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\begin{document}

\title{Geographic mosaics of interactions via heterospecific pollen transfer
may contribute to shape local and global patterns of plant diversity}



\author[1]{Gerardo Arceo-Gomez}%
\affil[1]{East Tennessee State University}%


\vspace{-1em}



  
  \date{May 07, 2024}


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\selectlanguage{english}
\begin{abstract}
Studies that aim to understand the processes that generate and organize
plant diversity in nature have a long history in Ecology. Among these,
pollinator-mediated plant-plant interactions that occur by altering
pollinator floral preferences have been at the forefront in this field.
Current evidence however indicates that plants can interact directly via
heterospecific pollen (HP) transfer, that these interactions are
ubiquitous, and can have strong fitness effects with implications for
floral evolution, speciation and community assembly. Hence, interest in
understanding their role in the diversification and organization of
plant communities is rapidly rising. The existence of geographic mosaics
of species interactions and their role in shaping patterns of diversity
is also well recognized. However, after 40 years of research, the
importance of geographic mosaics in HP intensity and effects remain
poorly known, thus ignoring its potential in shaping patterns of
diversity at local and global scales. Here, I develop a conceptual
framework and summarize existing evidence for the ecological and
evolutionary consequences of geographic mosaics in HP transfer
interactions and outline future directions in this field.%
\end{abstract}%



\sloppy


\textbf{Introduction}

Generalization in plant-pollinator interactions, where pollinators visit
more than one plant species and plants are visited by more than one
pollinator, is widespread in nature (e.g. Herrera 1988, Waser et al.
1996, Olesen \& Jordano 2002, Bascompte et al. 2003, Kaiser-Bunbury et
al. 2017). Hence, the study of plant-plant interactions via their
effects on pollinator choice (i.e. pre-pollination) and patterns of
pollinator visitation (e.g. pollinator competition) has been a prolific
are of study in ecology and evolutionary biology. Their study has
rendered important insights on the mechanisms of floral diversification
(Mitchell et al. 2009, Phillips et al. 2020) and the processes that
mediate community assembly (Sargent \& Ackerly 2008). It is thus also
not surprising that the study of pre-pollination interactions has
remained at the forefront in the fields of pollination biology and
community ecology for over 100 years (Robertson 1985, Phillips et al.
2020). However, the ultimate outcome of pre-pollination interactions
(via changes in pollinator visitation patterns) can be determined by
plant-plant interactions that take place via pollen on the stigma (i.e.
post-pollination) long after pollinators leave a flower (Morales \&
Traveset 2008, Ashman et al. 2020), nonetheless these have been far less
studied. It is thus imperative that we integrate the complexity of
heterospecific pollen (HP) transfer into our understanding of
pollinator-mediated interactions in order to fully uncover their
ecological and evolutionary consequences in nature. This is particularly
important as the ubiquity of HP transfer interactions is becoming
increasingly more evident (e.g. Morales \& Traveset 2008, Fang \& Huang
2013, Tur et al. 2016, Arceo-G\selectlanguage{ngerman}ómez et al. 2019a). Recent studies for
instance, have shown that HP transfer is widespread across taxonomic
(217 species; 88\% of all species evaluated), geographic (five
continents) and phylogenetic scales (52 plant families; Arceo-Gómez et
al. 2019a), with some species averaging up to 368.5 HP grains per stigma
(average of 11.83 ± 2.15 across species) and receiving HP in 50-100\% of
their flowers (Ashman \& Arceo-Gómez 2013). Detrimental male (e.g.
Muchhala et al. 2010, Muchhala and Thomson 2012) and female fitness
effects of HP receipt have also been widely demonstrated (Morales \&
Traveset 2008, Ashman \& Arceo-Gómez 2013), even if HP receipt occurs in
small amounts (1\% HP; Thomson et al. 1982a). For instance, a
meta-analysis of 20 HP donor-recipient pairs revealed a 20\% average
decrease in seed production as a result of HP deposition (Ashman \&
Arceo-Gómez 2013). Given the pervasive nature of these interactions and
its strong fitness effects, interest in understanding its role in the
diversification (e.g. Hopkins \& Rausher 2012, Armbruster et al. 2014,
Ashman \& Arceo-Gómez 2013, Moreira-Hernandez \& Muchhala 2019) and
organization of plant communities is rapidly rising (e.g. Eaton et al.
2012, Tur et al. 2016, Arceo-Gómez et al. 2019a).

