Disentangling drivers behind fungal diversity gradients along altitude and latitude
Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic
Typ dokumentu časopisecké články
Grantová podpora
21-20802M
Czech Science Foundation
CZ.02.01.01/00/22_008/0004597
Ministry of Education, Youth and Sports of the Czech Republic
PubMed
40007180
PubMed Central
PMC12138170
DOI
10.1111/nph.70012
Knihovny.cz E-zdroje
- Klíčová slova
- altitudinal and latitudinal gradients, biogeography, climate, ectomycorrhizal fungi, fungal diversity, join species distribution models, root endophytic fungi, saprotrophic fungi,
- MeSH
- Bayesova věta MeSH
- biodiverzita * MeSH
- houby * fyziologie MeSH
- mykorhiza fyziologie MeSH
- nadmořská výška * MeSH
- zeměpis MeSH
- Publikační typ
- časopisecké články MeSH
- Geografické názvy
- Evropa MeSH
Gradients in species diversity across elevations and latitudes have fascinated biologists for decades. While these gradients have been well documented for macroorganisms, there is limited consensus about their universality, shape and drivers for microorganisms, such as fungi, despite the importance of fungal diversity for ecosystem functions and services. We conducted a comprehensive survey of fungal species richness in forests across 17 elevational transects along a latitudinal gradient covering the continental scale of Europe. Diversity patterns along elevational and latitudinal gradients differed among fungal ecological guilds. Diversity of saprotrophs declined with elevation while ectomycorrhizal (ECM) fungal diversity peaked in mid-elevations. Moreover, the diversity of root endophytic fungi increased with latitude but did not change with elevation. Bayesian species distribution modeling suggests that fungal diversity is structured by deterministic rather than stochastic drivers. Importantly, ECM fungal diversity pattern persists even after accounting for the effects of environmental conditions. These results suggest that environmental conditions differentially shape the diversity of fungal guilds along elevational and latitudinal gradients, but this goes beyond soil and climatic factors in the case of ECM fungi. This study paves the way toward a better understanding of fungal diversity gradients across elevations and latitudes, with possible implications for macroecological theory, conservation and management.
Academy of Sciences and Arts of Bosnia Bistrik 7 71000 Sarajevo Bosnia and Herzegovina
Biotechnical Faculty University of Montenegro Mihaila Lalića 15 81000 Podgorica Montenegro
Department of Biosciences University of Oslo PO Box 1066 Blindern 0316 Oslo Norway
Faculty of Forestry University of Sarajevo Zagrebačka 20 71000 Sarajevo Bosnia and Herzegovina
Faculty of Science Charles University Albertov 6 Prague 128 40 Czechia
Nationalpark Harz Außenstelle Oderhaus Oderhaus 1 37444 Sankt Andreasberg Germany
Plant Pathology Unit INRAE 67 allée des chênes 84143 Montfavet France
Zobrazit více v PubMed
Adamczyk M, Hagedorn F, Wipf S, Donhauser J, Vittoz P, Rixen C, Frossard A, Theurillat J‐P, Frey B. 2019. The soil microbiome of GLORIA mountain summits in the Swiss Alps. Frontiers in Microbiology 10: 1080. PubMed PMC
Aronesty E. 2013. Comparison of sequencing utility programs. The Open Bioinformatics Journal 7: 1–8.
Bagchi R, Swinfield T, Gallery RE, Lewis OT, Gripenberg S, Narayan L, Freckleton RP. 2010. Testing the Janzen‐Connell mechanism: pathogens cause overcompensating density dependence in a tropical tree. Ecology Letters 13: 1262–1269. PubMed
Bahram M, Põlme S, Kõljalg U, Zarre S, Tedersoo L. 2012. Regional and local patterns of ectomycorrhizal fungal diversity and community structure along an altitudinal gradient in the Hyrcanian forests of northern Iran. New Phytologist 193: 465–473. PubMed
Baldrian P, Kohout P, Větrovský T. 2023. Global fungal diversity estimated from high‐throughput sequencing. In: Pöggeler S, James T, eds. The mycota. Evolution of fungi and fungal‐like organisms. Cham, Switzerland: Springer, 227–238.
