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Copyright The University of Chicago 2020. Preprint (not copyedited or formatted). Please use DOI when citing or quoting. DOI: https://doi.org/10.1086/708273

Why are there so many flowering plants? A multi-scale analysis of plant diversification

Tania Hernández-Hernández1,2 and John J. Wiens1*

1
Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ, 85721-

0088, U.S.A.
2
Catedrática CONACYT asignada a LANGEBIO-UGA Cinvestav, Libramiento Norte Carretera

León Km 9.6, 36821 Irapuato, Guanajuato, México

*Corresponding author: e-mail: [email protected]

Keywords: angiosperms, diversification, macroevolution, phylogeny, plants, species richness

Article type: Article

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All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).
Copyright The University of Chicago 2020. Preprint (not copyedited or formatted). Please use DOI when citing or quoting. DOI: https://doi.org/10.1086/708273

ABSTRACT

The causes of the rapid diversification and extraordinary richness of flowering plants

(angiosperms) relative to other plant clades is a long-standing mystery. Angiosperms are only

one among 10 major land plant clades (phyla), but include ~90% of land plant species. However,

most studies that have tried to identify which traits might explain the remarkable diversification

of angiosperms have focused only on richness patterns within angiosperms, and tested only one

or a few traits at a single hierarchical scale. Here, we assemble a database of 31 diverse traits

among 678 families and analyze relationships between traits and diversification rates across all

land plants at three hierarchical levels (phylum, order, family) using phylogenetic multiple

regression. We find that most variation (~85%) in diversification rates among major clades

(phyla) is explained by biotically mediated fertilization (e.g., insect pollination) and clade-level

geographic-range size. Different sets of traits explain diversification at different hierarchical

levels, with geographic-range size dominating among families. Surprisingly, we find that traits

related to local-scale species interactions (i.e. biotic fertilization) are particularly important for

explaining diversification patterns at the deepest timescales, whereas large-scale geographic

factors (i.e. clade-level range size) are more important at shallower timescales. This dichotomy

might apply broadly across organisms.

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Introduction

Explaining the dramatic differences in diversification and species richness among major plant

clades is a long-standing and unresolved problem (Raven 1977; Stebbins 1981; Doyle and

Donoghue 1986; Friis et al. 1987; Crepet and Niklas 2009; Givnish 2010). Land plants currently

contain ~300,000 species distributed among 10 major clades (phyla sensu Niklas 2016). The

differences in richness among these clades are striking (fig. 1), with ~90% of described land

plant species belonging to angiosperms (flowering plants; Magnoliophyta). Given that

angiosperms also appear to be relatively young, they clearly have a high overall diversification

rate (speciation minus extinction; Morlon 2014). The challenge is to identify which traits might

help explain this accelerated diversification, including traits related to ecology, morphology,

physiology, reproduction, and genomic characteristics. More generally, to resolve the question of

why there are such dramatic differences in richness among major clades of land plants, we need

to know which traits are most strongly correlated with variation in diversification rates among

them.

Many studies have attempted to explain high angiosperm species richness in terms of

particular traits. Nevertheless, most studies had one or more of four limitations. First, many

studies focused specifically on explaining richness and diversification patterns among

angiosperm clades (e.g., Ricklefs and Renner 1994; Davies et al. 2004; Sargent 2004; Kay et al.

2006; Vamosi and Vamosi 2010; Bromham et al. 2015; O’Meara et al. 2016; Igea et al. 2017;

Magallón et al. 2019; recent reviews in Sauquet and Magallón 2018; Vamosi et al. 2018).

Although this is an important topic, these studies do not necessarily explain why angiosperms are

more diverse than other plant clades. Specifically, it is unclear whether traits that explain

variation within angiosperms will also explain differences between angiosperms and other major

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plant clades. Second, most studies have focused on testing the impacts of single (or a few) traits

on diversity and diversification, even though numerous traits have been proposed as possible

explanations for variation in species richness and diversification rates. Third, some studies have

not addressed how much variation in diversification rates or richness is statistically explained by

each trait. Thus, traits could show a significant association with diversification or richness, but

still explain little overall variation in diversification rates and richness among clades. Fourth,

some studies focused on richness patterns alone, without analyzing diversification rates directly.

This is important because land-plant clades differ considerably in their ages (fig. 1). Traits may

be especially important if they occur in younger clades with high richness (thus having rapid

diversification rates) rather than in older clades with high richness (since older clades are

expected to have more species, all else being equal). Here, we address these limitations, building

on previous studies that identified potentially important traits. The traits previously hypothesized

as drivers of diversification include tropical distributions (Ricklefs and Renner 1994),

zygomorphic flowers (Sargent 2004), floral nectar spurs (Kay et al. 2006), geographic extent

(Vamosi and Vamosi 2010), and rates of genome-size evolution (Puttick et al. 2015).

The factors that explain patterns of plant richness may also have implications beyond

plants. A prominent theme in ecology is that local-scale species interactions are most important

for explaining community diversity patterns at shallow timescales, whereas large-scale factors

(like geographic and climatic distributions) are important at deeper timescales. For example, this

idea was emphasized in a classic paper by Ricklefs (1987), and in other well-known papers (e.g.,

fig. 1 in Cavender-Bares et al. 2009). This idea raises the broader question: which types of traits

are most important for explaining richness and diversfication at different scales? Surprisingly,

recent studies in animals have shown the importance of traits related to local-scale species

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interactions for explaining deep-scale diversification patterns (Wiens et al. 2015; Jezkova and

Wiens 2017). However, these studies did not compare the importance of these interaction-related

traits relative to large-scale ecological factors. Here, we provide the first test of the hypothesis

that traits related to biotic interactions are more important for explaining diversification rates at

deeper timescales, relative to large-scale factors (like range size).

