Symbiotic status alters fungal eco‐evolutionary offspring trajectories

Abstract

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.

Full text

Ecolog y Letters. 2023;26:1523–1534.
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wileyonlinelibrary.com/journal/ele
LETTER
Symbiotic status alters fungal eco- evolutionary offspring
trajectories
Carlos A.Aguilar- Trigueros1,2, 3,4 | Franz- SebastianKrah5 | William K.Cornwell6 |
Amy E.Zanne7 | NereaAbrego3,8 | Ian C.Anderson4 | Carrie J.Andrew9 |
PetrBaldrian10 | ClausBässler5 | AndrewBissett11 | V. BalaChaudhary12 |
BaodongChen13,14 | YongliangChen15 | ManuelDelgado- Baquerizo16,17 |
ColineDeveautour18 | EleonoraEgidi4 | HabacucFlores- Moreno7 | JacobGolan19 |
JacobHeilmann- Clausen20 | StefanHempel1 | YajunHu21 | HåvardKauserud22 |
Stephanie N.Kivlin23 | PetrKohout10 | Daniel R.Lammel1 | Fernando T.Maestre24,25 |
AnnePringle19 | JennaPurhonen3,26,27 | Brajesh K.Singh4,28 | Stavros D.Veresoglou1 |
TomášVětrovský10 | HaiyangZhang4,29 | Matthias C.Rillig1,2 | Jeff R.Powell4
1Institute of Biology, Freie Universität Berl in, Berlin, Germany
2Berlin- Brandenburg Institute of Advanced Biodiversity Research (BBIB), Berlin, Germany
3Department of Biological and Environmental Sc ience, University of Jy väskylä, Jyvaskyla, Finland
4Hawkesbury Institute for the Environment, Western Sydney University, Penrith, New South Wale s, Australia
5Faculty of Biological Scienc es, Department of Conservation Biology, Institute for Ecology, Evolution and Diversity, Goethe University Frankfurt, Frankfurt a m
Main, Germany
6Evolution & Ecology Re search Center, School of Biological, Earth, and Environmental Sciences, University of New South Wales, Sydney, New South Wales,
Australia
7Department of Biology, University of Miami, Coral Gables, Florida, USA
8Department of Agricultural Sciences, Un iversity of Helsinki, Helsinki, Finland
9Biology Depar tment, Oberl in College & Conservatory, Oberlin, Ohio, USA
10Laboratory of Environ mental Microbiology, Institute of Mic robiolog y of the Czech Academy of Sciences, Praha 4, Czech Republic
11Oceans and Atmosphere, CSIRO, Hobart, Tasmania, Australia
12Department of Environmental Studies, Dartmouth College, Hanover, New Hampsh ire, USA
13State Key Laboratory of Urban and Reg ional Ecolog y, Research Cent er for Eco- Environmental Scienc es, Chinese Academy of Sciences, Beijing, People's
Republic of Chi na
14University of Chine se Academy of Sciences, Beijing, People's Republic of China
15College of Resource s and Environmental Sciences, China Agricultural University, Beijing, People's Republic of China
16Laboratorio de Biodiversidad y Funcionamiento Ecosistémico. Instituto de Recursos Naturales y Agrobiología de Sev illa (IRNAS), CSIC, Sevilla, Spain
17Unidad Asociada CSIC- UPO (BioFun). Universidad Pablo de Olavide, Sevil la, Spain
18AGHYLE Research Unit, Institut Poly technique UniLaSalle, Mont- Saint- Aignan, France
19Departments of Botany and Bacter iology, University of Wisconsin– Madison, Madison, Wisconsin, USA
20Center for Macroecology, Evolution and Climate, GLOBE Institute, University of Copen hagen, Copenhagen, Den mark
21Key Laboratory of Agro- ecological Processes in Subtropical Region & Changsha Research Station for Agr icultural and Environmental Monitoring, Institute of
Subtropical Agricu lture, Chinese Ac ademy of Sciences, Hunan, China
22Evogene, Department of Bioscience s, University of Oslo, Oslo, Norway
23Department of Ecology and Evolution, University of Tennessee, Knoxville, Tennesse e, USA
24Instituto Multidisciplinar para el Estudio del Medio “Ra mon Margalef ”, Universidad de Alicante, Carretera de San Vicente del Raspeig s/n, Alicante, Spai n
25Departamento de Ecología, Universidad de Al icante, Car retera de San Vicente del Raspeig s/n, Alicante, Spain
Received: 11 April 2023
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Revised: 21 May 2023
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Accepted: 23 May 2023
DOI: 10.1111/ele.14271
This is an open access ar ticle under the ter ms of the Creative Commons Attribution-NonCommercial License, which per mits use, distribution and reproduction in
any medium, provided the original work is properly cited and is not used for commercial pur poses.
© 2023 The Authors. Ec ology Letters published by John Wiley & Sons Ltd.
Matthias C. Ri llig and Jeff R. Powell joint senior authorship.

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SYMBIOSIS ALTERS SPORE SIZE ECOLOGY
INTRODUCTION
In life- history theory, the ecology and evolution of off-
spring size is linked to environmental factors that species
encounter during reproduction, dispersal and early-
colonization, as well as physiological constraints during
their development (Stearns,1992). By providing a com-
mon framework where disparate offspring structures
such as plant seeds (Moles et al., 2005), animal ovules
(Neuheimer et al.,2015), avian eggs (Stoddard et al.,2017 )
and mammal size at weaning (Falster et al.,2008) can
be compared, life- history theory aims at discovering
general principles behind the drivers shaping the ecol-
ogy and evolution of species at earlier stages of their life
cycle. According to life- history theory, alterations in the
size of offspring structures of sessile organisms can in-
fluence their potential for both dispersal (moving to a
new habitat) and colonization (establishing a new indi-
vidual) (Falster et al.,2008; Kavanagh & Burns,2014).
The size of the offspring structure could impact how far
it can disperse and its capacity to withstand environ-
mental conditions during dispersal. Conversely, change
in size alter the amount of resources that can be packed
into offspring structures, resources which can facilitate
germination and earlier stages of development that ulti-
mately lead to successful colonization and the formation
of a new functional individual.
However, most life forms that have been used to
develop this knowledge are free- living macroorgan-
isms, ignoring the large diversity of microbial forms.