Baldrian P, Větrovský T, Lepinay C, Kohout P. 2022. High‐throughput sequencing view on the magnitude of global fungal diversity. Fungal Diversity 114: 539–547.
Barton K. 2009. mumin: multi‐model inference . [WWW document] URL http://r‐forge.r‐project.org/projects/mumin/ [accessed 14 February 2025].
Bates D, Mächler M, Bolker B, Walker S. 2015. Fitting linear mixed‐effects models using lme4. Journal of Statistical Software 67: 1–48.
Bhople P, Samad A, Šišić A, Antonielli L, Sessitsch A, Keiblinger K, Djukic I, Zehetner F, Zechmeister‐Boltenstern S, Joergensen RG et al. 2022. Variations in fungal community structure along elevation gradients in contrasting Austrian Alpine ecosystems. Applied Soil Ecology 177: 104508.
Breheny P, Burchett W. 2017. Visualization of regression models using visreg . The R Journal 9: 56.
Brown JH. 2001. Mammals on mountainsides: elevational patterns of diversity. Global Ecology and Biogeography 10: 101–109.
Bueno CG, Gerz M, Moora M, Leon D, Gomez‐Garcia D, de Leon DG, Font X, Al‐Quraishy S, Hozzein WN, Zobel M. 2021. Distribution of plant mycorrhizal traits along an elevational gradient does not fully mirror the latitudinal gradient. Mycorrhiza 31: 149–159. PubMed
Bueno CG, Moora M, Gerz M, Davison J, Öpik M, Pärtel M, Helm A, Ronk A, Kühn I, Zobel M. 2017. Plant mycorrhizal status, but not type, shifts with latitude and elevation in Europe. Global Ecology and Biogeography 26: 690–699.
Chambers SM, Curlevski NJA, Cairney JWG. 2008. Ericoid mycorrhizal fungi are common root inhabitants of non‐Ericaceae plants in a south‐eastern Australian sclerophyll forest. FEMS Microbiology Ecology 65: 263–270. PubMed
Chao A, Gotelli NJ, Hsieh TC, Sander EL, Ma KH, Colwell RK, Ellison AM. 2014. Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecological Monographs 84: 45–67.
Clemmensen KE, Bahr A, Ovaskainen O, Dahlberg A, Ekblad A, Wallander H, Stenlid J, Finlay RD, Wardle DA, Lindahl BD. 2013. Roots and associated fungi drive long‐term carbon sequestration in boreal forest. Science 339: 1615–1618. PubMed
Clemmensen KE, Finlay RD, Dahlberg A, Stenlid J, Wardle DA, Lindahl BD. 2015. Carbon sequestration is related to mycorrhizal fungal community shifts during long‐term succession in boreal forests. New Phytologist 205: 1525–1536. PubMed
Coince A, Cordier T, Lengellé J, Defossez E, Vacher C, Robin C, Buée M, Marçais B. 2014. Leaf and root‐associated fungal assemblages do not follow similar elevational diversity patterns. PLoS ONE 9: e100668. PubMed PMC
Colwell RK, Gotelli NJ, Ashton LA, Beck J, Brehm G, Fayle TM, Fiedler K, Forister ML, Kessler M, Kitching RL et al. 2016. Midpoint attractors and species richness: modelling the interaction between environmental drivers and geometric constraints. Ecology Letters 19: 1009–1022. PubMed
Colwell RK, Rahbek C, Gotelli NJ. 2004. The mid‐domain effect and species richness patterns: what have we learned so far? The American Naturalist 163: E1–E23. PubMed
Correia M, Espelta JM, Morillo JA, Pino J, Rodríguez‐Echeverría S. 2021. Land‐use history alters the diversity, community composition and interaction networks of ectomycorrhizal fungi in beech forests. Journal of Ecology 109: 2856–2870.
