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Research review
From pollen dispersal to plant diversification: genetic consequences of
pollination mode
Author for correspondence:
Carolyn A. Wessinger
Email: wessinc@mailbox.sc.edu
Received: 11 September 2020
Accepted: 2 November 2020
Carolyn A. Wessinger
Department of Biological Sciences, University of South Carolina, Columbia, SC 27708, USA
New Phytologist (2021) 229: 3125–3132
doi: 10.1111/nph.17073
Key words: gene flow, pollen dispersal,
pollination mode, population structure,
speciation.
Summary
Pollinators influence patterns of plant speciation, and one intuitive hypothesis is that pollinators
affect rates of plant diversification through their effects on pollen dispersal. By specifying mating
events and pollen flow across the landscape, distinct types of pollinators may cause different
opportunities for allopatric speciation. This pollen dispersal-dependent speciation hypothesis
predicts that pollination mode has effects on the spatial context of mating events that scale up to
impact population structure and rates of species formation. Here I consider recent comparative
studies, including genetic analyses of plant mating events, population structure and comparative
phylogenetic analyses, to examine evidence for this model. These studies suggest that highly
mobile pollinators conduct greater gene flow within and among populations, compared to less
mobile pollinators. These differences influence patterns of population structure across the
landscape. However, the effects of pollination mode on speciation rates is less predictable. In
some contexts, the predicted effects of pollen dispersal are outweighed by other factors that
govern speciation rates. A multiscale approach to examine effects of pollination mode on plant
mating system, population structure and rates of diversification is key to determining the role of
pollen dispersal on plant speciation for model clades.
Introduction
Interactions with pollinators have generated stunning diversity
in flowering plants through adaptive floral evolution and
through effects on speciation (Grant, 1949; Stebbins, 1970;
Wilson, 2012). The link between pollination ecology and
pollinator-driven plant diversification can now be quantified
using a phylogenetic comparative approach, allowing
researchers to test hypotheses on plant speciation (van der
Niet & Johnson, 2012). One classic hypothesis proposes that
floral isolation is a key contributor to plant speciation (Grant,
1949), where plant populations evolve divergent floral adapta-
tions in response to local differences in pollinator communities,
leading to reproductive isolation and eventually speciation.
However, pollinators may influence plant speciation indepen-
dently of their role in floral isolation –through their automatic
effects on the genetic structure of plant populations. Pollinators
enact mating events between plants and, in doing so, conduct
gene flow across the landscape. Because pollinators vary in their
mobilities, behavior and pollen transfer mechanics, different
pollinators may cause distinct patterns of gene flow within and
among plant populations (Wright, 1946). In theory, the
population genetic structure and connectivity of plant species
should affect the rate at which subpopulations become
reproductively isolated and differentiated as incipient species
(Mayr, 1963; Harvey et al., 2019).
This ‘pollen dispersal-dependent speciation’ hypothesis has been
persistent in the plant speciation literature (e.g. Loveless &
Hamrick, 1984; Schmidt-Lebuhn et al., 2007a; Givnish, 2010;
Kramer et al., 2011; Krauss et al., 2017; Schmidt-Lebuhn et al.,
2019; Kessler et al., 2020) and predicts that alternative pollinators
have effects on mating patterns that scale up to influence rates of
species diversification (Fig. 1). Here I review studies that directly
compare the effects of alternative pollinators on mating event s, gene
flow between populations or diversification rates, in order to
investigate the validity of this hypothesis and begin to evaluate the
connections between pollen dispersal patterns and macroevolu-
tionary trends.
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Review
Predicted effects of pollination mode on pollen
dispersal distances
Pollinators vary in their spatial movements between flowers due to
differences in pollinator size and foraging behavior. Small insects
may often conduct a local search for floral resources that minimizes
the distance traveled between flowers (e.g. Levin & Kerster, 1974).