Conspicuously absent is the Kingdom Fungi, which, with
136,000 described species and an estimated diversity of
3– 10 million species (Hawksworth & Lücking,2017), is a
large portion of the tree of life. This dearth represents a
fundamental knowledge gap because, as we report here
(Figure1), variation in fungal offspring size (up to eight
orders of magnitude) is as high or higher than that of
macroorganisms whose comparative offspring studies
(e.g. plant seeds and avian eggs) dominate the life- history
theory (Figure1). Here, we use fungal spores as offspring
26Department of Music, Art and Culture Studies, University of Jyväskylä, Jyvaskyla, Finland
27School of Re source Wisdom, University of Jyväskylä, Jyvaskyla, Finland
28Global Centre for Land Based Innovation, Western Sydney University, Penrith, New South Wales, Australia
29College of Life Sciences, Hebei University, Baoding, Chi na
Correspondence
Carlos A. Aguilar- Trigueros, Institute
of Biology, Freie Universität Berlin,
Altensteinstrasse 6, 14195 Berli n, Ger many.
Email: calgit@gmail.com
Funding information
Alexander von Humboldt- Stiftu ng,
Grant/Award Number: Feodor- Lynen
Fellowsh ip; Australian Research Cou ncil,
Grant/Award Number: DP190103714
and FT0100590; Bundesmin isterium
für Bildung und Forschung, Grant/
Award Number: 01LC1501A; Deutsche
Forschungsgemeinschaft, Grant/
Award Number: HE6183; Deutscher
Akademischer Austauschdienst; Division
of Environmental Biology, Grant/Award
Number: 1623040 and 1655759; Grantová
Agentura České Republiky, Grant /Award
Number: 21- 17749S; H2020 European
Research Council, Grant /Award Number:
647038 and 694368; Universities Australia
Editor: Dustin John Marshall
Abstract
Despite host- fungal symbiotic interactions being ubiquitous in all ecosystems,
underst anding how symbiosis has shaped the ecolog y 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.
KEYWOR DS
functional ecology, fungi, life- history, offspring size, symbiosis
FIGUR E 1 Interspecific variation in spore size and symbiotic lifestyles across the fungal kingdom: (a) Illustration of the diversity of shapes
and sizes among all fungal sexual and asexual spore types. (b) Interspecific spore size variation is more than eight orders of magnitude across
the kingdom, ranging from the mitospores of Phoma muscivora of 9.0 × 10 −2 μm3 to multinucleate spores of the mycorrhizal fungus Scutellospora
scutata of 7.8 × 10 7 μm3. This variation is comparable to that of other offspring structures such as angiosperm seeds and bird eggs (to aid
comparison, all offspring structures are presented on the same scale [μm3]). (c) Phylogenetic tree with terminal branches representing orders
(the number of species per order for which we collected spore data is given in parenthesis). The corresponding heatmap displays order averages
(in logarithmic scale) of spore size as volume in yellow- to- red colour scale for sexual and asexual spores separating spores types based on the
number of nuclei, which is a major distinction in spore types for fungi (see main text and supplementary material for a detailed explanation on
descriptions of the biology of these distinct spores). Fungal spores (n = 26, 134 species), avian egg data (n = 1395 species) were obtained from7,
while seed data (n = 34,390 species) were obtained from the seed database of Kew Botanical Garden (http://data.kew.org/sid/?_ga=2.73581
714.12873 66807.15010 84977-13091 87973.15010 84964).

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AGUILAR- TRIGUEROS et al.
structures (Figure1b) because they represent reproduc-
tive output units produced by a mature mycelium (the
‘parent’ fungus) that function as dispersal propagules to
colonize novel habitats that are usually distantly located
from the parental fungus. Each spore has the potential
to develop into a new mycelium, which is independent
from the parental one in the new habitat. Spore traits,
such as total size, are hypothesized to determine the
Mean sexual spore volume
1-2 Nuclei >2 Nuclei
(a) (b)
(c)
Eurotiales (n=946)
Onygenales (n=200)
Ascosphaerales (n=3)
Chaetothyriales (n=198)
Verrucariales (n=68)
Phaeomoniellales (n=12)
Lecanorales(n=533)
Umbilicariales (n=6)
Mytilinidiales (n=18)
Pleosporales (n=2047)
Patellariales (n=9)
Hysteriales (n=24)
Botryosphaeriales (n=462)
Venturiales (n=153)
Capnodiales (n=438)
Mycosphaerellales(n=3302)
Myriangiales (n=35)
Dothideales (n=66)
Arthoniales(n=171)
Magnaporthales (n=110)
Ophiostomatales (n=273)
Diaporthales(n=588)
Togniniales (n=57)
Sordariales (n=357)
Coniochaetales(n=32)
Glomerellales (n=251)
Hypocreales (n=2212)
Chaetosphaeriales (n=153)
Microascales (n=362)
Xylariales (n=629)
Amphisphaeriales (n=214)
Erysiphales (n=572)
Helotiales (n=532)
Pezizales (n=263)
Orbiliales (n=183)
Saccharomycetales (n=56)
Taphrinales (n=6)
Corticiales (n=154)
Agaricales (n=2292)
Atheliales (n=74)
Boletales (n=433)
Polyporales (n=1735)
Thelephorales (n=227)
Russulales (n=853)
Gloeophyllales (n=37)
Jaapiales (n=2)
Hymenochaetales (n=679)
Trechisporales (n=75)
Gomphales (n=38)
Geastrales (n=52)
Auriculariales (n=93)
Cantharellales (n=239)
Dacrymycetales (n=45)
Trichosporonales (n=6)
Tremellales (n=134)
Wallemiales (n=3)
Ceraceosorales (n=2)
Exobasidiales (n=31)
Microstromatales (n=8)
Ustilaginales (n=13)
Tilletiales (n=13)
Georgefischeriales (n=6)
Microbotryales (n=9)
Pucciniales (n=451)
Mucorales (n=311)
Umbelopsidales (n=9)
Endogonales (n=4)
Glomerales (n=119)
Diversisporales (n=130)
Mortierellales (n=54)
Basidiobolales (n=3)
Harpellales (n=63)
Kickxellales (n=16)
Dimargaritales (n=2)
Entomophthorales (n=29)
Zoopagales (n=16)
Rhizophydiales (n=2)
Chytridiales (n=7)
Spizellomycetales (n=3)
Neocallimastigales (n=3)
Blastocladiales (n=3)
Glugeida (n=6)
Dissociodihaplophasida (n=4)
Meiodihaplophasida (n=2)
Metchnikovellida (n=2)
Microsporidian fungi
Zoosporic fungi
Zygomycetous fungi
Basidiomycota
Ascomycota
Spore Volume
(μm3) [log scale]
100
Mean
107
Mean asexual spore volume
1-2 Nuclei >2 Nuclei
8 orders of magnitude variation
11 orders of magnitude variation
4 orders of magnitude var.