In this study, we perform a multi-scale analysis of diversification in land plants. This

analysis involves three main steps. First, we compile a database of 31 potentially relevant traits

for 678 families. We include traits related to fertilization (e.g., pollination mechanisms),

dispersal mechanisms, reproduction, life history (annual vs. perennial), genomic characteristics

(rate of genome-size change, polyploidy), and geographic range (e.g., range size, tropical vs.

temperate distribution). We then estimate the proportion of species in each clade having each

trait, at different phylogenetic scales. Specifically, we analyze data on 10 plant phyla, 140 orders,

and up to 678 families (Online Appendices A–J). Collectively, these higher taxa incorporate all

(or almost all) known land plant species. To our knowledge, these higher taxa are all

monophyletic, and thus represent clades. Taxonomic ranks are somewhat arbitrary, and named

clades may not represent a random sample of all possible clades in a tree (Beaulieu and O'Meara

2019). However, it is unclear how this issue would negatively impact our analysis. Furthermore,

the use of named clades allows us to incorporate all species in every clade (not just those

included in trees), and to readily address patterns at different scales (given that families are

generally younger than orders which are younger than phyla). Specifically, using the FPC tree

with all families (see below), the mean ages for land plant phyla, orders, and families are 393 Ma

(range=199–511), 149 Ma (48–428), and 79 Ma (7–428).

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Second, we estimate net diversification rates for each clade at each rank. Younger clades

with many species will have higher rates, and older clades with fewer species will have lower

rates (regardless of variation in rates within clades over time or among subclades). An important

advantage of using rate estimates for each clade (combined with regression) is that one can

include multiple variables simultaneously and quantify how much variation in diversification

rates among clades is explained by each trait at each scale, which is not possible using most other

approaches (e.g., SSE methods; FitzJohn et al. 2009).

Third, we test for pairwise relationships between each trait and diversification rates, using

phylogenetic generalized least squares regression (PGLS; Martins and Hansen 1997). PGLS

corrects for the potential non-independence of trait values and diversification rates among clades

due to phylogeny. We do this for each phylogenetic scale (phyla, orders, families), and both

across land plants and within angiosperms. We then conduct multiple regression analyses to

identify which combination of traits best explains variation in diversification rates at each scale.

This three-part approach (i.e., estimating trait frequencies and diversification rates within clades,

and then linking traits and rates with multiple regression) has now been successfully applied to

many organisms (e.g., Wiens et al. 2015; Jezkova and Wiens 2017). Note that we use “explain”

in a statistical sense, here and throughout.

Using this approach, we can explain considerable variation in diversification rates among

plant clades. Thus, our results help resolve the long-standing mystery of why major plant clades

differ so dramatically in their richness. Our results also show that different types of traits are

important for explaining diversification rates and richness patterns at different phylogenetic

scales. For example, biotic fertilization (e.g., insect pollination) explains considerable variation

in diversification rates among major plant clades (phyla). In contrast, geographic-range sizes of

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clades dominate diversification patterns at shallower timescales (among families). More

generally, these results contrast with the idea that traits related to local-scale species interactions

(like biotic fertilization) are primarily important for diversity patterns at shallower timescales

whereas large-scale geographic factors (like range size) dominate at deeper timescales.

Materials and Methods

Trait Database

An initial list of 678 land plant families (and their species richness) was obtained from Fiz-

Palacios et al. (2011). Data were then updated from various sources for bryophytes (Goffinet and

Shaw 2008; Goffinet et al. 2008; Vanderpoorten and Goffinet 2009) and ferns, gymnosperms,

and angiosperms (Kubitzki 1990–2015; The Plant List 2013; Stevens 2015).

We focused on traits previously hypothesized to be associated with increased species

richness or diversification rates of plant clades, following major reviews (e.g., Crepet and Niklas

2009; Givnish 2010) and previous studies (see above). However, we did not focus simply on

synapomorphies of clades. We also emphasized traits with data available for most phyla,

although we included some angiosperm-specific traits (e.g., flower morphology) and some

lacking data in some families (see below). The traits are listed in table A1 (Online Appendix A).

We describe the traits in further detail and how taxa were assigned to each state in app. A. We

did not always follow conventional terminology for trait names (app. A), because different

names have sometimes been applied to the same feaure in different groups (e.g., pollination vs.

fertilization). Data for each family (including literature sources), order, and phylum are given in

apps. B–H. All data are available in the online appendices, which are deposited in the Dryad

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Digital Repository: https://doi.org/10.5061/dryad.5tb2rbp10 (Hernández-Hernández and Wiens

2019).

We typically estimated the number of species in each family having each state based on

genus-level descriptions and richness (given the challenge of scoring 31 traits for ~300,000

species). This approach was potentially problematic when genera were variable for a given trait,

but the potential distortion of estimated trait frequencies should have limited impact on our

results, given that our analyses are among phyla, orders, and families, not genera. Specifically,

distortion should decrease at higher levels (i.e., the effects of variable genera on frequency

estimation should be mitigated by invariant genera and families at the level of orders and phyla;

app. A). Furthermore, analyses linking diversification rates and trait frequencies of clades can be

robust to considerable error in assigning traits to species (at least ~20%; Moen and Wiens 2017;

their app. B). We emphasize that trait frequencies are estimates, not known values. Some traits

were also coded at the family level (e.g., zygomorphy), and we also incorporated species-level

information in some cases (app. A).

For most traits, each clade was characterized by the estimated proportion of species

having that trait. Species in different clades (or even the same clade) need not share the same

trait through a single evolutionary origin. Indeed, statistical relationships from PGLS can be

stronger if traits arise independently in different clades. These analyses do not assume that each

trait originated concomitantly with the origin of a given clade. Instead, they assume that traits

that are more frequent among species in a clade can more strongly influence the clade’s overall

net diversification rate.

We acknowledge that there are scenarios whereby trait frequencies might appear to be

related to diversification, but without a causal relationship. For example, imagine a clade with

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two subclades (A and B), with the trait of interest in A but increased diversification in B

(Jezkova and Wiens 2017). However, this problematic scenario would need to be repeated across

multiple clades to yield a strong relationship between the trait and diversification, which seems

unlikely. Moreover, our analyses across multiple scales should reduce these artifacts (i.e.,

treating A and B as separate clades).

It is also possible that we failed to include one or more relevant traits. Nevertheless, to

our knowledge, we included more traits than any previous analysis of plant diversification.

Furthermore, this same criticism could apply to any study, no matter how many traits were

included. Finally, our results show that we identified important traits that explain considerable

variation in diversification rates at many scales.