Crowther TW, Boddy L, Hefin Jones T. 2012. Functional and ecological consequences of saprotrophic fungus–grazer interactions. The ISME Journal 6: 1992–2001. PubMed PMC
Davis KT, Dobrowski SZ, Higuera PE, Holden ZA, Veblen TT, Rother MT, Parks SA, Sala A, Maneta MP. 2019. Wildfires and climate change push low‐elevation forests across a critical climate threshold for tree regeneration. Proceedings of the National Academy of Sciences, USA 116: 6193–6198. PubMed PMC
Edgar RC. 2013. Uparse: highly accurate OTU sequences from microbial amplicon reads. Nature Methods 10: 996–998. PubMed
Forster JR. 1778. Observations made during a voyage round the world [in H.M.S. Resolution] on physical geography, natural history, and ethic philosophy, especially on. London, UK: G. Robinson.
Garnier S, Ross N, Rudis B, Sciaini M, Camargo AP, Scherer C. 2024. viridis: colorblind‐friendly color maps for R . [WWW document] URL https://cran.r‐project.org/web/packages/viridis/index.html [accessed 14 February 2025]
Geml J, Arnold AE, Semenova‐Nelsen TA, Nouhra ER, Drechsler‐Santos ER, Góes‐Neto A, Morgado LN, Ódor P, Hegyi B, Oriol G et al. 2022. Community dynamics of soil‐borne fungal communities along elevation gradients in neotropical and palaeotropical forests. Molecular Ecology 31: 2044–2060. PubMed
Geml J, Morgado LN, Semenova‐Nelsen TA, Schilthuizen M. 2017. Changes in richness and community composition of ectomycorrhizal fungi among altitudinal vegetation types on Mount Kinabalu in Borneo. New Phytologist 215: 454–468. PubMed
Gómez‐Hernández M, Williams‐Linera G, Guevara R, Lodge D. 2011. Patterns of macromycete community assemblage along an elevation gradient: options for fungal gradient and metacommunity analyse. Biodiversity and Conservation 21: 1–22.
Hawkins H‐J, Cargill RIM, Van Nuland ME, Hagen SC, Field KJ, Sheldrake M, Soudzilovskaia NA, Kiers ET. 2023. Mycorrhizal mycelium as a global carbon pool. Current Biology 33: R560–R573. PubMed
Hendershot JN, Read QD, Henning JA, Sanders NJ, Classen AT. 2017. Consistently inconsistent drivers of microbial diversity and abundance at macroecological scales. Ecology 98: 1757–1763. PubMed
Hillebrand H. 2004. On the generality of the latitudinal diversity gradient. The American Naturalist 163: 192–211. PubMed
Hsieh TC, Ma KH, Chao A. 2016. inext: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods in Ecology and Evolution 7: 1451–1456.
von Humboldt A, Bonpland A. 2013. Essay on the geography of plants (STJT by S Romanowski, Tran.). Chicago, IL, USA: University of Chicago Press.
Ihrmark K, Bodeker ITM, Cruz‐Martinez K, Friberg H, Kubartova A, Schenck J, Strid Y, Stenlid J, Brandstrom‐Durling M, Clemmensen KE et al. 2012. New primers to amplify the fungal ITS2 region – evaluation by 454‐sequencing of artificial and natural communities. FEMS Microbiology Ecology 82: 666–677. PubMed
Jumpponen A, Trappe JM. 1998. Dark septate endophytes: a review of facultative biotrophic root‐colonizing fungi. New Phytologist 140: 295–310. PubMed
Karger DN, Conrad O, Böhner J, Kawohl T, Kreft H, Soria‐Auza RW, Zimmermann NE, Linder HP, Kessler M. 2017. Climatologies at high resolution for the earth's land surface areas. Scientific Data 4: 170122. PubMed PMC
Kohout P. 2017. Biogeography of ericoid mycorrhiza. In: Tedersoo L, ed. Ecological studies. Biogeography of mycorrhizal symbiosis. Cham, Switzerland: Springer, 179–193.
Kõljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AFS, Bahram M, Bates ST, Bruns TD, Bengtsson‐Palme J, Callaghan TM et al. 2013. Towards a unified paradigm for sequence‐based identification of fungi. Molecular Ecology 22: 5271–5277. PubMed
Kuhn M. 2008. Building predictive models in R using the caret package. Journal of Statistical Software 28: 1–26.
Kuznetsova A, Brockhoff PB, Christensen RHB. 2017. lmertest package: tests in linear mixed effects models. Journal of Statistical Software 82: 1–26.