Birds
(eggs)
Plants
(seeds)
Fungi
(spores)
Offspring size as volume (μm3)
1013
1081018
103
Sexual spores Asexual spores 50 um

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SYMBIOSIS ALTERS SPORE SIZE ECOLOGY
likelihood of colonization based on spore interactions
with their environment during their release, movement,
attachment/landing, dormancy and germination (Golan
& Pringle,2 017; Halbwachs,2015; Kivlin,2020; Rockett
& Kramer,1974). Thus, spores are functionally analo-
gous to dispersal offspring propagules of other sessile
modular organisms like plant seeds (Moles et al.,2005)
or marine invertebrate eggs (Neuheimer et al.,2015).
We hypothesize that symbiotic status of fungal spe-
cies may explain this large variation in spore size because
of the contrasting conditions that spores encounter when
germinating and colonizing dead organic matter versus
living hosts. That is, most extant fungi can be placed
along a symbiotic spectrum spanning from asymbiotic
species whose spores start the colonization of organic
matter substrates, to a variety of symbiotic interactions
whose spores initiate the colonization (i.e. infection)
in hosts in almost all major domains of life (Lutzoni
et al.,2018; Naranjo- Ortiz & Gabaldon,2019) (Figure2;
FiguresS3 and S4). Furthermore, shifts between free-
living to symbiotic life styles have been a major driver in
trait evolution in the fungal k ingdom (Lutzoni et al.,2018;
Naranjo- Ortiz & Gabaldon,2019) raising the question of
how transitions in symbiotic status influence the ecol-
ogy and evolution of spores. Here, we use a definition of
symbiosis that is common in evolutionary biology: the
intimate physical living together of distinct species (usu-
ally distantly related), whether mutualistic, parasitic, or
commensal, including macrobe- microbe interactions,
where the former is considered the ‘host’ and the latter
the ‘symbiont’ (Chomicki et al.,2020).
Specifically, to understand the importance of symbi-
otic status in explaining differences in the size and func-
tion of spores across the fungal kingdom, we asked three
questions. First, are transitions in symbiotic status cor-
related with shifts in spore size? To answer this question,
we used linear phylogenetic regression to test whether the
spore si ze of symbiotic group s (e.g. insect p athogens, plant
pathogens, ectomycorrhizal) shift in size (i.e. increase or
decrease) compared to asymbiotic fungi across all major
fungal phyla. We then focused on plant- associated fungi
in the Dikarya clade to test whether symbiotic groups
of obligate lifestyles have larger offspring than symbiotic
groups with facultative lifestyles. We focus on fungi as-
sociated to plants in this clade because plants are by far
the host type with the largest diversification of symbiotic
lifestyles (Lutzoni et al.,2018). In addition, this hypothe-
sis has been repeatedly used to explain why the spores of
some obligate plant pathogenic and mutualistic fungi are
so large. This hypothesis posits that obligate symbionts
may benefit from the greater resources present in large
spores, since these resources represent the only means
of surviving during dispersal and initial colonization
(i.e. infection) of new hosts until resources can be ex-
changed with the host plant (Garrett,1970; McLaughlin
& Spatafora,2014). Second, we asked whether spore size
distribution across fungal communities at a global scale
can be explained by climate variables, regardless of sym-
biotic status. We hypothesized that climate may be more
important than symbiotic status in explaining spore size
distributions given the worldwide distribution of fungi
spanning diverse climatic zones. As both asymbiotic and
plant- associated fungal species release and disperse their
spores into the abiotic environment, climate may act as
a key driver of spore size variation (Kendrick,2 017). In
addition, based on predictions from life- history theory,
we expect species with larger offspring sizes to be asso-
ciated with limiting environmental regimes (Moles &
West oby, 2004). Third, we asked whether the dispersal
potential of spores differs between asymbiotic and plant-
associated fungi. Specifically, we tested whether species
with smaller spores have a broader geographic distri-
bution (i.e. higher extent of occurrence) and whether
this relationship varies between asymbiotic and plant-
associated fungi. One of the main ecological functions
of offspring is dispersal and, for several fungal groups,
it has been proposed that small offspring should travel
farther than large offspring, increasing the dispersal po-
tential of species (Norros et al.,2014). However, if plant-
associated fungi require large spore sizes, they may have
more- limited distributions than asymbiotic fungi.
MATERIALS AND METHODS
Assembly of spore database
Unlike macroorganisms such as plants and ani-
mals, no databases of offspring morphology for fungi
exist. Therefore, to answer our questions, we created
and populated a new database by text mining nearly
100,000 taxonomic descriptions deposited in Mycobank
(Robert et al., 2013) (http://www.mycob ank.org/; see
Supplementary material for further details). In total, we
collected information on spore width and length dimen-
sions for >26,000 accepted species (based on taxonomy
from the Catalogue of Life; https://www.catal ogueo flife.
org/), representing 20% of all described fungal species
(FigureS1). This database includes spore- dimension
data from both sexually and asexually produced spores
across major fungal lineages at different stages of fungal
life cycles. However, we restricted the analysis described
below to sexual spore types described as ‘ascospores’
and ‘basidiospores’ (henceforth referred to as ‘sexual
spores’) and asexual spore types described as ‘conidia’
and ‘sporangiospores’ (henceforth referred to as ‘asexual
spores’) because they represent the most frequently oc-
curring types of spores in our dataset and thus can be
compared across several fungal lineages and symbiotic
groups (Figure1c; FigureS2). We also excluded spores of
glomeromycete fungi for our main analyses because their
extreme large size may bias the results (see FigureS2 and
supplementary material for specific spore definitions and
nomenclature used in the analysis; Kendrick,2017 ). We

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AGUILAR- TRIGUEROS et al.
then calculated spore volume using width and length as
a proxy for spore size following the formula for a prolate
spheroid (Aguilar- Trigueros et al.,2019). We used volume
as a proxy for size because it captures the 3D structure
of fungal spores and, based on allometric theory, volume
scales with other measurements of size, such as weight.
