Symbiotic status alters fungal eco-evolutionary offspring trajectories.

Despite host-fungal symbiotic interactions being ubiquitous in all ecosystems, understanding how symbiosis has shaped the ecology and evolution of fungal spores that are involved in dispersal and colonization of their hosts has been ignored in life-history studies. We assembled a spore morphology database covering over 26,000 species of free-living to symbiotic fungi of plants, insects and humans and found more than eight orders of variation in spore size. Evolutionary transitions in symbiotic status correlated with shifts in spore size, but the strength of this effect varied widely among phyla. Symbiotic status explained more variation than climatic variables in the current distribution of spore sizes of plant-associated fungi at a global scale while the dispersal potential of their spores is more restricted compared to free-living fungi. Our work advances life-history theory by highlighting how the interaction between symbiosis and offspring morphology shapes the reproductive and dispersal strategies among living forms.

[1]  Jacob L. Steenwyk,et al.  A genome-scale phylogeny of the kingdom Fungi , 2021, Current Biology.

[2]  E. Kiers,et al.  The Evolution of Mutualistic Dependence , 2020 .

[3]  Nerea Abrego,et al.  Morphological traits predict host-tree specialization in wood-inhabiting fungal communities , 2020 .

[4]  M. Kolařík,et al.  GlobalFungi, a global database of fungal occurrences from high-throughput-sequencing metabarcoding studies , 2020, Scientific Data.

[5]  J. Stajich,et al.  Toward a Fully Resolved Fungal Tree of Life. , 2020, Annual review of microbiology.

[6]  J. Dettman,et al.  Nuclear Dynamics in the Arbuscular Mycorrhizal Fungi. , 2020, Trends in plant science.

[7]  Stephanie N. Kivlin,et al.  Global mycorrhizal fungal range sizes vary within and among mycorrhizal guilds but are not correlated with dispersal traits , 2020, Journal of Biogeography.

[8]  Scott T. Bates,et al.  Fungal functional ecology: bringing a trait‐based approach to plant‐associated fungi , 2019, Biological reviews of the Cambridge Philosophical Society.

[9]  F. Jeltsch,et al.  The role of active movement in fungal ecology and community assembly , 2019, Movement Ecology.

[10]  A. Howe,et al.  A meta-analysis of global fungal distribution reveals climate-driven patterns , 2019, Nature Communications.

[11]  D. Bebber,et al.  Geometry and evolution of the ecological niche in plant-associated microbes , 2019, bioRxiv.

[12]  F. Maestre,et al.  A few Ascomycota taxa dominate soil fungal communities worldwide , 2019, Nature Communications.

[13]  T. Gabaldón,et al.  Fungal evolution: major ecological adaptations and evolutionary transitions , 2019, Biological reviews of the Cambridge Philosophical Society.

[14]  Lei Liu,et al.  Contrasting latitudinal diversity and co-occurrence patterns of soil fungi and plants in forest ecosystems , 2019, Soil Biology and Biochemistry.

[15]  Marcus L. Roper,et al.  Mycofluidics: The Fluid Mechanics of Fungal Adaptation , 2019, Annual Review of Fluid Mechanics.

[16]  D. Hibbett,et al.  Contemporaneous radiations of fungi and plants linked to symbiosis , 2018, Nature Communications.

[17]  W. Cornwell,et al.  Bridging reproductive and microbial ecology: a case study in arbuscular mycorrhizal fungi , 2018, The ISME Journal.

[18]  Peter M. Letcher,et al.  Notes for genera: basal clades of Fungi (including Aphelidiomycota, Basidiobolomycota, Blastocladiomycota, Calcarisporiellomycota, Caulochytriomycota, Chytridiomycota, Entomophthoromycota, Glomeromycota, Kickxellomycota, Monoblepharomycota, Mortierellomycota, Mucoromycota, Neocallimastigomycota, Olp , 2018, Fungal Diversity.

[19]  D. Hibbett,et al.  Evolutionary dynamics of host specialization in wood-decay fungi , 2018, BMC Evolutionary Biology.

[20]  Emmanuel Paradis,et al.  ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R , 2018, Bioinform..

[21]  J. Heilmann‐Clausen,et al.  Fungal spore diversity reflects substrate-specific deposition challenges , 2018, Scientific Reports.

[22]  Stephen E. Fick,et al.  WorldClim 2: new 1‐km spatial resolution climate surfaces for global land areas , 2017 .

[23]  Paul-Christian Bürkner,et al.  brms: An R Package for Bayesian Multilevel Models Using Stan , 2017 .

[24]  Robert Lücking,et al.  Fungal Diversity Revisited: 2.2 to 3.8 Million Species , 2017, Microbiology spectrum.

[25]  Lei Liu,et al.  Plant diversity represents the prevalent determinant of soil fungal community structure across temperate grasslands in northern China , 2017 .

[26]  A. Pringle,et al.  Long-Distance Dispersal of Fungi , 2017, Microbiology spectrum.

[27]  Derya Akkaynak,et al.  Avian egg shape: Form, function, and evolution , 2017, Science.