Leopold DR. 2016. Ericoid fungal diversity: challenges and opportunities for mycorrhizal research. Fungal Ecology 24: 114–123.
Liang J, Gamarra JGP, Picard N, Zhou M, Pijanowski B, Jacobs DF, Reich PB, Crowther TW, Nabuurs G‐J, de‐Miguel S et al. 2022. Co‐limitation towards lower latitudes shapes global forest diversity gradients. Nature Ecology & Evolution 6: 1423–1437. PubMed
Liaw A, Wiener M. 2001. Classification and regression by randomforest . Forest 23. [WWW document] URL https://cran.r-project.org/web/packages/randomForest/index.html [accessed 18 February 2025].
Lomolino MV. 2001. Elevation gradients of species‐density: historical and prospective views. Global Ecology and Biogeography 10: 3–13.
Lukešová T, Kohout P, Větrovský T, Vohník M. 2015. The potential of dark septate endophytes to form root symbioses with ectomycorrhizal and ericoid mycorrhizal middle European forest plants. PLoS ONE 10: e0124752. PubMed PMC
Luo Y‐H, Ma L‐L, Seibold S, Cadotte MW, Burgess KS, Tan S‐L, Ye L‐J, Zheng W, Zou J‐Y, Chen Z‐F et al. 2023. The diversity of mycorrhiza‐associated fungi and trees shapes subtropical mountain forest ecosystem functioning. Journal of Biogeography 50: 715–729.
Mannion PD, Upchurch P, Benson RBJ, Goswami A. 2014. The latitudinal biodiversity gradient through deep time. Trends in Ecology & Evolution 29: 42–50. PubMed
Martino E, Morin E, Grelet G‐A, Kuo A, Kohler A, Daghino S, Barry KW, Cichocki N, Clum A, Dockter RB et al. 2018. Comparative genomics and transcriptomics depict ericoid mycorrhizal fungi as versatile saprotrophs and plant mutualists. New Phytologist 217: 1213–1229. PubMed
Martinović T, Odriozola I, Mašínová T, Doreen Bahnmann B, Kohout P, Sedlák P, Merunková K, Větrovský T, Tomšovský M, Ovaskainen O et al. 2021. Temporal turnover of the soil microbiome composition is guild‐specific. Ecology Letters 24: 2726–2738. PubMed
Mikryukov V, Dulya O, Zizka A, Bahram M, Hagh‐Doust N, Anslan S, Prylutskyi O, Delgado‐Baquerizo M, Maestre FT, Nilsson H et al. 2023. Connecting the multiple dimensions of global soil fungal diversity. Science Advances 9: eadj8016. PubMed PMC
Miyamoto Y, Nakano T, Hattori M, Nara K. 2014. The mid‐domain effect in ectomycorrhizal fungi: range overlap along an elevation gradient on Mount Fuji, Japan. The ISME Journal 8: 1739–1746. PubMed PMC
Moravcová A, Barbi F, Brabcová V, Cajthaml T, Martinović T, Soudzilovskaia N, Vlk L, Baldrian P, Kohout P. 2023. Climate‐driven shifts in plant and fungal communities can lead to topsoil carbon loss in alpine ecosystems. FEMS Microbiology Ecology 99: fiad041. PubMed
Netherway T, Bengtsson J, Buegger F, Fritscher J, Oja J, Pritsch K, Hildebrand F, Krab EJ, Bahram M. 2024. Pervasive associations between dark septate endophytic fungi with tree root and soil microbiomes across Europe. Nature Communications 15: 159. PubMed PMC
Netherway T, Bengtsson J, Krab EJ, Bahram M. 2021. Biotic interactions with mycorrhizal systems as extended nutrient acquisition strategies shaping forest soil communities and functions. Basic and Applied Ecology 50: 25–42.
Ni Y, Yang T, Zhang K, Shen C, Chu H. 2018. Fungal communities along a small‐scale elevational gradient in an alpine tundra are determined by soil carbon nitrogen ratios. Frontiers in Microbiology 9: 1815. PubMed PMC
Nilsson RH, Veldre V, Hartmann M, Unterseher M, Amend A, Bergsten J, Ryberg M, Jumpponen A, Abarenkov K, Kristiansson E. 2010. An open source software package for automated extraction of ITS1 and ITS2 from fungal ITS sequences for use in high‐throughput community assays and molecular ecology. Fungal Ecology 3: 284–287.