Indeed, volume has been used in life- history research
as a proxy for offspring size across several large clades
(Stearns,1992). Using this approach, we found that spore
size across species varied by more than eight orders of
magnitude (Figure1b).
Assembly of symbiotic status data
We also assembled a symbiotic status database (by min-
ing and crosschecking different functional databases)
where fungal species were categorized as asymbiotic
(i.e. saprotrophic species that have only been reported
as free- living during their whole life cycle) or symbiotic
with a wide diversity of host and types of interactions
as follows: (1) Asymbiotic saprotrophs; (2) Insect path-
ogens; (3) Lichen fungi; (4) Plant endophytes; (5) Plant
pathogenic necrotrophs; (6) Plant pathogenic biotrophs;
(7) Ectomycorrhizal fungi; (8) Arbuscular Mycorrhizal
fungi; (10) Human pathogens. For plant symbiotic fungi,
we further classify the level of specialization as either fac-
ultative symbiosis (species that are reported to alternate
between a free- living and symbiotic phase) or obligate
symbiosis (species that have been exclusively reported as
symbiotic to complete their life cycle) based on the biol-
ogy of their respective symbiotic group (see supplemen-
tary material for data sources and details on the criteria
used to define symbiotic groups).
Phylogenetic regression of shifts in
spore size and evolutionary transitions in
symbiotic groups
Because evolutionary history shapes how and where spe-
cies are today, the role of this history can be examined by
testing how traits shift across the tree of life. For fungal
spores, recent reviews and anecdotal evidence suggest
that spore size is expected to differ more widely in some
fungal clades than others (Aguilar- Trigueros et al.,2019;
Ingold, 2001). Thus, we used two phylogenies to test
whether transitions in symbiotic status correlate with
shifts in fungal spore size. The first phylogeny consists
of 1644 fungal species whose genome has been fully se-
quence d as recently published in (Li et al.,2021). Focusi ng
our analysis on these species allowed us to incorporate
the most robust, species- level phylogenetic tree available
to date for fungi (as this tree is based on whole genome
data) that captures the entire kingdom (i.e. it is not spe-
cific to only a subset of fungal clades). However, because
this tree only includes a limited number of species, we
also used a taxonomy- based phylogeny consisting of
23,000 species from which we obtained taxonomic data
from phylum- to- species level using the function as.phylo
from ape package (Paradis & Schliep,2018) (see further
details in the supplementary material for the construc-
tion of this tree).
Independently for each phylum or fungal group (i.e.
Ascomycota, Basidiomycota, zygomycetous fungi, zoo-
sporic fungi and microsporidan fungi), we conducted
phylogenetic linear regression models where the log-
arithm of spore volume was the response variable,
symbiotic status (based on the 10 symbiotic guilds clas-
sified here) was the explanatory variable and either the
genome- based phylogenetic tree from (Li et al.,2021) or
the taxonomy derived cladogram was used to account for
phylogenetic relatedness. These phylogenetic regressions
were conducted on sexual spores of the Ascomycota and
Basidiomycota (i.e. ascospores and basidiospores) and
asexual spores of all phyla and fungal groups (as de-
fined above, we only include asexual spores referred as
‘conidia’ or ‘sporangiospores’) separately as they repre-
sent two separate traits under different selection. These
phylogenetic linear regression models were conducted
using the function phylolm from the phylolm package
(Ho et al.,2016).
We conducted additional phylogenetic regression
models testing whether spore size is bigger for obligate
symbionts compared to facultative symbionts for sexual
spores of plant- associated fungi in the Ascomycota and
Basidiomycota and asexual spores of the Ascomycota.
As above, this phylogenetic regressions were performed
the genome- based phylogenetic tree (Li et al., 2021) or
the taxonomy- based cladogram.
Relative importance of symbiotic status against
climate variables in explaining spore size
variation across communities
To obtain climatic information, we first mapped the
geographic distributions of fungal species observed in
several large- scale, high- throughput DNA- sequencing
studies of fungal communities from soil and plant
samples covering an extensive breadth of biomes and
occurring on all seven continents (FigureS5; see supple-
mentary material section for details on how species an-
notations were performed). Then, we collected climatic
data associated with the locations where those species
were found, estimated mean values for each species, and
compared the ability of those climate variables and each
species’ symbiotic status to explain variation in spore
size.
For this analysis, we focused on species that in our
database are reported to produce only one spore type be-
cause it is not possible to determine the spore type asso-
ciated with environmental DNA sequences. We assessed
the importance of fungal symbiotic status (i.e. whether

1528
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SYMBIOSIS ALTERS SPORE SIZE ECOLOGY
fungi are free- living saprotroph or plant- associated) in
explaining interspecific variation in spore size relative
to other drivers, including spore type (i.e. sexual and
asexual) and climate across communities worldwide.
Phylogenetic linear regression models were fit using the
following predictors: spore type (categorical variable),
climate (averages of mean annual temperature and pre-
cipitation, temperature and precipitation seasonality,
maximum solar radiation and minimum water- vapour
pressure calculated across locations in which each spe-
cies was detected; as continuous variables) and symbiotic
status (as a categorical variable— free- living or plant-
associated). As before, we conducted this analysis using
two phylogenetic regression (one using the genome- based
phylogenetic tree from (Li et al.,2021) and the other one
using the taxonomy- based tree).