Larger bees and moths take longer foraging trips than smaller
insects (e.g. Greenleaf et al., 2007; Dick et al., 2008; Skogen et al.,
2019), with observed exceptions (e.g. Castilla et al., 2017;
O’Connell et al., 2018). The class of largest pollinators, birds and
bats, potentially travel substantial distances (kilometers) while
foraging (Linhart, 1973; Horner et al., 1998; Byrne et al., 2007;
Krauss et al., 2017). Some large bees and vertebrate pollinators
adopt a trapline foraging strategy, where an individual pollinator
establishes a regular foraging route with stops at a sequence of
spatially scattered flower patches (e.g. Lemke, 1984; Ohashi &
Thomson, 2013; Tello-Ramos et al., 2015). Traplining can be an
efficient strategy for visiting plants that have long flowering periods
but few flowers open at a time (Ohashi & Thomson, 2005). A
contrasting strategy to traplining is territoriality, where bird or bat
pollinators defend a patch of flowers (e.g. Linhart, 1973; Linhart
et al., 1987; Diniz et al., 2019). Unlike trapliners, territorial
pollinators have restricted movements within the territory between
flowers on the same or neighboring plants (Linhart, 1973).
Different pollinators also can cause distinct patterns of pollen
carryover. Pollen carryover occurs when pollen that is removed
from a flower is not completely deposited on the next visited
flower –instead it is deposited gradually onto several recipient
flowers. If pollen carryover is high, a pollinator deposits pollen
from multiple donor individuals on recipient flowers, causing
multiple paternity within a given fruit, decreased rates of selfing
and decreased rates of nearest-neighbor pollination. Floral visitors
such as bees often collect pollen as a floral reward through pollen
grooming behaviors. These behaviors tend to cause reduced
pollen carryover, relative to pollen carryover by nectar-collecting
pollinators such as hummingbirds, bats and hawkmoths (e.g.
Thomson, 1986; Castellanos et al., 2003; Muchhala & Thom-
son, 2010; Holmquist et al., 2012).
Considering differences in both foraging movements and in
patterns of pollen carryover, we can make the following predictions.
Small pollinators with limited foraging movements, especially
those that collect pollen, should generate localized mating patterns
between flowers on a given plant and between neighboring plants.
Such visitation patterns will generate selfed progeny if the
population is self-compatible. In this case, most outcrossing events
will involve a small set of neighboring plants, leading to correlated
paternity among seeds in a fruit (Schoen & Clegg, 1984).
Territorial pollinators defending one or a small number of plants,
or pollinators such as bees that systematically probe flowers on a
given plant, should also elevate rates of selfing, rates of nearest
neighbor pollination and levels of correlated paternity (Pyke, 1978;
Hadley et al., 2014). By contrast, highly mobile pollinators,
particularly vertebrate nectar-seeking pollinators, should transport
pollen more widely across the landscape and promote outcrossing
between genetically diverse individuals, causing high outcrossing
rates and higher rates of multiple paternity (Linhart et al., 1987;
Ohashi & Thomson, 2009).
Studies confirm that highly mobile pollinators
promote outcrossing over greater spatial distances
A direct approach to test the prediction that different floral visitors
influence the spatial context of mating patterns is to compare pollen
dispersal patterns of different pollinators visiting the same (or
similar) plants. Pollen dispersal can be inferred by simply observing
how pollinators move between flowers (e.g. Schmitt, 1980),
although this approach assumes that pollinator movements reflect
pollen transfer events and that there is no difference in pollen
carryover. Other studies track the movement of pollen surrogates,
often powdered fluorescent dyes, that approximate pollen movement
(e.g. Waser, 1988; Campbell, 1991). Yet not all pollen grains that are
deposited on a given stigma result insuccessful fertilization. Realized
pollen flowmust be estimated using population genetic analyses that
genotype flowering plants within a local area, along with panels of
their progeny (reviewed by Smouse & Sork, 2004). Paternal parents
can then be inferred from pollen genotypes, allowing researchers to
determine the average distance between plants, along with
Less mobile pollinator Highly mobile pollinator
Mating
patterns
Population
structure
Potential
allopatric
speciation
Fig. 1 The hypothesized effects of pollinator mobility on mating patterns, population genetic structure and potential allopatric speciation, according to the
pollen dispersal-dependent speciation hypothesis. Dots represent individual plants and dashed lines represent a sample of pollination events.
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frequencies of selfing, nearest-neighbor pollination and multiple
paternity. The most commonly used markers for genetic analyses of
pollen dispersal are microsatellites, although single nucleotide
polymorphisms (SNPs) derived from Illumina sequencing are
becoming more common (e.g. Colicchio et al., 2020).