Niskanen T, Lücking R, Dahlberg A, Gaya E, Suz LM, Mikryukov V, Liimatainen K, Druzhinina I, Westrip JRS, Mueller GM et al. 2023. Pushing the frontiers of biodiversity research: unveiling the global diversity, distribution, and conservation of fungi. Annual Review of Environment and Resources 48: 149–176.
Odriozola I, Martinović T, Mašínová T, Bahnmann BD, Machac A, Sedlák P, Tomšovský M, Baldrian P. 2024. The spatial patterns of community composition, their environmental drivers and their spatial scale dependence vary markedly between fungal ecological guilds. Global Ecology and Biogeography 33: 173–188.
Ogwu MC, Takahashi K, Dong K, Song H‐K, Moroenyane I, Waldman B, Adams JM. 2019. Fungal elevational rapoport pattern from a high mountain in Japan. Scientific Reports 9: 6570. PubMed PMC
Oksanen J. 2007. vegan: community ecology package. R package v.1.8‐5. [WWW document] URL http://www.cran.r‐project.org
Ovaskainen O, Abrego N. 2020. Joint species distribution modelling: with applications in R. Cambridge, UK: Cambridge University Press.
Perotto S, Daghino S, Martino E. 2018. Ericoid mycorrhizal fungi and their genomes: another side to the mycorrhizal symbiosis? New Phytologist 220: 1141–1147. PubMed
Peters MK, Hemp A, Appelhans T, Becker JN, Behler C, Classen A, Detsch F, Ensslin A, Ferger SW, Frederiksen SB et al. 2019. Climate‐land‐use interactions shape tropical mountain biodiversity and ecosystem functions. Nature 568: 88–92. PubMed
Polme S, Abarenkov K, Henrik Nilsson R, Lindahl BD, Clemmensen KE, Kauserud H, Nguyen N, Kjoller R, Bates ST, Baldrian P et al. 2021. FungalTraits: a user‐friendly traits database of fungi and fungus‐like stramenopiles. Fungal Diversity 105: 1–16.
Qin C, Pellitier PT, Van Nuland ME, Peay KG, Zhu K. 2023. Niche modelling predicts that soil fungi occupy a precarious climate in boreal forests. Global Ecology and Biogeography 32: 1127–1139.
R Core Team . 2022. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
Rahbek C. 2005. The role of spatial scale and the perception of large‐scale species‐richness patterns. Ecology Letters 8: 224–239.
Sabatini FM, Jiménez‐Alfaro B, Jandt U, Chytrý M, Field R, Kessler M, Lenoir J, Schrodt F, Wiser SK, Arfin Khan MAS et al. 2022. Global patterns of vascular plant alpha diversity. Nature Communications 13: 4683. PubMed PMC
Sagova‐Mareckova M, Cermak L, Novotna J, Plhackova K, Forstova J, Kopecky J. 2008. Innovative methods for soil DNA purification tested in soils with widely differing characteristics. Applied and Environmental Microbiology 74: 2902–2907. PubMed PMC
Shigyo N, Hirao T. 2021. Saprotrophic and ectomycorrhizal fungi exhibit contrasting richness patterns along elevational gradients in cool‐temperate montane forests. Fungal Ecology 50: 101036.
Smith SE, Read D, eds. 2008. Mycorrhizal symbiosis, 3rd edn. London, UK: Academic Press, 769–787.
Soudzilovskaia NA, van Bodegom PM, Terrer C, Zelfde MV, McCallum I, Luke McCormack M, Fisher JB, Brundrett MC, de Sá NC, Tedersoo L. 2019. Global mycorrhizal plant distribution linked to terrestrial carbon stocks. Nature Communications 10: 5077. PubMed PMC
Steidinger BS, Crowther TW, Liang J, Van Nuland ME, Werner GDA, Reich PB, Nabuurs G, de‐Miguel S, Zhou M, Picard N et al. 2019. Climatic controls of decomposition drive the global biogeography of forest‐tree symbioses. Nature 569: 404. PubMed
Sterkenburg E, Clemmensen KE, Lindahl BD, Dahlberg A. 2019. The significance of retention trees for survival of ectomycorrhizal fungi in clear‐cut Scots pine forests. Journal of Applied Ecology 56: 1367–1378.