Differences between saprotrophic and plant-
associated fungi in the relationship between
spore size and geographic spread
We assessed the role that fungal lifestyle plays in deter-
mining the relationship between geographic range and
spore size. As with the previous analysis, we focused on
species that in our database are reported to produce only
one spore type because it is not possible to determine
the spore type associated with environmental DNA se-
quences. To do this, we estimated species’ geographic
ranges from their mapped distributions in environmen-
tal DNA- sequencing studies. Specifically, geographic
range for each species was estimated in two ways: (1)
as the maximum distance in meters between samples,
in which the species was detected using the ellipsoid
method (Vincenty,1975) calculated with the distVincen-
tyEllipsoid function from the ‘geosphere’ package in R
(Hijmans et al.,2019); and (2) as the range area in square
meters using alpha- hull- derived measures (Edelsbrunner
et al.,1983) incorporating all samples in which the spe-
cies was detected using the getDynamicAlphaHull
function from the ‘rangeBuilder’ package in R (Davis
Rabosky et al.,2016). Each estimate of range size was
then used as a response variable in linear models to esti-
mate slopes representing the strength of the relationship
between geographic range and spore volume for fungi
with saprotrophic lifestyles (free- living) and those from
plant- associated lifestyles (symbiotic). These models in-
cluded random intercepts representing the taxonomic
order (to account for non- independence among fungal
species) and the primer set used to amplify fungal DNA
(to account for biases among primer sets in their ability
to detect fungal species). Because point- estimates can be
sensitive to unbalanced sampling designs and, therefore,
are unreliable, we used functions in the ‘lme4’ (Bates
et al.,2015) and ‘brms’ (Bürkner,2017 ) packages in R to
fit Bayesian models and estimate posterior distributions
of the slope parameters and calculated 95%- credible
intervals from four MCMC chains (each 2000 itera-
tions with a 1000- iteration burn- in) to assess differences
among fungal lifestyles. To assess relationships within
individual orders, separate linear mixed- effects models
were also fitted for each combination of taxonomic order
and fungal lifestyle for which a minimum of five species
with spore volume and geographic extent were available.
All st atistic al analyses were p erformed using R version
4.0.1 (Team,2020). Spore volume was log10- transformed
prior to statistical analyses.
RESULTS
Strong differences in spore size among fungal
clades
Spore size variation among sexual and asexual spores
was strongly structured by species’ evolutionary history
(Figure1c, Ta blesS1 and S2). For instance, the asexual
spores from the glomeromycetes are the largest in the
kingdom, from 1.5- to- 4 orders of magnitude larger com-
pared to other spores (either sexual or asexual) from
other groups and this difference shows strong phyloge-
netic structure (Pagel's lambda ~0.7 depending on the
comparison, see Tab leS1). These spores of glomeromy-
cetous fungi, however, are unique among other fungi be-
cause they contain hundreds of nuclei (an unparalleled
feature in the kingdom (Kokkoris et al., 2020)), which
might partly explain their extremely large size (Aguilar-
Trigueros et al., 2019). Further, we found that sexual
spores of basidiomycetes are on average 6 μm3 smaller
than ascomycetes across the tree (Pagel's lambda = 0.8,
see TableS2). While this pattern alone cannot determine
the mechanisms behind this size difference, it is consist-
ent with the hypothesis that sexual spores of basidiomy-
cetes are smaller than those of the ascomycetes because
the Basidiomycota, as a whole, evolved a spore launch-
ing mechanism (‘the surface tension catapult’) that
depends on spore size. In contrast, the launching mech-
anism of ascomycetes does not (Ingold,2001; Roper &
Seminara,2019). This potential mechanism suggests that
the size of the spore is dependent on the anatomy and
morphology of the reproductive structure of the paren-
tal fungus. Such parent- to- offspring regulation has also
been observed in other taxa, such as placental mammals,
for whom size at birth depends on the anatomical con-
straints of the reproductive structure where the offspring
develops (Stearns,1992).
Correlation between transitions in symbiotic
status and shifts in spore size vary among
fungal clades
We found support for our hypothesis that evolution-
ary transitions in symbiotic status correlate with shifts

|
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AGUILAR- TRIGUEROS et al.
FIGUR E 2 Shifts in size of sexual and asexual spores between asymbiotic fungi (blue points) and symbiotic groups (red points) across
Dikarya (a, b) and non- Dikarya fungi (c). Point ranges show the predicted mean values (points) and associated standard errors (ranges) for each
symbiotic group based on phylogenetic linear regression models using a taxonomy- based phylogeny. The horizontal blue lines are added to help
comparison of asymbiotic and symbiotic fungi (except for Microsporidan fungi that have not recorded asymbiotic species). Similar results were
obtained in models using a genome- based phylogeny (see FigureS2).
Insect pathogens
Insect pathogens
Ascomycota Basidiomycota
10
2
10
3
10
4
Sexual spore size (
μ
m³)
(a)
Ascomycota Basidiomycota
10
1
10
2
10
3
Asexual spore size (
μ
m³)
(b)
Microsporidia Zoosporic
fungi
Zygomycetous
fungi
10
1
10
2
10
3
Asexual spore size (
μ
m³)
(c)
Asymbiotic
saprotrophs
Asymbiotic
saprotrophs
Asymbiotic
saprotrophs
Asymbiotic
saprotrophs
Asymbiotic
saprotrophs
Human pathogens
Human pathogens
Human pathogens
Human pathogens
Lichen fungi
Lichen fungi
Lichen fungi
Lichen fungi
Fungal parasite
Plant endophytes
Plant endophytes
Necrotrophic
plant pathogens
Necrotrophic
plant pathogens
Necrotrophic
plant pathogens
Necrotrophic
plant pathogens
Necrotrophic
plant pathogens
Ectomycorrhizal
fungi
Ectomycorrhizal
fungi
Biotrophic
plant pathogens
Biotrophic
plant pathogens
Biotrophic
plant pathogens
Biotrophic
plant pathogens
Asymbiotic
saprotrophs
Insect pathogens
Insect pathogens
Insect pathogens
Animal endopa
rasite
Animal endopa
rasite

1530
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SYMBIOSIS ALTERS SPORE SIZE ECOLOGY
in the size of both sexual and asexual spores (TablesS3
and S4; Figure2; FigureS3). However, the direction and
strength of this correlation highly depended on the sym-
biotic group, spore type and phylum considered. We
found that shifts in sexual spore size during transitions
from saprotrophic to symbiotic groups were stronger in
the Ascomycota compared to the Basidiomycota, specifi-
cally, we found shifts to larger spore sizes among insect
pathogens, ectomycorrhizal, lichen and mildew fungi in
the Ascomycota (although statistical support for the last
two groups was found on only one phylogenetic regres-
sion; see TableS3). For asexual spores, we also observed
stronger shifts of size and symbiotic status among groups
in the Ascomycota compared to the Basidiomyota, al-
though shifts in asexual spore sizes were more heterogene-
ous: shifts to larger asexual spores were associated with
biotrophic and necrotrophic plant pathogens, while shifts
to smaller asexual spore sizes were associated with lichen
and insect pathogenic fungi (TableS4). Finally, we also
detected shifts towards larger asexual spore sizes among
insect and necrotrophic pathogens of zygomycetous fungi
(TableS4) and for insect pathogens in the Microsporidia.