Comparative studies suggest that pollinators do differ in how
they disperse pollen among plants. In some contexts, bird
pollination promotes outcrossing over greater spatial scales com-
pared with insect pollination. For example, genetic analyses of
Australian Eucalyptus have found that bird pollination causes
higher outcrossing rates, higher multiple paternity and lower
nearest-neighbor pollination, compared with bee pollination
(Breed et al., 2015; Bezemer et al., 2019), probably due to higher
mobility of the dominant bird pollinators in these communities
relative to bee pollinators (Byrne et al., 2007). North American
hummingbirds also are predicted to transport pollen long distances
relative to insects (Krauss et al., 2017). Pollen carryover is greater
for hummingbirds relative to bees visiting North American
Penstemon species (Castellanos et al., 2003), suggesting humming-
birds will transport pollen greater distances than bees, and reduce
levels of selfing and nearest-neighbor pollination. A study focused
on the North American species Delphinium nuttalianum also
suggests greater pollen carryover associated with hummingbird
pollination relative to bee pollination (Waser, 1988). I am unaware
of any genetic analyses of North American plants that compare
pollen dispersal distance by bees vs hummingbirds.
However, this pattern of greater pollen dispersal by birds
compared to insects may not hold for birds engaged in territorial
behavior. A recent comparative study of several Neotropical Justicia
species by Schmidt-Lebuhn et al. (2019) tracked the movement of
fluorescent dye for six hummingbird-adapted species and four bee-
adapted species and found that bees moved pollen analogs farther
than territorial hummingbirds. Yet it is possible that realized pollen
dispersal by hummingbirds is greater than predicted in this study,
because the movements of pollen analogs do not necessarily reflect
realized pollen flow. A recent study in the Neotropical understory
herb Heliconia tortuosa illustrates this disconnect between pollen
deposition and successful fertilization. The flowers of H. tortuosa
can recognize and favor pollination by traplining hummingbirds
over territorial hummingbirds, as only trapliners fully drain the
available nectar –the signal that triggers pollen tube growth (Betts
et al., 2015). This pollinator recognition mechanism results in high
realized pollen dispersal, as is expected for pollination by trapliners
(Torres-Vanegas et al., 2019). The prevalence of such recognition
systems is unknown. Additional comparative studies support the
prediction that traplining and territorial hummingbirds cause
distinct mating patterns. Linhart et al. (1987) tracked the
movement of pollen analogs for two co-occurring Acanthaceae
species and inferred that the species pollinated by territorial
hummingbirds has lower pollen dispersal distances and higher
selfing rates than the species pollinated by traplining humming-
birds. A genetic study of Palicourea rigida found that pollen
deposited by territorial hummingbirds was more genetically similar
to the recipient plant than pollen deposited by nonterritorial
hummingbirds (Maruyama et al., 2016), suggesting territorial
hummingbirds promote restricted pollen flow.
Among insect pollinators, moths seem to promote greater pollen
flow than bees. Genetic studies of Oenothera harringtonii have
found that hawkmoth pollination causes greater multiple paternity
and longer pollen dispersal distances than bee pollination (Rhodes
et al., 2017; Skogen et al., 2019). A study of moth vs bee pollination
in Silene alba also found that moths moved pollen analogs farther,
and to more recipient flowers, compared with bees (Young, 2002).
In Aquilegia coerulea, higher outcrossing rates were associated with
moth pollination relative to bee pollination (Brunet & Sweet,
2006). In these studies, greater pollen flow caused by nectar-seeking
moths is attributed to their greater mobility and higher pollen
carryover relative to pollen-collecting bees.
Other studies have compared pollen dispersal patterns caused by
diverse types and sizes of insect pollinators visiting generalist plants.
Genetic studies of Miconia affinis, a Neotropical understory tree,
found that bees of difference sizes did not differ in their mean pollen
dispersal distances (Castilla et al., 2017; O’Connell et al., 2018),
contrary to expectations (e.g. Greenleaf et al., 2007). A genetic
study conducted in the Mediterranean herb Erysimum
mediohispanicum found that small hoverflies promoted high selfing
rates, whereas long-tongued beeflies promoted genetic diversity in
offspring, suggesting differences in pollen carryover that shape
mating events (Valverde et al., 2019). A genetic study that
genotyped individual pollen grains present on diverse pollinating
insects of Castanea crenata trees in Japan found that bumblebees
promoted outcrossing and carried more genetically diverse pollen
relative to small bees and beetles (Hasegawa et al., 2015). Therefore,
small insect pollinators can vary in their pollen dispersal capabil-
ities, and regional differences in the spatial distribution of plants
could affect pollinator behavior and dispersal.