The existence of complex geographic mosaics of species interactions and
their role in shaping broad patterns of diversity has also been
well-recognized (Thompson 1999, Gomulkiewicz et al. 2000, Thompson \&
Cunningham 2002). The most central tenet of these studies is that the
intensity and outcomes of interactions between a pair, or group of
species, can differ greatly across the geographic landscape, such that
different traits are favored in different communities (Thompson 1999,
Singer \& McBride 2012). Geographic mosaics of species interactions have
been observed in plant-pollinator (e.g. Thompson \& Cunningham 2002),
plant-herbivore (e.g. Singer \& McBride 2012), plant-microbiome (e.g.
Andonian et al. 2012), predator-prey (e.g. Toju \& Sota 2006) and
host-parasite interactions (e.g. Gandon \& Nuismer 2009) among others.
Surprisingly however, after 40 years of research (Morales and Traveset
2008, Ashman and Arceo-Gómez 2013), the extent as well as the ecological
and evolutionary consequences of geographic mosaics of plant-plant
interactions via HP transfer (intensity and effects) remains poorly
understood. The ecological, environmental and genetic landscape on which
HP transfer interactions occur changes constantly (see below). Thus, the
intensity and outcomes of these interactions are likely to fluctuate and
elicit different evolutionary responses in different populations (e.g.
Hopkins \& Rausher 2012, Arceo-Gómez \& Ashman 2014a, Arceo-Gómez et al.
2016a), potentially contributing to local and global patterns of plant
diversification and assembly.

Changes in the intensity of HP donation and receipt can result from
spatial variation in conspecific flower density (Thomson et al. 2019)
and changes in plant and pollinator community assemblages across the
landscape (Arceo-Gómez \& Ashman 2014a, Johnson \& Ashman 2019).
Variation in HP effects on the other hand, can fluctuate as a result of
variation in resource availability (Celaya et al. 2005), pollen
donor-recipient species co-existence history (Arceo-Gómez et al. 2016a)
or genetic architecture (i.e. selfer vs outcrosser; Arceo-Gómez \&
Ashman 2014b). In spite of this, the intensity of HP receipt in any
given species has been typically evaluated at a single location (but see
Emer et al. 2015, Tur et al. 2016), and its fitness effects tested under
constant greenhouse conditions (reviewed in Morales \& Traveset 2008,
Ashman \& Arceo-Gómez 2013; but see Briggs et al. 2015). Thus, to this
day, the degree to which the intensity and effects of HP receipt varies
across broad spatial scales is virtually unknown for any species (but
see Waites \& Agren 2004). Hence, we have so far ignored the potential
for geographic variation in HP transfer interactions in contributing to
shape plant communities in nature.

Community-level changes in the intensity of HP transfer may also lead to
differences in its importance as a driver of diversification and as a
mediator of co-flowering community assembly at larger spatial scales.
For instance, different HP transfer interaction landscapes, where the
incidence and intensity of HP transfer varies across communities (e.g.
Johnson \& Ashman 2019, Tur et al. 2016) or geographic regions
(Arceo-Gómez et al. 2019a), may result in evolutionary hotspots (high HP
transfer; as in Thompson 1999). Heterospecific pollen receipt has been
shown to influence the evolution of floral traits (e.g. Armbruster et
al. 1994, Muchhala \& Thomson 2012), mating systems (Fishman \& Wyatt
1999, Randle et al. 2018), flowering time (Waser 1978) and even play a
role in reinforcing speciation (e.g. Hopkins \& Rausher 2012). Thus,
HP-mediated evolutionary hotspots may have the potential to foster
global patterns of plant diversification (Arceo-Gómez et al. 2019a,
Moreira-Hernandez \& Muchhala 2019). The existence of geographic mosaics
of species interactions has been proposed as an important contributor to
the diversification and organization of life (Thompson 1999), and
interactions via HP transfer may not be the exception. Here, I outline a
conceptual framework and summarize existing evidence for the causes and
potential ecological and evolutionary consequences of geographic
variation in HP transfer interactions and propose future directions in
this field.