Time-Calibrated Phylogenies

We used three tree topologies at each of three taxonomic levels (phyla, orders, families). We also

analyzed angiosperm orders and families separately. We also performed separate family-level

analyses within the more diverse non-angiosperm clades (bryophytes, liverworts, ferns, and

gymnosperms). However, our trait sampling did not focus on these latter groups.

Our primary analyses used a time-calibrated phylogeny that combined a comprehensive

tree of land-plant families (Fiz-Palacios et al. 2011) with a more recent phylogeny of angiosperm

families (Magallón et al. 2015). The former tree (Fiz-Palacios et al. 2011) includes all land-plant

families (Stevens 2015) and was estimated from concatenated plastid and nuclear genes. The

topology is broadly congruent with more recent studies having more extensive gene sampling but

more limited taxon sampling (e.g., Wickett et al. 2014; APGIII 2016). The phylum-level

relationships and divergence times are very similar to those of Magallón et al. (2013), and

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broadly similar to Morris et al. (2018). However, we utilized the tree of Fiz-Palacios et al. (2011)

given its more comprehensive sampling of families.

The primary tree of Fiz-Palacios et al. (2011) was calibrated by fixing the age of eudicots

at 121 Ma, using 16 calibration points, and setting a maximum age of 725 Ma. We refer to this as

the unconstrained phylogeny (FPU). These authors also performed an analysis that constrained

the maximum age of angiosperms to a young age (130 Ma) similar to other estimates. We refer

to this as the constrained phylogeny (FPC).

Our main analyses combined the non-angiosperm portion of the FPC tree with a more

recent angiosperm tree (Magallón et al. 2015). The latter study is the most extensive dating

analysis of higher-level angiosperm phylogeny to date, including 792 taxa and 137 fossil

calibration points. We first pruned this tree to include one species per family (note: all species

have the same length to the family stem age). Next, we substituted the angiosperm portion of the

FPC tree with this pruned tree (Magallón et al. 2015). We refer to this as the FPCM tree. The

dates for angiosperm origins within these trees differ only by ~9.4 Myr (within the confidence

interval from Magallón et al. 2015). The FPCM tree was used for the main analyses, but we

addressed the robustness of the results with two alternative trees (FPU, FPC). At the family level,

these two source trees (Fiz-Palacios et al. 2011; Magallón et al. 2015) differ in taxon sampling

and treatment of some groups. Thus, we assembled different databases for angiosperms and land

plants (apps. E–H). The FPC and FPU trees and databases included 678 families, whereas the

FPCM tree and database included 603. The three trees differed primarily within angiosperms.

Trees were pruned to obtain phylogenies at the order and phylum levels (i.e., including one

terminal taxon per order and phylum). The stem age for angiosperms is the same in the FPC and

FPCM trees. Therefore, we used only two pruned topologies for analyses among phyla

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(FPCM/FPC and FPU). All trees used are available in app. I. Overall, different trees had

relatively little impact on our conclusions (see Results), so we focused primarily on the preferred

FPCM tree.

Diversification Rates

Net diversification rates for each clade were estimated using the standard method-of-moments

estimator for stem-group ages (Magallón and Sanderson 2001), with the R package GEIGER

version 2.0.6 (Pennell et al. 2014). Many other approaches are available to study diversification

(Morlon 2014). However, most other methods would be impractical here, since they utilize

detailed species-level phylogenies within each clade, which are unavailable for many plant

clades. Furthermore, the use of net diversification rates makes it straightforward to use

regression to assess how much variation in rates is explained by each trait. This would be

impossible to infer using most other methods (e.g., SSE models). Finally, our goal here is to

explain differences in richness and diversification rates among clades, and not shifts in

diversification rates over time.

Diversification rates were estimated using the stem-group estimator. The crown-group

estimator requires a time-calibrated tree with many species per clade (currently difficult for

many families), whereas the stem-group estimator requires only one species per clade.

Furthermore, incomplete species sampling can bias rate estimates using crown ages (by

underestimating crown ages), but not stem ages (Meyer and Wiens 2018). Most importantly,

stem-based estimators generally show stronger relationships with true rates in simulations, even

with complete taxon sampling (Meyer and Wiens 2018).

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The method-of-moments estimator requires the age and species richness of each clade,

and a relative extinction fraction (epsilon). Epsilon is intended to correct for the overestimation

of diversification rates due to the failure to include extinct clades (a potential source of

“ascertainment bias” when estimating diversification rates; Beaulieu and O'Meara 2019). It is

typically assumed across an entire tree, and not estimated within individual clades. Following

standard practice, three values (0, 0.5, 0.9) were used. Results were similar across different

values (see Results). Therefore, we primarily focused on the intermediate value (0.5). In

simulations, different epsilon values yield similar relationships between true and estimated rates

for the stem estimator (Meyer and Wiens 2018). Use of a single epsilon value does not assume

that extinction rates are identical in all clades: diversification rates within clades reflect the

balance of speciation and extinction over time, and estimated diversification rates can still

accurately reflect the true rates when a single epsilon value is assumed but extinction rates vary

among clades (Meyer and Wiens 2018).

Some authors (Rabosky et al. 2012) have stated that these rate estimators require constant

rates within clades, and are only valid if there is a positive relationship between clade age and

species richness among clades. However, true and estimated rates are strongly correlated in

simulations, regardless of whether there is a positive or negative relationship between clade age

and richness or between clade age and diversification rates (Kozak and Wiens 2016), and

regardless of variation in rates between subclades within a clade (Meyer and Wiens 2018) and

within clades over time (Meyer et al. 2018). Thus, these estimators can correctly assign high net

rates to young clades with many species and low net rates to older clades with few species.

Nevertheless, fast diversification rates in younger clades can potentially uncouple diversification

rates and richness patterns, which would make it problematic to interpret diversification rates as

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explaining richness patterns (Kozak and Wiens 2016; Scholl and Wiens 2016). Strong positive

relationships between age and richness can also yield weak relationships between diversification

rates and richness (Kozak and Wien 2016; Scholl and Wiens 2016). Therefore, it is important to

test whether diversification rates and richness are significantly related. The mere fact that

richness is included in the calculation of diversification rates does not make such an analysis

“circular” since these variables can be unrelated (Kozak and Wiens 2016; Scholl and Wiens

2016). We confirmed that diversification rates and richness are strongly related at all levels (app.