Together, these comparative studies support the prediction that
larger nectar-seeking pollinators, such as traplining birds and bats,
moths, and larger bees, move pollen greater distances than small
pollen-collecting insects, with the caveat that territorial pollinators
may restrict pollen movement. This pattern has also been detected
by two meta-analyses that find selfing rates and patterns of
correlated paternity are greater for plants with less mobile
pollinators (Breed et al., 2015; Krauss et al., 2017). I am unaware
of any study comparing the effects of wind pollination vs animal
pollination on pollen dispersal distances, probably because it would
be impossible to fully distinguish these pollination modes under
field conditions. However, many studies have estimated pollen
dispersal for wind-pollinated species using genetic markers. There
is potential for long-distance pollen dispersal by wind, despite the
expectation that much wind-dispersed pollen settles near the source
plant (Friedman & Barrett, 2009). For example, a genetic study of a
Scots pine population located in Spain found significant pollen
import from over 100 km away (Robledo-Arnuncio, 2011).
Highly mobile pollinators (and wind pollination) are
associated with reduced population genetic structure
Over time, the effects of individual mating events will accumulate,
causing a population genetic signature in which increased genetic
structure is associated with restricted pollen flow (Wright, 1946,
1949). Researchers routinely quantify population genetic structure
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using the F
ST
statistic (Cockerham & Weir, 1993) and quantify
fine-scale genetic isolation as a function of distance between
individuals using the Sp statistic (Vekemans & Hardy, 2004). F
ST
and Sp are estimated using genetic marker data, for example
microsatellites and, increasingly, Illumina-based SNP data. Studies
that compare genetic structure of co-occurring species that share life
history features (e.g. seed dispersal mechanisms) but have
contrasting pollinators are ideal for disentangling the effects of
pollen dispersal from other ecological, historical and landscape
influences (Table 1).
Comparative studies suggest that vertebrate pollination is
associated with reduced population genetic structure compared
to insect pollination. Kramer et al. (2011) studied two bee- and one
hummingbird-pollinated species of Penstemon in the North
American Great Basin region and found lower average population
genetic differentiation for the hummingbird-pollinated species
compared to the two bee-pollinated species. Of the two bee-
pollinated species, the one pollinated by large bees showed lower
population structure than the species pollinated by small bees. This
result is consistent with the hypothesis that larger bees promote
greater gene flow due to larger foraging ranges (Greenleaf et al.,
2007). Lower population differentiation associated with hum-
mingbird relative to bumblebee pollination was also reported in
irises that occur near the Mississippi River (Hamlin & Arnold,
2014). Perhaps hummingbirds in North America routinely
conduct long-distance gene flow across the landscape, leading to
greater connectivity of hummingbird-pollinated plant species. Bird
pollination appears to also promote gene flow in regions outside
North America. A comparison between bird- vs fly-pollinated
Streptocarpus species that occur in southern Africa found that the
bird-pollinated species S. dunnii has lower population genetic
structure compared to the fly-pollinated species S. primulifolius
(Hughes et al., 2007). A survey of gene flow in cactus species
suggests that bat-pollinated species tend to have lower population
genetic differentiation than insect-pollinated species, although this
was not a statistical meta-analysis (Hamrick, 2002). We currently
lack studies that compare the genetic structure of co-occurring bee
vs hummingbird plants in Neotropical communities where
resident territorial hummingbird species may restrict mating
patterns.
Wind pollination is also associated with reduced population
structure relative to insect pollination. A study of two Chamaedorea
species in Veracruz, Mexico, found that wind-pollinated
C. tepijilote shows reduced isolation by distance compared to the
insect-pollinated C. elatior, indicating reduced fine-scale genetic
structure for C. tepijilote (Luna et al., 2005). A second study
compared average population differentiation between two co-
occuring species in southern Spain, and found that the wind-
pollinated Pistacia lentiscus shows reduced population differenti-
ation compared to the insect-pollinated Myrtus communis (Nora
et al., 2015). A third study conducted above the species level
compared two species radiations of similar size and age in the high
Andes and found that wind-pollinated Polylepsis species showed
reduced genetic differentiation between species and reduced
isolation by distance, relative to the insect-pollinated
Minthostachys species (Schmidt-Lebuhn et al., 2007b).