\textbf{Geographic mosaics of HP transfer interactions}

Drivers of spatial variation in patterns of HP receipt

While there is a growing body of literature describing among-species
differences in the intensity and diversity of HP receipt (reviewed in
Morales \& Traveset 2008, Ashman \& Arceo-Gómez 2013, Arceo-Gómez et al.
2019a), little has been done to understand the extent and potential
drivers of within-species variation in HP receipt across spatial scales.
Here I briefly outline and provide evidence for four non-mutually
exclusive and likely interlinked sources of within-species variation in
HP receipt (Fig. 1). The first two (Fig. 1a-b) are related to the
abundance and spatial distribution of the HP recipient, whereas the
remaining two (Fig. 1c-d) are related to changes in the surrounding
plant and pollinator community.

\emph{I and II. Density and fine-scale spatial arrangement of
conspecific flowers} - I) It is well known that variation in conspecific
flower density can influence pollinator attraction, flower visitation
rate, conspecific pollen deposition and overall reproductive success
(e.g. Rathcke 1983, Kunin 1997, Hegland \& Boeke 2006, Spigler \& Chang
2008). What has been less explored, however, is how variation in
conspecific flower density influences pollen transfer dynamics with
co-flowering species, i.e. HP donation and receipt (Waal et al. 2015,
Thomson et al. 2019; Fig. 1a). For instance, as conspecifics decrease in
density across the landscape HP receipt can be expected to increase as a
result of increasing pollinator visits to heterospecific flowers
(Thomson et al. 2019, Ashman et al. 2020). Waal et al. (2015) found
support for this prediction in an experimental study with South African
daisies. They found an increase in HP receipt with decreasing
conspecific density leading to reduced fecundity in populations of low
relative abundance (Waal et al. 2015). However, it has also been
proposed, that HP receipt may increase with increasing conspecific
flower density as plants become larger and/or more frequent targets for
HP delivery, particularly from wind-pollinated HP donors (Parra-Tabla et
al. 2020). The direction of the relationship between conspecific density
and HP receipt may thus depend on the pollination system (wind vs
animal-pollinated) of the main HP donor. These predictions however,
require further testing.

II) It has also been shown that density-dependent effects on HP receipt
can be influenced by plant species' spatial distribution within a site,
particularly when pollinators respond to fine-scale (within meters)
spatial patterns of flowering species distribution (e.g. intermixed vs
isolated; Fig. 1b Thomson et al. 1982, Hanoteaux et al. 2013, Thomson et
al. 2019). For instance, experimental studies have shown that
within-species patterns of HP transfer dynamics can vary significantly
between isolated, patchy and intermixed arrays of plants within a site
(Bruckman \& Campbell 2016, Thomson et al. 2019), with HP receipt
typically increasing in intermixed arrays. Waal et al. (2015) even show
evidence suggesting that the spatial aggregation of plants can buffer
against the increasing incidence of HP receipt that occurs with
decreasing conspecific density. It has further been shown that
within-species variation in the diversity and intensity of HP receipt
can be more than two times higher than among-species variation within a
single community (Arceo-Gómez et al. 2016b), thus supporting the idea
that fine-scale spatial drivers of HP receipt are at play. Overall, the
evidence so far suggests that within-species patterns of HP receipt can
vary extensively within and across communities, generating complex
geographic mosaics of HP transfer and receipt. Population-level
differences in pollen transfer dynamics may in turn lead to a mosaic of
adaptive landscapes (discussed below) if population differences in HP
receipt persist over time (e.g. Arceo-Gómez et al. 2016a, Fang et al.
2019). However, to my knowledge, very few studies have evaluated the
extent and drivers of spatial variation in HP receipt within a species,
which has limited our understanding of its potential evolutionary
consequences.