K). For phyla, the r2 between richness and diversification rates ranged from 0.80–0.92 (across

trees and epsilon values), for orders from 0.75–0.86, and for families from 0.40–0.74 (with lower

values in more complete family-level trees). Thus, diversification rates are relevant for

explaining richness patterns among clades, especially for orders and phyla. Yet, diversification

rates and richness are not identical, especially among families (despite studies that focused on

explaining family-level richness without incorporating diversification rates).

In general, variation in richness among clades can be explained by variation in their

diversification rates (speciation-extinction) and/or ages (e.g., Scholl and Wiens 2016), because

only speciation and extinction directly change richness in a clade. We confirmed that all

relationships between clade ages and richness were weak and negative, using the FPCM tree

among land plant phyla, orders, and families (app. K). This further confirms that variation in

richness is explained by variation in diversification rates.

Finally, we also performed analyses among phyla using diversification rates estimated

from the crown-group age of each clade. This was important because the crown-age of

angiosperms may be substantially younger than the stem age (leading to slower diversification

rates considering only stem-group estimates). Phylum-level analyses should not suffer from

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incomplete species sampling, because all major clades within each phylum were sampled. We

used ε=0.9, given that crown-group estimates are most accurate using this value in simulations

(Meyer and Wiens 2018). We used only the FPC tree, the tree with the younger age estimate for

crown-group angiosperms.

Testing Relationships Between Traits and Diversification Rates

We estimated relationships between diversification rates (dependent variable) and other traits

(independent variables) using PGLS regression with the R package caper version 0.5.2 (Orme

2013). Following standard practice, we used the maximum likelihood transformation of branch

lengths optimized for the data (lambda=ML), based on the estimated phylogenetic signal

(lambda). Kappa and delta branch-length transformations were fixed at 1. Lambda estimates and

corrects for the observed phylogenetic signal in the data, but does not require that all traits

evolve following a Brownian motion model. PGLS is also valid when independent variables are

categorical and the dependent variable is continuous (like diversification rates: see Martins and

Hansen 1997).

We first did pairwise regression analyses between diversification rates and each trait. We

then performed multiple regression analyses with models that included only those traits showing

significant (P<0.05) and marginally significant (P<0.10) relationships. Excluding some traits

was especially important given the many traits considered (i.e., the number of possible trait

combinations would be intractable, but many combinations would be suboptimal given traits

with weak relationships in pairwise analyses). We did not correct P-values for multiple

comparisons, because our goal was simply to identify candidate traits for inclusion in multiple

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regression models. Multiple regression models were then chosen based on their overall fit, not

their P-values.

In multiple regression analyses, all candidate traits were included and then sequentially

excluded (i.e., backward elimination). Thus, after running the first multiple regression model, the

trait with the highest P-value was excluded and the analysis was rerun. We repeated this process

until models included only two variables. Preliminary analyses using other variable-selection

procedures (e.g., forward selection) yielded similar results. The best-fitting model was generally

considered the one with the lowest AIC (Akaike Information Criterion; Burnham and Anderson

2002). However, models within 0–4 AIC units may be considered indistinguishable from the best

model (Burnham and Anderson 2002). When the best models differed by only 0–4 units, we

selected the model including the fewest traits. No analyses included more traits than taxa. Traits

that are highly correlated should be removed by this selection procedure, since redundant traits

will add unnecessary parameters without increasing model fit. We also confirmed that for our

best-fitting models (table 1), the relationships between included traits were either non-significant

or very weak (all r2<0.12, with most r2<0.05; app. P).

Prior to these analyses, we excluded traits with a low frequency in all taxa in each dataset

(<10% of species having that trait across all clades). It would be problematic to infer that a trait

was responsible for a clade’s high diversification rate if that trait were present in relatively few

species. The specific value (10%) is arbitary, but alternative values should have little impact,

given that the traits in the best-fitting models either do not involve frequencies (e.g., number of

ecozones, rates of genome-size evolution) or differ strongly in frequencies among taxa (e.g.,

biotic fertilization, tropical distribution, annual life history, zygomorphic flowers, non-water

dispersal).

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Some traits had missing data in some taxa, such as reproductive traits in poorly studied

families. Thus, our data for each trait at each taxonomic level had different proportions of

missing data (0–0.70; app. J). Mean completeness per taxon varied based on taxonomic level

(family=0.80: range:0.20–1.00; order=0.87; range:0.31–1.00; phylum=0.90: range:0.77–1.00).

PGLS analyses eliminate taxa with any missing values (Orme 2013). We used two strategies to

deal with missing data. First, to minimize data loss in each round of analyses, we excluded traits

with extensive missing data across taxa (>0.30, see app. J). However, deleting observations with

missing data reduces statistical power and can increase estimation bias (Nakagawa and

Freckleton 2008). Therefore, we also used phylogenetic imputation to fill in missing data, with

the R package Rphylopars (Goolsby et al. 2016). Imputation uses a phylogenetic covariance

matrix to estimate trait values in taxa lacking data for that trait. To estimate the covariance

matrix, we first fit three evolutionary models to each dataset: Brownian Motion, Ornstein-

Uhlenbeck, and Early-Burst (Goolsby et al. 2016). We selected the best-fitting model based on

AIC values and then used this model to estimate the covariance matrix with likelihood. The final,

imputed matrix had no missing data. Details are given in app. Q. Imputed data are in apps. B–H.

Importantly, PGLS results from the reduced datasets and the imputed data were similar (e.g.,

compare tables R1 and R2, and table 1 to table R3). This similarity is not surprising, given the

limited missing data overall (~10–20% see above). For brevity, the main analyses were based on

the imputed dataset, which is more complete.