Among plant- associated fungi, we found a global
trend towards increased sexual spore size in fungi with
more obligate symbioses in the Ascomycota only (i.e.
we found no statistical support for this hypothesis with
plant- associated groups in the Basidiomycota). For sex-
ual spores, plant obligate symbionts in the Ascomycota
were about 29 μm3 larger than spores of facultative sym-
bionts counterparts, while for asexual spores, obligate
symbionts were up to 59 μm3 larger than spores of faculta-
tive symbionts (all p- values <0.0 01; FigureS4; TableS5).
A possible mechanism behind large spores being associ-
ated with these groups is that spore reserves or thicken-
ing of spore cell walls increase chances of survival when
dispersing to a host, overwintering and/or overcoming
initial host resistance (e.g. penetration of the hard cuticle
or the epidermal tissue) (Kemen & Jones,2012; Wang &
Wang,2017).
Our results are congruent with previous research re-
porting small differences in spore size across functional
groups in Basidiomycota fungi, particularly when com-
paring the sexual spores of ectomycorrhizal and sapro-
trophic fungi suggesting than other reproductive traits,
such as sporocarp size and shape, might be more func-
tional (Bässler et al.,2014; Calhim et al.,2018; Halbwachs
et al.,2017; Kauserud et al.,2008). As we show here, this
small difference might be due to the already small size
of sexual spores of basidiomycete fungi relative to as-
comycete fungi, which prompts the hypothesis that for
the Basidiomycota the demand for small spores for the
launching platform leaves little room for differentiation
during evolution of the symbiotic lifestyle. In the case of
necrotrophic pathogens or plant endophytes, the over-
lap in spore sizes with asymbiotic fungi and their rel-
ative large variation in sizes (Figure2; FigureS3) may
reflect differences in the level of symbiotic specialization
(Mengiste, 2012) that is not captured with the current
classification. Plant pathologists have long speculated
that larger spores may provide the necessary resources
for highly host- specialized necrotrophs to overcome
host defences and infect healthy host tissue, while such
resources may be less important among less specialized
necrotrophic pathogens that can only infect weakened
plants (Garrett, 1970). We also found large variation
in spore size across asymbiotic saprotrophic fungi (for
any group or spore type; Figure2; FigureS3). This vari-
ation suggest the existence of different niches filled by
saprotrophic species, such as during decay of different
substrates or in different successional stages (Purhonen
et al., 2020). Finally, we also included in a separate
analysis the peculiar case of fungi that cause disease in
humans due to their importance. Most of these fungi
are described as opportunistic (i.e. causing disease in
immuno- compromised individuals (Kendrick, 2 017))
and are commonly found growing as free- living in na-
ture; these fungi are, thus, generally considered asymbi-
otic rather than symbiotic in the mycological literature
(Moore et al.,2011). Our results, however, show that such
fungi, despite their expected asymbiotic nature, have
on average smaller sizes than other asymbiotic fungi (a
pattern that holds across the phylogeny in some of our
models, Table sS3 and S4, Figure2). While it is not possi-
ble to pinpoint mechanisms, we hypothesize that smaller
spores for these fungi may enhance the likelihood to be
passively inhaled or ingested (Moore et al.,2011).
Relative importance of species’ symbiotic status
in explaining offspring size variation
Symbiotic status was also more important for explaining
interspecific variation in spore size than climate vari-
ables associated with the distributions of fungal species
(Table1). After symbiotic status, mean annual tempera-
ture was the second most important variable explaining
spore size variation across communities. This is con-
gruent with previous research highlighting that in some
species of mushroom- forming fungi, thicker spore walls
have higher resistance to UV light exposure and freez-
ing temperatures than species with smaller and lighter
spores (Norros et al.,2015). Possibly, for symbiotic fungi,
environmental microclimate plays a minor role as the
host will buffer these variables (e.g. fungal symbionts of
warm- blooded fungal symbionts will be buffered against
changes in environmental temperature).
Relationship between offspring size and
species’ geographic distributions depends on
symbiotic status
Finally, we tested the relationships between spore
size and geographic distributions for asymbiotic and

|
1531
AGUILAR- TRIGUEROS et al.
plant- associated fungal species, which we expect to be
negative if smaller offspring size facilitates spread of
propagules. Spore size was negatively correlated with the
geographic range of free- living fungal species (95% cred-
ible interval for slope of maximum geographic distance:
−0.71 to −0.11; 95% credible interval for slope of range
area: −1.01 to −0.14; Figure3) but not for symbiotic groups
(95% credible intervals for slope of maximum distance:
−0.23 to 0.01; 95% credible intervals for slope of range
area: −0.25 to 0.09; Figure3). In asymbiotic fungi, species
with larger spores had a more- limited geographic range
compared to species with smaller spores, which may
move more easily to new environments. Conversely, geo-
graphic range was unrelated to spore size for symbiotic
TABLE 1 Relative importance of symbiotic lifestyle versus climatic variables in explaining interspecific spore size variation. The fit of
two phylogenetic linear regression models with lifestyle and six climatic variables as explanatory factors is compared to the fit of models in
which one of these predictors was removed (indicated in the respective row). The f irst model uses the phylogenetic tree based on whole genome
sequences as provided in (Li et al.,2021), which includes 281 species from which we collected climatic data (referred to as the ‘genome tree
model’). The second model uses a taxonomy- based cladogram for species based on their taxonomy from kingdom to species level (referred to
as the ‘taxonomy tree model’), which includes 1137 species from which we collected climatic data. AIC, Akaike's Information Criterion; dAIC,
delta AIC (difference between the AIC of each model and the one containing all terms). A dAIC > 10 indicates no support for dropping that
term from the model because it results in a large decline in model fit; dAIC between 4 and 7 indicate considerably low support for dropping that
term; and dAIC<2 indicates strong support for dropping that term as it improves model fit (Burnham & Anderson,2002).
