modelling the distribution of stygobionts in the Jura Mountains (eastern France). Implications for the protection of ground waters. Divers. Distrib. 13, 213–224 (2007).
    Article  Google Scholar 

    10.
    Deharveng, L. et al. Groundwater biodiversity in Europe. Freshw. Biol. 54, 709–726 (2009).
    Article  Google Scholar 

    11.
    Fattorini, S., Fiasca, B., Di Lorenzo, T., Di Cicco, M. & Galassi, D. M. P. A new protocol for assessing the conservation priority of groundwater dependent ecosystems. Aquat. Conserv. 30, 1483–1504 (2020).
    Article  Google Scholar 

    12.
    Pipan, T., Culver, D. C., Papi, F. & Kozel, P. Partitioning diversity in subterranean invertebrates: the epikarst fauna of Slovenia. PLoS ONE 13, e0195991 (2018).
    Article  CAS  Google Scholar 

    13.
    Iannella, M. et al. Jumping into the grids: mapping biodiversity hotspots in groundwater habitat types across Europe. Ecography 43, 1–17. https://doi.org/10.1111/ecog.05323 (2020).
    Article  Google Scholar 

    14.
    Cantonati, M. et al. Characteristics, main impacts, and stewardship of natural and artificial freshwater environments: consequences for biodiversity conservation. Water 12, 260 (2020).
    Article  Google Scholar 

    15.
    Galassi, D. M. P., Huys, R. & Reid, J. W. Diversity, ecology and evolution of groundwater copepods. Freshw. Biol. 54, 691–708 (2009).
    Article  Google Scholar 

    16.
    Galassi, D. M. P. Groundwater copepods: diversity patterns over ecological and evolutionary scales. Hydrobiologia 453, 227–253 (2001).
    Article  Google Scholar 

    17.
    Fiasca, B. et al. The dark side of springs: what drives small-scale spatial patterns of subsurface meiofaunal assemblages. J. Limnol. 73, 71–80 (2014).
    Article  Google Scholar 

    18.
    Galassi, D. M. P. et al. Earthquakes trigger the loss of groundwater biodiversity. Sci. Rep. 4, 6273 (2014).
    CAS  Article  Google Scholar 

    19.
    Fattorini, S., Di Lorenzo, T. & Galassi, D. M. P. Earthquake impacts on microcrustacean communities inhabiting groundwater-fed springs alter species-abundance distribution patterns. Sci. Rep. 8, 1501 (2018).
    ADS  Article  CAS  Google Scholar 

    20.
    Boxshall, G. A., Kihara, T. C. & Huys, R. Collecting and processing non-planktonic copepods. J. Crustacean Biol. 36, 576–583 (2016).
    Article  Google Scholar 

    21.
    Korbel, K. L., Stephenson, S. & Hose, G. C. Sediment size influences habitat selection and use by groundwater macrofauna and meiofauna. Aquat. Sci. 81, 39 (2019).
    Article  CAS  Google Scholar 

    22.
    Giere, O. Meiobenthology: The Microscopic motile Fauna of Aquatic Sediments 2nd edn. (Springer, Berlin, 2009).
    Google Scholar 

    23.
    Galassi, D. M. P. et al. Groundwater biodiversity in a chemoautotrophic cave ecosystem: how geochemistry regulates microcrustacean community structure. Aquat. Ecol. 51, 75–90 (2017).
    CAS  Article  Google Scholar 

    24.
    Lamoreux, J. Stygobites are more wide-ranging than troglobites. J. Cave Karst. Stud. 66, 18–19 (2004).
    Google Scholar 

    25.
    Kubisch, A., Holt, R. D., Poethke, H. J. & Fronhofer, E. A. Where am I and why? Synthesizing range biology and the eco-evolutionary dynamics of dispersal. Oikos 123, 5–22 (2014).
    Article  Google Scholar 

    26.
    Strayer, D. L., Power, M. E., Fagan, W. F., Pickett, S. T. & Belnap, J. A classification of ecological boundaries. Bioscience 53, 723–729 (2003).
    Article  Google Scholar 

    27.
    Mazzucco, R., Doebeli, M. & Dieckmann, U. The influence of habitat boundaries on evolutionary branching along environmental gradients. Evol. Ecol. 32, 563–585 (2018).
    Article  Google Scholar 

    28.
    Potts, J. R., Hillen, T. & Lewis, M. A. The, “edge effect” phenomenon: deriving population abundance patterns from individual animal movement decisions. Theor. Ecol. 9, 233–247 (2016).
    Article  Google Scholar 

    29.
    Ries, L., Fletcher, R. J. Jr., Battin, J. & Sisk, T. D. Ecological responses to habitat edges: mechanisms, models, and variability explained. Annu. Rev. Ecol. Evol. Syst. 35, 491–522 (2004).
    Article  Google Scholar 

    30.
    Cornu, J.-F., Eme, D. & Malard, F. The distribution of groundwater habitats in Europe. Hydrogeol. J. 21, 949–960 (2013).
    ADS  Article  Google Scholar 

    31.
    Margules, C. R. & Pressey, R. L. Systematic conservation planning. Nature 405, 6783 (2000).
    Article  Google Scholar 

    32.
    Eme, D. et al. Multi-causality and spatial non-stationarity in the determinants of groundwater crustacean diversity in Europe. Ecography 38, 531–540 (2015).
    Article  Google Scholar 