These comparative population genetic studies suggest that
pollination mode shapes population genetic structure in plants,
with highly mobile pollinators and wind pollination causing lower
population structure relative to less mobile pollinators, as predicted
based on spatial patterns of pollen flow. A recent comprehensive
meta-analysis by Gamba & Muchhala (2020) aggregated data for
337 plant species and tested for an effect of pollination mode,
among other factors, on population genetic differentiation while
accounting for phylogeny. Their analysis found that species
pollinated by small insects have greater population structure
compared to plants pollinated by large insects, vertebrates and
wind, consistent with predictions based on differences in pollen
dispersal.
The complicated association of pollination mode with
diversification rate
The pollen dispersal-dependent speciation hypothesis assumes that
longer-term macroevolutionary processes can be extrapolated from
population genetic processes acting at on a shorter timescale
Table 1 Comparative studies reporting the effect of pollination mode on population genetic structure.
Study species Pollinator Findings Reference
Penstemon rostriflorus Hummingbirds Average R
ST
=0.1116 Kramer et al. (2011)
Penstemon pachyphyllus Large bees Average R
ST
=0.2531
Penstemon deustus Small bees Average R
ST
=0.4076
Iris fulva Hummingbirds Average F
ST
=0.0387 Hamlin & Arnold (2014)
Iris brevicaulis Bees Average F
ST
=0.4087
Streptocarpus dunnii Birds Average F
ST
=0.09 Hughes et al. (2007)
Streptocarpus primulifolius Flies Average F
ST
=0.246
Chamaedorea tepejilote Wind I
W
=0.009 Luna et al. (2005)
Chamaedorea elatior Insects I
W
=0.034
Pistacia lentiscus Wind Average F
ST
=0.013 Nora et al. (2015)
Myrtus communis Insects Average F
ST
=0.044
Polylepsis spp. Wind Slope of IBD =0.36 Schmidt-Lebuhn et al. (2007b)
Minthostachys spp. Insects Slope of IBD =0.51
IBD, isolation by distance; I
W
, weighted average of Moran’s I-statistic which is proportional to the slope of IBD; R
ST
:F
ST
calculations optimized for microsatellite
markers.
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(Harvey et al., 2019). Evolutionary biologists use phylogenetic
approaches to detect associations between diversification rates and
organismal or ecological features. Given a phylogenetic tree for a
clade of interest and character data for each tip, one can evaluate an
association between key traits and species diversification using
sister-clade comparisons and state-dependent speciation and
extinction (SSE) methods. Sister-clade analyses test for significant
differences in species richness in a sample of sister lineages that
differ in state (Mitter et al., 1988). SSE approaches use a
phylogenetic framework to jointly model transitions in character
state and state-dependent diversification, allowing the effects of the
trait on diversification to be distinguished from biased transitions
between states (Maddison et al., 2007). Evidence for an association
is strengthened by replicate evolutionary transitions between
alternative character states (Maddison & FitzJohn, 2015).
Previous phylogenetic comparative studies in a broad range of
taxa have found a positive association or no association between
diversification rate and spatial genetic structure (reviewed by
Harvey et al., 2019), which indicates that speciation rate is more
strongly influenced by spatial genetic structure in certain taxo-
nomic groups and contexts over others. This is not surprising given
the numerous and complex causes of variation in speciation rates,
which include diverse ecological and historical factors.
According to the dispersal-dependent speciation hypothesis, we
expect to find a significant association between pollination mode
and diversification rate. Specifically, we expect highly mobile
pollinators will be associated with low speciation rates because high
levels of gene flow prevent population genetic differentiation.
However, shifts in pollination mode may have additional effects on
diversification rates. For example, an association between pollina-
tion mode and plant speciation could be explained by functional
diversity of individual pollinator species that promotes plant
speciation through increased niche partitioning and specialization.
Macroevolutionary studies consistently show that transitions from
abiotic to animal pollination are associated with increased
diversification rates, a phenomenon that is generally ascribed to
pollinator specialization (reviewed by Kay & Sargent, 2009).