Finally, for the best-fitting multiple regression models for the main results (FPCM tree,

ε=0.5; imputed data), we calculated standardized partial regression coefficients (SPRC) for each

variable (code from Moen and Wiens 2017). These coefficients quantify the relative importance

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of different variables in the multiple regression models, showing the influence of each variable

when all others are held constant (Sokal and Rohlf 1995).

Among angiosperm families, the three traits related to range size (geographic extent,

number of ecozones, and area available for expansion) were strongly associated with each other

(r2=0.7–0.8; P<0.0001; app. K). For these analyses, we included only the trait showing the

highest r2 and lowest P-value in multiple trait models (geographic extent). For analyses across

land plants and in non-angiosperm taxa, we used the number of ecozones, since precise data on

geographic extent and available area were not available. We used the eight ecozones from

Vamosi and Vamosi (2010: Nearctic, Neotropical, Palearctic, Afrotropical, Indo-Malayan,

Australasia, Oceania, Antarctic) and tallied the number of ecozones that each clade occurred in.

Results

Phylum-Level Analyses

The phylogeny, species richness, and diversification rates of the 10 phyla are summarized in

figure 1. For this and all other analyses, we describe results using our preferred tree (FPCM),

imputed data (for missing entries), and an intermediate ε (0.5; see apps. K–L for complete

results). Twenty-three traits were individually tested for relationships with diversification rates

(table R1; app. K), excluding 8 traits relevant only to angiosperms or having low frequencies.

Five traits showed significant or marginally significant relationships (table R1, app. K). The best-

fitting model included two traits (table 1, app. L), and explained 85% of the variation in

diversification rates. Standardized partial regression coefficients (SPRC) showed that the most

influential trait was biotic fertilization (0.51) followed closely by range size (0.48; number of

ecozones). Among phyla, biotic fertilization was present at high frequencies (>10%) only in

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angiosperms (87%) and cycads (75%), and is predominantly mediated by insects in both groups

(app. B). Range size is largely invariant among phyla (80% are present in all or almost all 8

ecozones), but the phylum with the lowest diversification rate (Gingkophyta) is present in only

one (app. B). These two traits together explain most variation in diversification rates among

phyla, but biotic fertilization is clearly the one most relevant to the rapid diversification of

angiosperms. Models including two additional variables (genome-size rates, tropical distribution)

explain more variance in diversification rates (93%), but have almost identical fit (app. L).

Results were generally similar across topologies, epsilon values, and non-imputed

matrices (tables R2–R3, app. L). Specifically, the best-fitting model included biotic fertilization

and range size, and explained similar amounts of variance in diversification rates. However,

using the non-imputed data and ε=0.9, rates of genome-size evolution were also included in the

best-fitting model, and using the FPU tree, non-imputed data, and ε=0.9, the best-fitting model

included biotic fertilization, range size, dioecy, and annual life history, and explained 97% of the

variance in diversification rates. Analyses using crown-age rate estimates (app. O and

emphasizing variables present in >25% of species) supported a model including only biotic

fertilization and genome-size rates (but not range size), which explained 90% of the variance.

Order-Level Analyses Across Land Plants

Twenty-five traits were analyzed among the 140 land plant orders, excluding traits present only

in angiosperms (e.g., floral characters, table A1, app. K). Many traits showed significant

relationships with diversification rates in pairwise analyses (table R1, app. K), but only one

explained >10% of the variation in diversification rates (number of ecozones: 43%). The best-

fitting model included seven traits and explained 56% of the variance in diversification rates

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among orders (table 1). The number of ecozones was the most influential trait (SPRC=0.30).

Biotic fertilization was also influential (0.16), as was non-water fertilization (0.23). Although

these two variables might seem redundant, they were not significantly related (r2=0.108;

P=0.35). Annual life history, rate of genome-size evolution, non-water dispersal, and polyploidy

were also included in the model, but showed smaller effects (SPRC=0.06–0.09; table 1). Results

were broadly similar using alternative data, trees, and rate estimates, with range size and annual

life history being consistently important, along with traits related to fertilization and dispersal

(app. L).

Angiosperm Order-Level Analyses

A total of 28 traits were analyzed among the 66 angiosperm orders (app. K). Twelve traits

showed significant or marginally significant relationships with diversification (app. K). Besides

number of ecozones (r2=0.54), all remaining traits explained 20% or less of the variation in

diversification rates (table R1). The best-fitting multiple regression model explained 72% of the

variation (table 1), and included four traits: number of ecozones (SPRC=0.43), annual life history

(0.20), zygomorphic flowers (0.22), and non-water dispersal (0.12). Analyses using alternative

data, trees, and rate estimates consistently supported range size and annual life history as

important, and almost always supported zygomorphic flowers, whereas inclusion of other traits

(e.g., dispersal, fertilization, growth form) was more variable (app. L).

Land Plant Family-Level Analyses

Twenty-five traits were analyzed among 603 families (app. K). Many showed significant

relationships in pairwise analyses. The number of ecozones explained 42% of the variation, and

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other traits explained 5% or less (table R1). The best fitting model included six traits, and

explained 45% of the variation (table 1), with the number of ecozones being the most important

(SPRC=0.55) and other traits less so (SPRC=0.05–0.22; annual life history, biotic fertilization,

non-water dispersal, rates of genome-size evolution, tropical distribution). Across trees, data, and

rates, the variables included in the best-fitting model varied substantially, but always included

range size and non-water dispersal, and only sometimes included biotic fertilization (app. L).

Angiosperm Family-Level Analyses

Thirty traits were analyzed among 363 angiosperm families (app. K). Seventeen showed

significant or marginally significant relationships (app. K). Most explained relatively little

variation in diversification rates, but the three traits related to range size each explained

substantial variation (>40%; table R2). The best model explained 54% of the variation and

included six variables (table 1). Geographic extent was the most influential variable

(SPRC=0.57), whereas other traits had weaker effects (zygomorphic flowers, biotic fertilization,

epiphytic habit, rates of genome-size evolution, and non-water dispersal). These results were for

the FPCM tree, which did not include all angiosperm families. Analyses using alternative trees

that did include all families, and using alternative rates and data, all consistently supported range

size (geographic extent). Inclusion of other variables in the best-fitting model varied (app. L), but

typically included zygomorphic flowers, biotic fertilization and/or herbaceous growth form.