Phylogenetic regression model Adjusted r2L oglike AIC dAIC Phylogeny used
All variables 0.21 −336.72 699.43 Genome tree
0.09 −1328.2 2684.39 Ta xo nomy tree
(−) Symbiotic lifestyle 0.18 −341.41 706.82 7. 39 Genome tree
0.07 −1333.42 2690.85 6.45 Ta xono my tre e
(−) mean annual temperature 0.21 −337.97 699.9 4 0.51 Genome tree
0.09 −1328.23 2682.45 −1.9 4 Taxono my tre e
(−) mean annual precipitation 0.21 −337.25 698.49 −0.94 Genome tree
0.09 −1328.3 4 2682.68 −1.71 Taxono my tre e
(−) Temperature seasonality 0.22 −337.02 698.04 −1.39 Genome tree
0.09 −1328.23 2682.47 −1.93 Taxonomy tre e
(−) Precipitation seasonality 0.21 −337 698 −1.43 Genome tree
0.09 −1329.66 2685.32 0.93 Ta xo nomy tree
(−) Maximum solar radiation 0.18 −341.29 706.59 7.15 Genome tree
0.08 −133 0.52 26 87. 05 2.66 Taxono my tre e
(−) Minimum vapour pressure 0.22 −336.72 69 7.43 −2 Genome tree
0.09 −1328.25 2682.49 −1.9 Taxon omy tre e
FIGUR E 3 Asymbiotic fungal species exhibit a negative relationship between spore size and geographic distributions, while species
plant- associated fungi do not. (a, c). Relationship between spore size and geographic distribution (based on polygon area [a] and the maximum
distance between samples in which species were detected [c]) for asymbiotic fungal species and fungal species exhibiting varying degrees of
host association to plants. Fungal species were detected in global surveys of environmental DNA from soil and plant material. (b, d) Bayesian
models were fitted to estimate posterior distributions of the slope parameters representing the strength of the relationship between geographic
extent and spore volume. The density plot represents the likelihood that a value associated with the slope estimate was present in the posterior
distribution. These models included random intercepts representing the taxonomic order and spore type, as well as the primer set used to
amplify fungal DNA (Tabl esS6– S8). Only species producing a single spore type were used in this analysis.
6
−15
−10
−5
0
−10
−5
0
5
Spore size (
Geographic extent
(relative to maximum distance/area, logit)
(a)
−1.5 −1.0 −
0240.50.0
0
2
4
0
2
4
Slope estimate
Density
(b)
(d)
Free−livingPlant−associated
(c)
µm3)

1532
|
SYMBIOSIS ALTERS SPORE SIZE ECOLOGY
species, for which host- related factors (including the geo-
graphic spread of the host itself) may offset any differ-
ence in dispersal due to spore size. For example, smaller
spore sizes might actually reduce the chances of ‘landing’
on a suitable host because smaller spores remain more
easily aloft (Norros et al.,2014). The role of other spore
traits (such as appendage morphology or spore wall or-
namentation) must be assessed to fully understand the
dispersal of symbiotic fungi (Gareth Jones,2006).
DISCUSSION
In this study, we uncover massive variation in spore size in
the fungal kingdom whose ecology and evolution is partly
explained by transitions in symbiotic status of the species.
However, we also found that the direction of this effect (i.e.
shifts to smal ler or larger spore siz es in symbiotic fungi) and
its importance varies widely among symbiotic groups and
phyla. For plant- associated fungi in the Ascomycota, our
results provide support to the hypothesis that as symbiosis
transitions from facultative to obligate, large spore reserves
become more important for their survival during dispersal
to and assist colonization of the plant. The results empha-
size the critical role of symbiotic relationships in driving
the evolution of life- history traits, especially in Fungi and
suggest two avenues for further research. First, determin-
ing the mechanisms behind correlations between shits in
spore size along transition to symbiosis; and second, de-
termining why in some symbiotic groups and clades, spore
size does not change along symbiotic gradients. For exam-
ple, shifts to smaller spore sizes in symbiotic groups could
be explained by host transmission dynamics. In other sym-
biotic interactions, such as parasitic animals, it has been
proposed that small- sized offspring propagules are pro-
duced to increase the chances of transmission when hosts
are hard to locate (Poulin,2011). Exploring the influence of
host transmission dynamics on fungal reproductive ecol-
ogy can reveal intricate life- history strategies in the Fungi
beyond spore structures. Direct transmission between
hosts, for instance, may reduce reliance on spore dispersal
and instead utilize alternative structures like hyphal exten-
sions (as observed in mycorrhizal fungi (Bielčik et al.,2019))
or yeast phenotypes (as it is commonly seen in most insect
gut endosymbionts (Gibson & Hunter,2010)). In addition,
as host- symbiont specialization is a long- term evolutionary
process (Chomicki et al.,2020), the age of symbiosis might
be a predictor of reproductive trait changes (for both host
and symbionts). Thus, we propose that the reliance of fungi
in other ways of transmission other than spores might ex-
plain weaker correlation and symbiotic state we found in
some clades. In those cases, variation in spore size might be
driven by neutral processes such as drift (which we did not
test). In order to test these hypothesis it would be necessary
to include more species across different symbiotic lifestyles
in phylogenetic studies (James et al.,2020) and the need to
populate databases with fungal reproductive traits. Such
data would allow tests of even the most fundamental tenets
in life- history for the fungal branch of the tree of life, such
as the existence of trade- offs in offspring output- offspring
size or allometric scaling relationships between parent size
and offspring size.
Finally, information on the diversity of dispersal and col-
onization strategies among asymbiotic and symbiotic fungi
will be useful to forecast the impact of global change on eco-
system functions provided by fungi. For example, disease
risk caused by fungal plant pathogens is forecasted to change
with increasing global temperature (Chaloner et al.,2020).
Such changes are likely due to direct effects on survival of
spores during dispersal, and indirect effects of changing hab-
itat quality (e.g. host susceptibility). Information on fungal
dispersal strategies for symbiotic groups will refine forecasts
of pathogen expansions and likelihood of pathogen spillover
from natural ecosystems to croplands. Considering that
fungi represent the main cause of crop yield losses and are
a main threat to animal health (Fones et al.,2017 ), such re-
finements in forecasting are particularly relevant to maintain
food security and ecosystem health.