Another possibility is that pollination modes might differ in
extinction rates, for example if one mode causes higher levels of
sustained selfing that reduce genetic variation in populations
(Goldberg et al., 2010). Several studies have looked for a
macroevolutionary association between pollination mode and
diversification rate using sister clade or SSE approaches (Table 2).
These studies have tended to focus on the effects of pollination by
vertebrates (often birds) vs pollination by insects. An emerging
theme is that the effects of vertebrate pollination on species
diversification are complex and depend on context.
Our best example where reduced diversification rates are
associated with highly mobile pollinators is bird-pollinated plants
in North America, Australia and New Zealand. The North
American genus Penstemon has experienced repeated transitions
from bee pollination to hummingbird pollination that are
associated with reduced diversification (Wessinger et al., 2019),
consistent with reduced genetic structure for hummingbird-
relative to bee-pollinated species in this region (Kramer et al.,
2011; Hamlin & Arnold, 2014). We currently lack additional
phylogenetic comparative studies for plants in this region, although
a nonstatistical survey of hummingbird-adapted lineages in North
America found that transitions from insect to hummingbird
pollination are rarely followed by species diversification (Abra-
hamczyk & Renner, 2015). Reduced diversification for bird
pollination compared to insect pollination has also been detected in
Australian legume tribes Mirbelieae and Bossiaeae (Toon et al.,
2014), and in a broad survey of plants native to New Zealand
(Jesson, 2007). These studies are consistent with the expectation
that highly mobile pollinators prevent population genetic differ-
entiation, and provide our best evidence that patterns of pollen
dispersal may influence plant diversification rates. An alternative
explanation is that, in these regions, bee and insect pollinators show
greater functional diversity relative to bird pollinators, and the
higher diversification rates for bee- and insect-pollinated species are
driven by specialization on diverse types of bees and insects.
However, this explanation seems unlikely to explain the difference
in diversification in Penstemon, where large clades of related bee
syndrome species share similar pollinators (Crosswhite, 1967;
Wilson et al., 2004).
In contrast to these studies from North America, Australia and
New Zealand, several studies of Neotropical plants have found that
pollination by birds (and bats) is associated with increased species
diversification, relative to pollination by insects (Schmidt-Lebuhn
et al., 2007a). This has been reported in Gesneriaceae (Roalson &
Roberts, 2016; Serrano-Serrano et al., 2017), bromeliads (Givnish
et al., 2014) and Ruellia (Tripp & Tsai, 2017). Vertebrate
pollination by birds or bats may also be associated with increased
diversification relative to insect-pollinated lineages in Neotropical
bellflowers (Lagomarsino et al., 2016), with no significant
difference in diversification rates for bird vs bat pollination
(Lagomarsino et al., 2017). In Cactaceae, transitions from ancestral
bee pollination to derived pollination models, including bird, bat
and moth pollination (all expected to increase pollen flow), are
associated with increased diversification rate (Hernandez-
Hernandez et al., 2014). The contrasting effects of vertebrate
pollinators on diversification rates in Neotropical groups compa red
to other regions (North America, Australia and New Zealand) is
striking and indicates that bird and bat pollination in the
Neotropics have positive associations with diversification that are
more important than any effects on pollen dispersal. Humming-
birds are exceptionally diverse in the Neotropics relative to North
America, in terms of both species number as well as functional
diversity, a feature that may elevate species diversity of humming-
bird-pollinated plants in this region (e.g. Givnish et al., 2014). In
addition, vertebrate pollination may covary with other biotic and
abiotic factors that influence diversification rates in Neotropical
communities (Givnish et al., 2014; Lagomarsino et al., 2016;
Roalson & Roberts, 2016; Kessler et al., 2020). For example,
hummingbird pollination may allow plants to invade montane
habitats characterized by habitat complexity that may allow for
increased geographic isolation of populations, as has been proposed
for bellflowers (Lagomarsino et al., 2017).