Non-Angiosperm Clades

Few studies have addressed correlates of large-scale diversification patterns in non-angiosperm

clades. Analyses of the clades with the most families (mosses, liverworts, ferns, gymnosperms)

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showed that range size (number of ecozones) was strongly related to diversification rates in all

four (table 2; app. M). This variable alone explained considerable (56%, app. L) variation in

diversification rates in gymnosperms. Range size and tropical distribution were the most

important variables in mosses and liverworts (together explaining 44% and 30% of the total

variance in each group, respectively; table 2; app. N). Range size and leaf-vein density were

most important in ferns (40%).

Discussion

In this study, we conducted a multi-scale analysis of diversification among land plant clades. At

each scale, we identified a limited set of traits that explained considerable variation in

diversification rates. Among phyla, most variation (85%) was explained by biotic fertilization

(pollination) and range size (table 1). More specifically, the rapid diversification of angiosperms

was largely explained by biotic fertilization. Furthermore, these two traits (biotic fertilization,

range size) remained influential among land-plant orders, with smaller contributions from other

traits. Within angiosperms, most variation among orders (72%) was explained by range size,

along with annual life history, zygomorphic flowers, and non-water dispersal. Range size was

then the most important trait at the family level among land plants, within angiosperms, and

within non-angiosperm clades (tables 1, 2). Overall, these results contrast with the idea that

species interactions (like biotic fertilization) are important primarily at shallow timescales

whereas large-scale geographic factors (like range size) are important at deeper timescales.

Below, we discuss patterns across land plants and angiosperms, focusing on biotic fertilization

and range size (not all traits), and then discuss broader implications beyond plants.

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Patterns Across Land Plants

A major goal of our study was to analyze patterns across all land plants, not merely angiosperms.

Few studies have examined correlates of diversification at this scale. One study (Puttick et al.

2015) analyzed genome sizes and rates of genome-size evolution across land plants. We

confirmed that genome-size rates are significantly related to diversification (app. K), but this

variable is not included in the best-fitting model (table 1).

We strongly supported the importance of biotic fertilization, and the idea that flowers

drove rapid angiosperm diversification. We acknowledge that almost any trait unique to

angiosperms and widespread among them might show a significant relationship with

diversification rates among phyla, given the high rate in angiosperms. At the same time, few

traits actually had such a distribution. In fact, we did not directly include flowers or fruit. Instead,

we treated mechanisms of biotic and abiotic fertilization and dispersal as traits, including specific

abiotic mechanisms (wind, water) and biotic agents (insects, vertebrates). Our analyses did not

support vertebrate or biotic seed dispersal (e.g., fruit) as major drivers of diversification. Indeed,

neither trait is present in >50% of angiosperm species and they actually show higher frequencies

in another phylum (Gnetophyta). Instead, we supported biotically mediated fertilization in

general (present in 87% of angiosperms; app. B), and insect-mediated fertilization in particular

(in 70%), as explanations for high angiosperm richness. Among phyla, biotic fertilization is

largely confined to angiosperms and cycads, where it occurs at high frequencies (and at very low

frequencies in Bryophyta and Gnetophyta). This trait presumably evolved independently in each

group. Intriguingly, cycads also have relatively high diversification rates (see also Nagalingum et

al. 2011), especially based on their crown-group ages (app. O). Thus, biotic fertilization itself

seems to be important, not just flowers.

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Biotic fertilization (i.e., animal pollination) has long been suggested as a key to

angiosperm success (e.g., Stebbins 1981; Niklas 2016). Nevertheless, the specific mechanisms

linking diversification and flowers remain an area of active investigation (Crepet and Niklas

2009; Van der Niet et al. 2014). Pollinator-mediated divergence in floral traits is considered an

important reproductive isolating mechanism in plants (Grant 1949, 1981; Raven 1977; Doyle and

Donoghue 1986; Crepet and Niklas 2009). Yet, the observation that specialist pollinator species

are infrequent (Robertson 1929; Ollerton et al. 2009) suggests that there is not a simple one-to-

one relationship between pollinator shifts and speciation. Nevertheless, there are dramatic

differences in flower morphology that appear to have evolved in association with particular

groups of pollinator species (Harder and Barrett 2006). Furthermore, particular flower

morphologies (i.e., zygomorphy) significantly impacted diversification rates within angiosperms

(table 1). Specifically, zygomorphy is thought to be important in restricting access to pollen by

non-specialist pollinators and thereby increasing pollinator specificity and reproductive isolation

among plant species (review in Sargent 2004). Biotic fertilization might also influence

diversification without being so directly linked to speciation. For example, Raven (1977)

suggested that insect pollination was advantageous in increasing accurate transfer of pollen

among widely spaced conspecific individuals. This could increase range sizes and buffer species

from extinction. Overall, there is an extensive literature on pollination biology and speciation,

which is too vast to review here (see instead Kay et al. 2006; Crepet and Niklas 2009; Givnish

2010; and others). Our results strongly support the idea that biotic fertilization drives large-scale

patterns of plant diversification, and should provide greater impetus for smaller-scale studies on

the specific mechanisms by which flowers drive speciation and diversification.

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Our study does not address patterns of diversification over time, but rather variation in

extant richness and net diversification among clades. However, since net diversification rates

reflect both speciation and extinction, our results are fully compatible with the idea that some

species-poor extant clades (e.g., ferns, gymnosperms) were once more species-rich than they are

today (Niklas 2016).

Patterns within Angiosperms

Many previous studies have addressed diversity patterns in angiosperms (see Introduction), and

we expand upon them by including many variables, considering different scales (orders,

families), and utilizing diversification rates instead of richness. Our results show several areas of

agreement with these studies. For example, we supported the importance of range sizes (e.g.,

Vamosi and Vamosi 2010; Tang et al. 2017), although previous studies analyzed richness rather

than diversification rates. Our results also supported zygomorphic flowers (Sargent 2004) and

rates of genome-size evolution (Puttick et al. 2015). We also found annual life history and non-

water seed dispersal (including biotic and wind) to be important, especially among orders (table

1). Dispersal modes were included in some analyses of angiosperm diversity (e.g., Ricklefs and

Renner 1994) and may increase diversification by facilitating range expansion (see below).