[28]  J. Heilmann‐Clausen,et al.  Mean spore size and shape in ectomycorrhizal and saprotrophic assemblages show strong responses under resource constraints , 2017 .

[29]  M. Fisher,et al.  Emerging Fungal Threats to Plants and Animals Challenge Agriculture and Ecosystem Resilience , 2017, Microbiology spectrum.

[30]  Chengshu Wang,et al.  Insect Pathogenic Fungi: Genomics, Molecular Interactions, and Genetic Improvements. , 2017, Annual review of entomology.

[31]  Carla M. Zammit,et al.  Introducing BASE: the Biomes of Australian Soil Environments soil microbial diversity database , 2016, GigaScience.

[32]  Christian L. Cox,et al.  Coral snakes predict the evolution of mimicry across New World snakes , 2016, Nature Communications.

[33]  Scott T. Bates,et al.  FUNGuild: An open annotation tool for parsing fungal community datasets by ecological guild , 2016 .

[34]  K H Andersen,et al.  Adult and offspring size in the ocean over 17 orders of magnitude follows two life history strategies. , 2015, Ecology.

[35]  R. Brandl,et al.  Ectomycorrhizal fungi have larger fruit bodies than saprotrophic fungi , 2015 .

[36]  O. Ovaskainen,et al.  Spore sensitivity to sunlight and freezing can restrict dispersal in wood-decay fungi , 2015, Ecology and evolution.

[37]  Gianluigi Cardinali,et al.  International Society of Human and Animal Mycology (ISHAM)-ITS reference DNA barcoding database--the quality controlled standard tool for routine identification of human and animal pathogenic fungi. , 2015, Medical mycology.

[38]  C. Bässler,et al.  Gone with the wind - a review on basidiospores of lamellate agarics , 2015 .

[39]  K. Burns,et al.  The repeated evolution of large seeds on islands , 2014, Proceedings of the Royal Society B: Biological Sciences.

[40]  D. Bates,et al.  Fitting Linear Mixed-Effects Models Using lme4 , 2014, 1406.5823.

[41]  O. Ovaskainen,et al.  Do small spores disperse further than large spores? , 2014, Ecology.

[42]  Pedro W. Crous,et al.  MycoBank gearing up for new horizons , 2013, IMA fungus.

[43]  Eduard Szöcs,et al.  taxize: taxonomic search and retrieval in R , 2013, F1000Research.

[44]  Jonathan D. G. Jones,et al.  Obligate biotroph parasitism: can we link genomes to lifestyles? , 2012, Trends in plant science.

[45]  J. Amler.  The Fifth Kingdom , 2011 .

[46]  M. S. Hunter,et al.  Extraordinarily widespread and fantastically complex: comparative biology of endosymbiotic bacterial and fungal mutualists of insects. , 2010, Ecology letters.

[47]  M. Westoby,et al.  A General Model for the Scaling of Offspring Size and Adult Size , 2008, The American Naturalist.

[48]  L. Ryvarden,et al.  Relationship between basidiospore size, shape and life history characteristics: a comparison of polypores , 2008 .

[49]  E. Jones.  Form and function of fungal spore appendages , 2006 .

[50]  Campbell O. Webb,et al.  A Brief History of Seed Size , 2005, Science.

[51]  Mercedes S. Foster,et al.  Biodiversity of Fungi: Inventory and Monitoring Methods , 2004 .

[52]  M. Westoby,et al.  Seedling survival and seed size: a synthesis of the literature , 2004 .

[53]  C. Ingold.  Range in size and form of basidiospores and ascospores , 2001 .

[54]  D. McLaughlin,et al.  Systematics and Evolution , 2000, The Mycota.

[55]  R. Poulin.  Evolutionary Ecology of Parasites , 1997 .

[56]  David G. Kirkpatrick,et al.  On the shape of a set of points in the plane , 1983, IEEE Trans. Inf. Theory.

[57]  T. Vincenty.  DIRECT AND INVERSE SOLUTIONS OF GEODESICS ON THE ELLIPSOID WITH APPLICATION OF NESTED EQUATIONS , 1975 .

[58]  C. L. Kramer,et al.  Periodicity and total spore production by lignicolous basidiomycetes. , 1974, Mycologia.

[59]  Thorsten Ahl,et al.  Pathogenic Root-Infecting Fungi , 1969 .

[60]  D. Hughes,et al.  Diversity of Entomopathogenic Fungi: Which Groups Conquered the Insect Body? , 2016, Advances in genetics.

[61]  C. Cerri,et al.  Land use, soil and litter chemistry drive bacterial community structures in samples of the rainforest and Cerrado (Brazilian Savannah) biomes in Southern Amazonia , 2015 .

[62]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[63]  Mark P. J. van der Loo,et al.  The stringdist Package for Approximate String Matching , 2014, R J..

[64]  T. Mengiste.  Plant immunity to necrotrophs. , 2012, Annual review of phytopathology.

[65]  R. Halling.  Biodiversity of Fungi: Inventory and Monitoring Methods , 2005 .

[66]  M. Giovannetti.  Spore Germination and Pre-Symbiotic Mycelial Growth , 2000 .

[67]  C. M. Lessells,et al.  The Evolution of Life Histories , 1994 .