\emph{III and IV. Co-flowering and pollinator community composition} -
III) The intensity and diversity of HP receipt in individual species may
also vary with varying pollinator species composition across the
landscape (identity, abundance and diversity; Herrera 1988, 1995), as
pollinators vary in the size and diversity of HP loads they transfer
(Fig. 1c; e.g. King et al. 2013, Arceo-Gómez et al. 2016b, Minnaar et
al. 2019b). For instance, Johnson and Ashman (2019) showed that 70\% of
variation in the composition of HP loads transferred among plants across
13 communities in Hawaii was the result of differences in pollen loads
transported by~\emph{Apis~mellifera} . As a result, most of the
site\selectlanguage{english}-to\selectlanguage{english}-site variation in HP receipt within a species was attributed to
differences in the abundance of this introduced pollinator species
(Johnson \& Ashman 2019). In another study Kay et al. (2019) showed that
hawkmoths vary extensively in the amount of HP transferred
among\emph{Clarkia} species, suggesting that the presence/absence of
this pollinator can have large effects on overall HP transfer dynamics.
Changes not only in the identity, but in the overall diversity of the
flower visiting insect community, have also been predicted to lead to
extensive changes in patterns of HP receipt (e.g. Arceo-Gomez et al.
2016b, Ashman et al. 2020). With HP load size predicted to increase with
increasing pollinator diversity (Arceo-Gomez et al. 2016b).

IV) Fluctuations in plant species composition have also been shown to
have large impacts on patterns of HP receipt (Fig. 1d). These changes in
HP receipt can be mediated by variation in plant species identity,
diversity and even in the functional trait composition in a community
(e.g. floral trait similarity; Eaton et al. 2012). For instance, the
abundance of a single plant species in co-flowering communities in
Hawaii significantly altered patterns of HP receipt, with plants
receiving smaller HP loads and being less connected via HP transfer in
sites where it was dominant (Johnson \& Ashman 2019). In another study,
Arceo-Gomez and Ashman (2014a) showed that \emph{Mimulus guttatus}plants
receive up to four times more HP depending on the overall diversity of
the plant community where they occur. Changes in plant community
composition may not only alter overall HP load size and diversity but
also the identity of the interacting partners. For instance, a recent
study showed that the presence of one (invasive) species (\emph{Cirsium
arvense} ) causes a rearrangement of HP transfer interactions in the
community, such that some HP transfer interactions disappear while new
ones emerge (Daniels \& Arceo-Gomez 2020). This reorganization of HP
transfer interactions may also have the potential to alter species'
evolutionary trajectories within a community (Ashman \& Arceo-Gomez
2013). What is evident from these studies, is that the intensity,
diversity and identity of HP loads on individual recipient species can
vary extensively across the landscape as a result of changes in plant
and pollinator community composition, including the addition of invasive
and non-native plants and pollinators to native communities.~Moreover,
even in cases where plant and pollinator community composition remain
relatively constant, the identity of pairwise plant-plant interactions
via HP transfer could still vary across communities, as it has been
shown in plant-pollinator interaction networks (Carstensen et al. 2014).
It is evident that individual plant species can experience large
variation in the surrounding plant (e.g. Arceo-Gomez \& Ashman, 2014a,
Albor et al. 2019) and pollinator community (Herrera 1988, Cosacov et
al. 2008), and evidence suggesting this plays a key role in mediating
within-species variation in HP transfer dynamics is rapidly accumulating
(e.g. Arceo-Gomez \& Ashman 2014a, Ashman \& Johnson 2019, Kay et al.
2019). In spite of this, and although studies have evaluated spatial
changes in overall pollen transfer network structure (e.g. Emer et al.
2015, Tur et al 2016), to my knowledge no study has documented the
extent to which changes in community species composition mediate
within-species variation in HP receipt across a wide geographical scale.

Drivers of spatial variation in HP effects

While many studies have documented the existence of fitness effects of
HP receipt (reviewed in Morales \& Traveset 2008, Ashman \& Arceo-Gomez
2013, Moreira-Hernandez \& Muchhala 2019), little work has been done
evaluating the extent and potential drivers of within-species variation
in these effects. Here I outline and provide existing evidence to
support three potential sources of variation (Fig. 2).