Annual life history is less studied, but can decrease generation times and thereby increase the

potential for rapid evolutionary change. Overall, our study is unique in combining these traits

and showing that each remains important when considered in the context of the others (table 1).

Interestingly, we found that range size is the most important variable among angiosperm orders

and families (table 1), and among orders and families across all land plants.

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We explained considerable variance in diversification rates among angiosperm orders

(72%) and families (54%; table 1), but some remained unexplained at each level. This remaining

variance might be explained by variation in substitution rates (e.g., Bromham et al. 2015), rates

of change in seed size (e.g., Igea et al. 2017), and other aspects of flower morphology (e.g.,

O’Meara et al. 2016).

Effects of Range Size

Our results on range size raise at least three important questions for future research. First, does

range size actually drive diversification or does diversification drive range size? Second, how

does range size increase diversification? Third, why do some clades have larger range sizes than

others?

Faster diversification rates might contribute to larger clade range sizes, especially by

driving higher species richness. Higher species richness within a region might then facilitate

dispersal among regions. However, many clades can be broadly distributed without high species

richness, including a family with one species shared across all 8 regions (Lunulariaceae; app. F).

Many broadly distributed low-richness families are in Bryophyta and Marchantiophyta, but some

are angiosperms (e.g., Nelumbonaceae, with 2 species across 5 regions, Ceratophyllaceae with 6

in 6). Interestingly, the most diverse plant families (Orchidaceae, Asteraceae, Fabaceae) occur in

only 7 regions, not all 8. Thus, high richness is not necessary (or sufficient) for dispersal among

all regions, and there is considerable variation in diversification rates unrelated to range size. Our

results do not resolve this issue, but they should motivate further research on the mechanisms

linking range area and diversification in plants, which could disentangle the causal relationships

between these variables.

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If clade range sizes primarily drive diversification instead of the converse, how might this

occur? In general, large range sizes may provide more opportunities for allopatric speciation, and

might buffer clades from extinction (Rosenzweig 1995). Future studies that separately estimate

speciation and extinction rates (e.g., with species-level phylogenies) could address how these

two processes are related to range sizes of clades. Dispersal to new regions might also increase

diversification rates by creating new ecological opportunities (e.g., Vamosi and Vamosi 2010;

Yoder et al. 2010), and this should also be tested.

The third question is: why do some clades have larger range sizes than others? This could

be addressed by testing which traits are most strongly related to clade range sizes, such as

different seed-dispersal mechanisms. Note that range sizes in some clades might be influenced

by range contractions over time, not merely expansions.

Broader Implications

Beyond plants, our results offer insights into the general factors that drive diversification. By

analyzing many kinds of traits at different levels (phyla, order, family), our results address

whether the types of traits that are most important in driving diversification change with

phylogenetic scale. Intriguingly, our results here concur with recent studies in animals showing

the importance of traits related to local-scale species interactions (between unrelated clades) as a

major driver of diversification patterns at deep timescales (i.e., with clades that originated ~500–

200 Ma; fig. 1). For example, herbivory increases diversification rates among insect orders

(~500–100 Ma; Wiens et al. 2015), as does parasitism among animal phyla (~900–300 Ma;

Jezkova and Wiens 2017).

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Furthermore, our results show that a trait related to local-scale species interactions (biotic

fertilization) is as important for explaining diversification patterns as large-scale geographic

factors at this deep phylum-level scale (table 1). Yet, traits related to large-scale distributions

(i.e., range size) were the most important at shallower timescales, especially among families

(tables 1–2). These results contrast with the idea that local-scale interactions are less important

for diversity patterns at deeper timescales relative to large-scale geographic factors (Ricklefs

1987).

These interpretations are based on standardized partial regression coefficients from the

best-fitting models (tables 1–2). However, the shift in the relative importance of range size and

biotic fertilization across scales is also apparent from pairwise regression (app. K). Range size

and biotic fertilization separately explain similar amounts of variance in diversification rates

among phyla (47–72% vs. 31–57%: among trees and ε values), whereas range size explains

much more among land plant orders (32–44% vs. 4–17%) and even more among families (23–

41% vs. 1–6%).

We speculate that these scale-specific patterns might be explained by greater variability

in traits related to local-scale interactions at deeper timescales, and greater variability in large-

scale geographic factors at shallower timescales (Wiens 2017). For example, most phyla are

cosmopolitan in distribution, reducing potential differences in range size among them (60% in all

8 ecoregions, compared to only 12% of 603 families; apps. B, F). Conversely, biotic fertilization

varies among plant phyla but is relatively invariant within most clades (i.e., present in most

angiosperms and cycads, but absent in most other major clades).

We acknowledge that levels of variability in these traits can depend on how they are

defined. For example, biotic fertilization is defined broadly here, not in terms of specifc

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pollinator species (which would be more variable). Nevertheless, traits were defined the same

way across all scales here, allowing for comparison.

Finally, we note that “deep” vs. “shallow” may depend on the study. The deeper

timescales here are similar to those in studies of animal phyla and insect orders, with plant phyla

having a mean age of 393 Ma and orders with a mean age of 149 Ma. However, our “shallow”

timescale here might be considered relatively old (mean=91 Ma for the FPCM tree). Regardless,

the generality of these patterns will require testing across many other groups, traits, and

timescales.

Conclusions

In summary, we provide an analysis of land plant diversification based on multiple traits at

multiple phylogenetic scales. We show that different traits are important at different scales, and

that multiple traits are important at every scale. Thus, focusing on a single trait at a single scale

may be problematic. At the largest scale (phyla), biotic fertilization (e.g., insect pollination)

helps explain the extraordinary richness of flowering plants. Thus, local-scale species

interactions seem to help drive diversity patterns at deep phylogenetic scales. Conversely,

variation in geographic range sizes of clades dominates diversification patterns at shallower

timescales (among families). Overall, these results run counter to the idea that local-scale

interactions are primarily important at shallower timescales and large-scale distributions

dominate at deeper timescales.