In summary, expanding the realm of life- history anal-
ysis beyond plants and animals to other diverse and im-
portant clades such as fungi highlights symbiosis as a
key biotic driver influencing the ecology and evolution
of offspring- size variation. Life- history frameworks are
biased towards free- living organisms (Falster et al.,2008;
Stearns, 1992) with relatively limited inclusion of par-
asitic animals (Poulin, 2011). Yet, symbiosis is perva-
sive through the entire tree of life (including animals
and plants) and, as we show here, it explains offspring
variation among major clades in the fungal kingdom.
Including symbiosis as a life- history parameter creates
the need for new theoretical frameworks to determine,
for instance, how much the host controls the offspring
traits of the symbionts (as in fungi, and possibly bacteria
and protists) and how much the symbionts control the
offspring traits of their macroorganism hosts.
AUTHOR CONTRIBUTIONS
CAAT conceived the study together with FSK, WKC,
JRP and MCR. WKC downloaded data from Mycobank.
FSK developed the text mining algorithm. CAAT, JRP,
CD and HZ mined the text data and cleaned spore data
entries. CAAT digitized manually the spore size data not
present in Mycobank, managed the spore database and
assembled the fungal functional database. JRP managed
and assembled climatic and geographic data. CAAT and
JRP performed statistical analysis with input from WKC
and FSK. CAAT wrote the first draft, and all authors
contributed to the writing of the paper.
ACKNO WLE DGE MENTS
We thank J. Antonovics and Tessa Camenzind for help-
ful comments. Noa Terracina helped sort out plant dis-
ease information. We thank Louis Weiss for providing
information on the natural history of microsporidian

|
1533
AGUILAR- TRIGUEROS et al.
fungi. We also thank anonymous reviewers for helpful
comments to this manuscript. Funding. This research
was supported by funding from the Federal Ministry of
Education and Research (BMBF) within the collaborative
Project ‘Bridging in Biodiversity Science (BIBS)’ (funding
number 01LC1501A) to MCR. CAAT was supported by a
Feodor Lynen Fellowship from the Humboldt Foundation.
MCR acknowledges support from an ERC Advanced
Grant (694368). CAAT, ICA, CD, HZ, MCR and JRP
were supported by the Australia- Germany Joint Research
Cooperation Scheme, an initiative of Universities Australia
(UA) and the Deutscher Akademischer Austauschdienst
(DAAD), for the project: ‘A new tool of the trade: Trait- ba sed
approaches in fungal ecology’. JRP acknowledges support
from the Australian Research Council (FT0100590). We
acknowledge the contribution of the Biomes of Australian
Soil Environments (BASE) consortium in the generation of
data used in this publication. The BASE project was sup-
ported by funding from Bioplatforms Australia through
the Australian Government National Collaborative
Research Infrastructure Strategy (NCRIS). TV and PK
were supported by the Czech Science Foundation (grant
21- 17749S to T. Vetrovsky). Research on microbial distri-
bution and colonization in the BKS laboratory is funded
by the Australian Research Council (DP190103714). SH ac-
knowledges funding from the German Science Foundation
(grant HE6183). SNK was supporte d by start- up funds from
the University of Tennessee, Knoxville. FTM acknowl-
edges support from the European Research Council (ERC
Grant Agreement 647038 [BIODESERT]) and Generalitat
Valenciana (CIDEGENT/2018/041). AEZ acknowledges
support from the National Science Foundation (DEB:
1623040, ‘MacroMycoFunc – Forming an integrated un-
derstanding of function across fungi’ and DEB: 1655759;
‘Collaborative Research: NSFDEB- NERC: Tropical dead-
wood carbon f luxes: Improving carbon models by incor-
porating termites and microbes’). Open access funding
enabled and organized by ProjektDEAL. Open Access
funding enabled and organized by Projekt DEAL.
FUNDING INFORMATION
Alexander von Humboldt- Stiftung, Grant/Award
Number: Feodor- Lynen Fellowship; Australian
Research Council, Grant/Award Number:
DP190103714FT0100590; Bundesministerium für
Bildung und Forschung, Grant/Award Number:
01LC1501A; Deutsche Forschungsgemeinschaft, Grant/
Award Number: HE6183; Deutscher Akademischer
Austauschdienst; Division of Environmental Biology,
Grant/Award Number: 16230401655759; Grantová
Agentura České Republiky, Grant/Award Number:
21- 17749S; H2020 European Research Council, Grant/
Award Number: 647038694368; Universities Australia
CONFLICT OF INTEREST STATEMENT
The authors confirm that there are no competing
interests.
PEER REVIEW
The peer review history for this article is available at
https://www.webof scien ce.com/api/gatew ay/wos/peer-
revie w/10.1111/ele.14271.
DATA AVA ILA BILITY STATEM ENT
We confi rm that all dat a and code used for th is paper have
been d eposite d in the d atabase Fu nFun: https://g ithub.com/
trait ecoev o/funga ltrait as well as in a Zenodo (10.5281/
zenodo.7953831) and GitHub repository (https://github.
com/aguil art/Symbi otic-status-and-fungal-spore-size).
ORCI D
Carlos A. Aguilar- Trigueros https://orcid.
org/0000-0003-0512-9500
Franz- Sebastian Krah https://orcid.
org/0000-0001-7866-7508
Amy E. Zanne https://orcid.org/0000-0001-6379-9452
Nerea Abrego https://orcid.org/0000-0001-6347-6127
Petr Baldrian https://orcid.org/0000-0002-8983-2721
Claus Bässler https://orcid.org/0000-0001-8177-8997
Andrew Bissett https://orcid.org/0000-0001-7396-1484
Baodong Chen https://orcid.org/0000-0002-1790-7800
Manuel Delgado- Baquerizo https://orcid.
org/0000-0002-6499-576X
Stavros D. Veresoglou https://orcid.
org/0000-0001-6387-4109
Haiyang Zhang https://orcid.org/0000-0001-7951-0502
Jeff R. Powell https://orcid.org/0000-0003-1091-2452
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SUPPORTING INFORMATION
Additional supporting information can be found online
in the Supporting Information section at the end of this
article.
How to cite this article: Aguilar- Trigueros, C.A.,
Krah, F.-S., Cornwell, W.K., Zanne, A.E., Abrego,
N., Anderson, I.C. et al. (2023) Symbiotic status
alters fungal eco- evolutionary offspring
trajectories. Ecology Letters, 26, 1523 –1534.
Available from: https://doi.org /10.1111/e l e .14271