No studies have yet examined the effects of different types of
insect pollinators (e.g. moths vs bees) on diversification rates,
although some studies have grouped sets of functional pollinator
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types together to test the effects of transitions to one of multiple
derived pollinator types on diversification rate. In southern African
Gladiolus, transitions from the ancestral pollination system (long-
tongued bees) to derived pollination modes (short-tongued bees,
moths, sunbirds, flies, butterflies or beetles) are associated with
increased diversification rates (Valente et al., 2012). However, it is
not straightforward to associate these transitions with particular
patterns of spatial genetic structure because these different types of
derived pollinators undoubtedly cause distinct patterns of pollen
dispersal. Instead, increased diversification rates associated with
derived pollination modes could reflect the positive effect of
pollinator shifts on speciation rates. The model that floral isolation
is a key contributor to speciation predicts a macroevolutionary
association between pollinator shifts and increased species diver-
sification rates, which has been found in recent studies (e.g. Valente
et al., 2012; van der Niet & Johnson, 2012; Forest et al., 2014;
Breitkopf et al., 2015; Lagomarsino et al., 2017). For example, the
evolution of sexual deception in Ophrys bees has led to many
transitions between specialized bee pollinators, probably driving
increased species diversification (Breitkopf et al., 2015).
Future directions
These empirical studies provide support for the intuitive prediction
that different modes of pollination cause distinct patterns of mating
and pollen dispersal and that these effects influence patterns of
population structure. There is less evidence that these shorter-term
effects on population-level variation affect diversification rates over
longer timescales because patterns of gene flow are just one of many
contributing processes to rates of species formation. To disentangle
the effects of population structure on speciation rates from other
contributing effects such as pollinator isolation, we need to study
focal clades at multiple scales in detail. A starting point is to focus on
clades that include multiple transitions in pollination mode,
allowing us to assess the statistical association with speciation.
When diversification rate is significantly associated with pollina-
tion mode, genetic studies of mating patterns and population
structure conducted in multiple species that represent phylogenetic
replicates of each pollination mode will help establish how patterns
of pollen dispersal may contribute to population isolation. At the
same time, we should determine the degree of pollinator isolation
between related species in these focal clades, which will allow us to
quantify the contribution of pollinator isolation and potential floral
specialization on patterns of speciation. Using these complemen-
tary approaches, we will begin to understand the relative impor-
tance of pollen dispersal in addition to floral specialization on
diversification rates.
Acknowledgements
I thank Jerry Hilbish, Ashley Hamilton and three anonymous
reviewers for helpful comments on the manuscript. In addition, I
appreciate support from the University of South Carolina.
ORCID
Carolyn A. Wessinger https://orcid.org/0000-0003-3687-
2559
Table 2 Studies that examine the effect of pollination mode on species diversification using sister-clade comparisons or state-dependent speciation and
extinction (SSE) models.
Study system
Geographic
region Method
Alternative pollination modes: inferred net
diversification rates Reference
Penstemon crown clade North America SSE models Hummingbird: r=0.01
Bee: r=2.61
Wessinger et al. (2019)
Mirbelieae and Bossiaeeae
(Fabaceae)
Australia Sister-clade
comparison
Bird: reduced species richness
Bee: greater species richness
Toon et al. (2014)
Angiosperms (42 lineages) New Zealand Sister-clade
comparison
Bird: reduced species richness
Insect: greater species richness
Jesson (2007)
Gesnerioideae (Gesneriaceae) Neotropics SSE models Bird: r=0.4326
Insect: r=0.1487
Roalson & Roberts (2016)
Gesnerioideae (Gesneriaceae) Neotropics SSE models Hummingbird: r=0.225
Insect: r=0.087
Serrano-Serrano et al. (2017)
Bromeliaceae Neotropics SSE models Hummingbird: r=0.87
Insect: r=0.293
Givnish et al. (2014)
Ruellia Neotropics SSE models Hummingbird: r=0.444
Nonbird (mostly bee): r=0.222
Tripp & Tsai (2017)
Lobelioideae (Campanulaceae) Neotropics SSE models Vertebrate: r=0.973
Invertebrate: r=0.028
Lagomarsino et al. (2016)
Centropogonid clade
(Campanulaceae)
Neotropics SSE models Hummingbird: r=0.92
Bat: r=0.92
Lagomarsino et al. (2017)
Cactaceae Neotropics SSE models Bird, bat or moth: r=0.333
Bee: 0.155
Hern
andez-Hern
andez et al.
(2014)
Gladiolus Southern
Africa
SSE models Long-tongued bees: r=0.102
Other pollinators: r=0.576
Valente et al. (2012)
r, net diversification rate (speciation –extinction).
New Phytologist (2021) 229: 3125–3132 Ó2020 The Authors
New Phytologist Ó2020 New Phytologist Foundation
www.newphytologist.com
Review Research review
New
Phytologist
3130
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