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Acknowledgments

For their help in compiling data for this study, we thank the following undergraduate students:

B. K. Mayer, P. Santoro, K. Croneigh, and J. Delbert. We thank D. Moen for providing R code

for calculating partial regression coefficients. We thank M. Sanderson, D. Kerkhoff, A. Winn,

C. Bacon, and anonymous reviewers for helpful comments on the manuscript. THH was

supported by a joint postdoctoral fellowship from CONACYT and the University of Arizona.

JJW was funded by U.S. National Science Foundation grant DEB 1655690.

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Tables

Table 1: Results of multiple regression analyses testing relationships between diversification

rates and traits.

Taxonomic scope Taxonomic Best-fitting model r2 P

(mean clade ages) level
Land plants Phyla number of ecozones (0.48) + biotic fertilization 0.85 0.0014
(353.5 Ma, n=10 (0.51)
range=199.5–510.9)

Land plants Orders number of ecozones (0.30) + biotic fertilization 0.56 <0.0001
(157.6 Ma, n=140 (0.16) + non-water fertilization (0.23) + annual life
range=68.4–428.2) history (0.08) + rates of genome-size evolution
(0.07) + non-water dispersal (0.09) + percentage of
polyploids (0.06)

Angiosperms Orders number of ecozones (0.43) + annual life history 0.72 <0.0001
(109.1 Ma, n=66 (0.20) + zygomorphic flowers (0.22) + non-water
range=69.4–139.4) dispersal (0.14)

Land plants Families number of ecozones (0.55) + annual life history 0.45 <0.0001
(91.1 Ma, n=603 (0.06) + biotic fertilization (0.22) + rates of
range=22.0–428.2) genome-size evolution (0.09) + non-water dispersal
(0.07)

Angiosperms Familiesgeographical extent (0.57) + zygomorphic flowers 0.54 <0.0001

(72.9 Ma, n=363 (0.15) + biotic fertilization (0.09) + rates of
range=22.0–139.4) genome-size evolution (0.09) + epiphytic habitat
(0.08) + water dispersal (0.05)
The best-fitting multiple regression model is shown for each analysis. The full results for each analysis
(and results with alternative methods and trees) are given in app. L. For each analysis, the mean stem age
of the included clades (and range of ages) are given in parentheses with the taxonomic scope. Numbers in
parentheses adjacent to each trait indicate standardized partial regression coefficients (SPRC), showing
the relative contribution of each trait to the multiple regression model. Analyses are based on the imputed
data, the FPCM tree, and diversification rates estimated using ε=0.5. Comparable results using non-
imputed data are summarized in table R3.

This content downloaded from 128.230.234.162 on January 25, 2020 17:03:46 PM

Table 2: Relationships between diversification rates and traits within select non-angiosperm

plant groups.

Taxonomic scope Taxonomic Best-fitting model r2 P

(mean clade ages) level
Mosses Families number of ecozones 0.44 <0.0001
(Bryophyta; 72.4 Ma, n=108 (0.78) + tropical
range=24.9–327.6) distribution (0.22)

Liverworts Families number of ecozones 0.30 <0.0001

(Marchantiophyta; n=68 (0.81) + tropical
168.3 Ma, range=23.0– distribution (0.19)
428.2)

Ferns Families number of ecozones 0.40 <0.0001

(Polypodiophyta; n=42 (0.75) + LVD (0.25)
133.7 Ma,
range=48.4–315.7)

Gymnosperms Families number of ecozones 0.73 <0.001

(119.8 Ma, n=14 (0.77) + water
range=70.1–203.0) dispersal (0.23)

The best-fitting multiple regression model is shown for each analysis. Full results are given in
app. N. For each analysis, the mean stem age of the included clades (and range of ages) are given
in parentheses with the taxonomic scope. Numbers in parentheses adjacent to each trait indicate
standardized partial regression coefficients (SPRC), showing the relative contribution of each
trait to the multiple regression model. Analyses are based on the imputed data, the FPC tree, and
diversification rates estimated using an epsilon of 0.5. Gymnosperms include the phyla
Cycadophyta, Ginkophyta, Gnetophyta, and Pinophyta.

This content downloaded from 128.230.234.162 on January 25, 2020 17:03:46 PM

Figure Legends

Figure 1: Summary of the phylogeny, species richness, and net diversification rates of the major

clades (phyla) of land plants. Angiosperms (flowering plants) are Magnoliophyta. The apex of

each colored triangle indicates the crown-group age of each phylum. Colors within triangles

indicate the approximate diversification rate of each clade (based on stem-group ages and

epsilon=0.5). The tree shown here is used in the primary analyses (FPCM tree), and combines

estimates from Fiz-Palacios et al. (2011) for non-angiosperm relationships and Magallón et al.

(2015) within angiosperms. Alternative trees used are given in app. I. Source of photos: free

images from pixabay.com and public domain images from flickr.com. Photographers, from top

to bottom: Anonymous, K. Paulick, Nhelia, S. Buissine, W. Claussen, M. Gaida, M. Machová

(pixabay.com), Tab Tannery (www.flickr.com/photos/tabtannery/25648174636/, CC BY-NC-SA

2.0), banusevim, hekakoskinen.

This content downloaded from 128.230.234.162 on January 25, 2020 17:03:46 PM

All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).
Figure 1
278,180 species Magnoliophyta
0.03
(flowering plants)
Copyright The University of Chicago 2020. Preprint (not copyedited or formatted). Please use DOI when citing or quoting. DOI: https://doi.org/10.1086/708273
Net diversification
rate (species/Myr) 559 species
Pinophyta
(pines, firs, spruces,
cypresses, etc)
0
66 species Gnetophyta
(Gnetum, Welwitschia,
Ephedra)
169 species Cycadophyta
(cycads)

1 species
Ginkgophyta
(Ginkgo)
9,070 species
Polypodiophyta
(ferns, horsetails)

1,280 species
Lycopodiophyta
(clubmosses,
quillworts)
191 species Anthocerotophyta
(hornworts)

12,864 species
Bryophyta
(mosses)

4,596 species
Marchantiophyta
(liverworts)

PALEOZOIC MESOZOIC CENOZOIC

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