Stoffel MA, Nakagawa S, Schielzeth H. 2024. partr2: partitioning R2 in GLMMs . [WWW document] URL https://peerj.com/articles/11414/ [accessed 14 February 2025].
Storch D, Bohdalková E, Okie J. 2018. The more‐individuals hypothesis revisited: the role of community abundance in species richness regulation and the productivity–diversity relationship. Ecology Letters 21: 920–937. PubMed
Stritih A, Senf C, Seidl R, Grêt‐Regamey A, Bebi P. 2021. The impact of land‐use legacies and recent management on natural disturbance susceptibility in mountain forests. Forest Ecology and Management 484: 118950.
Tedersoo L, Bahram M, Põlme S, Kõljalg U, Yorou NS, Wijesundera R, Ruiz LV, Vasco‐Palacios AM, Thu PQ, Suija A et al. 2014. Global diversity and geography of soil fungi. Science 346: 1256688. PubMed
Tedersoo L, Bahram M, Toots M, Diédhiou AG, Henkel TW, Kjøller R, Morris MH, Nara K, Nouhra E, Peay KG et al. 2012. Towards global patterns in the diversity and community structure of ectomycorrhizal fungi. Molecular Ecology 21: 4160–4170. PubMed
Tikhonov G, Opedal ØH, Abrego N, Lehikoinen A, de Jonge MMJ, Oksanen J, Ovaskainen O. 2020. Joint species distribution modelling with the R‐package hmsc . Methods in Ecology and Evolution 11: 442–447. PubMed PMC
Treseder KK, Maltz MR, Hawkins BA, Fierer N, Stajich JE, McGuire KL. 2014. Evolutionary histories of soil fungi are reflected in their large‐scale biogeography. Ecology Letters 17: 1086–1093. PubMed
Van Der Heijden MGA, Bardgett RD, Van Straalen NM. 2008. The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecology Letters 11: 296–310. PubMed
Van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf‐Engel R, Boller T, Wiemken A, Sanders IR. 1998. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396: 69–72.
Větrovský T, Baldrian P, Morais D. 2018. Seed 2: a user‐friendly platform for amplicon high‐throughput sequencing data analyses. Bioinformatics 34: 2292–2294. PubMed PMC
Větrovský T, Kohout P, Kopecký M, Machac A, Man M, Bahnmann BD, Brabcová V, Choi J, Meszárošová L, Human ZR et al. 2019. A meta‐analysis of global fungal distribution reveals climate‐driven patterns. Nature Communications 10: 5142. PubMed PMC
Vohník M. 2020. Ericoid mycorrhizal symbiosis: theoretical background and methods for its comprehensive investigation. Mycorrhiza 30: 671–695. PubMed PMC
Vohník M, Mrnka L, Lukešová T, Bruzone MC, Kohout P, Fehrer J. 2013. The cultivable endophytic community of Norway spruce ectomycorrhizas from microhabitats lacking ericaceous hosts is dominated by ericoid mycorrhizal Meliniomyces variabilis. Fungal Ecology 6: 281–292.
White T, Bruns T, Lee S, Taylor J, Innis M, Gelfand D, Sninsky J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, eds. PCR protocols: a guide to methods and applications. New York, NY, USA: Academic Press, 315–322.
Wickham H, François R, Henry L, Müller K, Vaughan D. 2023. dplyr: a grammar of data manipulation . [WWW document] URL https://cran.r‐project.org/web/packages/dplyr/index.html [accessed 14 February 2025].
Willig MR, Kaufman DM, Stevens RD. 2003. Latitudinal gradients of biodiversity: pattern, process, scale, and synthesis. Annual Review of Ecology, Evolution, and Systematics 34: 273–309.
Wood SN. 2011. Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. Journal of the Royal Statistical Society: Series B (Statistical Methodology) 73: 3–36.