    33.
    Brunetti, M., Magoga, G., Iannella, M., Biondi, M. & Montagna, M. Phylogeography and species distribution modelling of Cryptocephalus barii (Coleoptera: Chrysomelidae): is this alpine endemic species close to extinction?. ZooKeys 856, 3 (2019).
    Article  Google Scholar 

    34.
    Iannella, M., Liberatore, L. & Biondi, M. The effects of a sudden urbanization on micromammal communities: a case study of post-earthquake L’Aquila (Abruzzi Region, Italy). Ital. J. Zool. 83, 255–262 (2016).
    Article  Google Scholar 

    35.
    Shen, X. et al. Effectiveness of management zoning designed for flagship species in protecting sympatric species. Conserv. Biol. 34, 158–167 (2020).
    Article  Google Scholar 

    36.
    Zagmajster, M. et al. Geographic variation in range size and beta diversity of groundwater crustaceans: insights from habitats with low thermal seasonality. Glob. Ecol. Biogeogr. 23, 1135–1145 (2014).
    Article  Google Scholar 

    37.
    Stoch, F. & Galassi, D. M. P. Stygobiotic crustacean species richness: a question of numbers, a matter of scale. Hydrobiologia 653, 217–234 (2010).
    CAS  Article  Google Scholar 

    38.
    Stein, H. et al. Stygoregions—a promising approach to a bioregional classification of groundwater systems. Sci. Rep. 2, 673 (2012).
    Article  CAS  Google Scholar 

    39.
    Council of the European Communities. Council Directive 92/43/EEC of 21 May 1992 on the conservation of natural habitats and of wild fauna and flora. O. J. L. 206, 7–50 (1992).

    40.
    Galassi, D. M. P., Stoch, F., Fiasca, B., Di Lorenzo, T. & Gattone, E. Groundwater biodiversity patterns in the Lessinian Massif of northern Italy. Freshw. Biol. 54, 830–847 (2009).
    CAS  Article  Google Scholar 

    41.
    Rouch, R. Sur la répartition spatiale des Crustacés dans le sous-écoulement d’un ruisseau des Pyrénées. Ann. Limnol. 24, 213–234 (1988).
    Article  Google Scholar 

    42.
    Gibert, J., Malard, F., Turquin, M. J. & Laurent, R. Karst Ecosystems in the Rhône River Basin. In Subterranean Ecosystems. Ecosystems of the World (eds Wilkens, H. et al.) 533–558 (Elsevier, Amsterdam, 2000).
    Google Scholar 

    43.
    Boulton, A. J. Conservation of groundwaters and their dependent ecosystems: Integrating molecular taxonomy, systematic reserve planning and cultural values. Aquat. Conserv. 30, 1–7 (2020).
    Article  Google Scholar 

    44.
    Smith, T. B., Kark, S., Schneider, C. J., Wayne, R. K. & Moritz, C. Biodiversity hotspots and beyond: the need for preserving environmental transitions. Trends Ecol. Evol. 16, 431 (2001).
    Article  Google Scholar 

    45.
    Álvarez-Martínez, J. M. et al. Modelling the area of occupancy of habitat types with remote sensing. Methods Ecol. Evol. 9, 580–593 (2018).
    Article  Google Scholar 

    46.
    Armstrong, D. P. Integrating the metapopulation and habitat paradigms for understanding broad-scale declines of species. Conserv. Biol. 19, 1402–1410 (2005).
    Article  Google Scholar 

    47.
    Myers, N., Mittermeier, R. A., Mittermeier, C. G., Da Fonseca, G. A. & Kent, J. Biodiversity hotspots for conservation priorities. Nature 403, 853–858 (2000).
    ADS  CAS  Article  Google Scholar 

    48.
    Malard, F. et al. Diversity patterns of stygobiotic crustaceans across multiple spatial scales in Europe. Freshw. Biol. 54, 756–776 (2009).
    Article  Google Scholar 

    49.
    Stoch, F. et al. Exploring copepod distribution patterns at three nested spatial scales in a spring system: Habitat partitioning and potential for hydrological bioindication. J. Limnol. 75, 1–13 (2016).
    Google Scholar 

    50.
    Di Lorenzo, T., Cipriani, D., Fiasca, B., Rusi, S. & Galassi, D. M. P. Groundwater drift monitoring as a tool to assess the spatial distribution of groundwater species into karst aquifers. Hydrobiologia 813, 137–156 (2018).
    Article  CAS  Google Scholar 

    51.
    Illies, J. Limnofauna Europaea (Fischer, Stuttgart, 1978).
    Google Scholar 

    52.
    Botosaneanu, L. Stygofauna Mundi (Brill, Leiden, 1986).
    Google Scholar 

    53.
    Knight, L. Hypogean Crustacea Recording Scheme. (Accessed 1 October 2020); https://hcrs.freshwaterlife.org (2012).

    54.
    Ruffo, S. & Stoch, F. Checklist e distribuzione della fauna italiana. (2005).

    55.
    ESRI. ArcMap 10.0. ESRI, Redlands, California (2010).

    56.
    Wang, Y. et al. Comparing the performance of approaches for testing the homogeneity of variance assumption in one-factor ANOVA models. Educ. Psychol. Meas. 77, 305–329 (2017).
    Article  Google Scholar 

    57.
    Holm, S. A simple sequentially rejective multiple test procedure. Scand. J. Stat. 6, 65–70 (1979).
    MathSciNet  MATH  Google Scholar  More