\emph{I. Environmental and resource variability} - It is known that
variation in resource conditions (e.g. water and nutrients) can have
strong effects on fertilization success (e.g. Herrera 1995, Lush et al.
1998, Feng et al. 2000). Specifically, the availability of water (Lush
et al. 1998), light (e.g. Feng et al. 2000, Campbell et al. 2001) and
temperature (Lankinen 2001) have been shown to affect conspecific pollen
germination and pollen tube growth. For instance, conspecific pollen
germination rate decreased with decreasing water and light availability
in \emph{Nicotiana alata} (Lush et al. 1998). It has also been shown
that changes in soil composition can alter style chemistry, which in
turns affects conspecific pollen performance (Searcy \& Macnair 1990).
If variability in abiotic resources and environmental conditions affects
conspecific pollen performance on the stigma/style, then we can expect
that this variability would also affect its ability to compete and
succeed in the face of HP interference (Fig. 2a). If this is the case,
then it is likely effects of HP receipt may vary across a species'
distribution range. In spite of this possibility, the great majority of
studies have evaluated HP effects under constant greenhouse conditions
(reviewed in Morales \& Traveset 2008, Ashman and Arceo-Gomez 2013), and
results from these studies have been used to make wide-ranging
inferences of overall species' HP tolerance or susceptibility. Plants
however, often experience a wide range of environmental conditions in
nature (e.g. Chapin et al. 1987, Davis et al. 2000, Torang et al. 2010),
and thus HP effects derived from greenhouse studies may lead to an
incomplete understanding of such effects (Celaya et al. 2015). To my
knowledge, only one study has evaluated the role of resource
availability in mediating HP effects on reproductive success (Celaya et
al. 2015; but see Ruane \& Donohue 2007 for environmental effects on
hybridization). In this study, Celaya et al. (2015) showed that HP
effects are stronger (reduced pollen tube growth) under stressful
abiotic conditions, that is, when the availability of water, light or
both is low. Interestingly, they did not observe any effects of HP
receipt when both, water and light availability, where high (Celaya et
al. 2015). These conditions of `unlimited' resources however, represent
the conditions under which most greenhouse studies on HP effects have
been conducted, suggesting that HP effects could be underestimated for
some species or populations. Such limitations could ultimately obscure
our understanding of the real effects and consequences of HP transfer in
nature. Here I argue that the outcome of HP transfer interactions are
likely to be context-dependent, and strongly depend on the particular
abiotic conditions where these interactions take place. Interpopulation
variation in HP effects may in turn lead to geographic mosaics of
selection, as the strength of HP receipt as a selective pressure would
vary (via female fitness) across the landscape (discussed below).
However, to my knowledge, this prediction has not been explored.

\emph{II. Pollen donor-recipient co-existence history} - Another
potential driver of within-species variation in HP effects is variation
in a population's history of exposure to HP receipt (Fig. 2b). As
mentioned above, within-species variation in the intensity of HP receipt
can be large and driven by various sources (Fig. 1) across a specie's
distribution range. With this in mind, we could predict that plant
populations that have been continually exposed to high levels of HP
receipt (i.e. large history of exposure) will be more likely to evolve
tolerance strategies to minimize its negative effects on reproductive
success (Ashman \& Arceo-Gomez 2013, Arceo-Gomez et al. 2016a). As a
result, these populations would show little to no reproductive effects
when exposed to HP compared to populations that typically receive
minimal or infrequent amounts of HP (e.g. Arceo-Gomez et al. 2016a).
However, whether plant populations can evolve tolerance mechanisms to HP
receipt is not fully known. Nevertheless, if this level of local
adaption to HP effects occurs (e.g. Kay \& Schemske 2008, Arceo-Gomez et
al. 2016a), then variation in the history/intensity of exposure to HP
transfer could underlie population divergence in HP tolerance. For
instance, in one of the few studies to date, Arceo-Gomez et al. (2016a)
showed evidence indicating that \emph{Clarkia xantiana} populations vary
in their level of HP tolerance according to their history of exposure to
HP. Specifically, \emph{Clarkia} pollen from populations with no history
of HP exposure had lower reproductive success when subjected to HP
hand-pollination treatments compared with populations that had been
naturally exposed to HP for more than 30 years (Arceo-Gomez et al 2016a;
also see Kay \& Schemske 2008). This study also suggested that local
adaption to different HP exposure regimes may not only occur in response
to selective pressures on female (stigma/style) fitness, but that
selective pressures could act on male (pollen) fitness as well
(Arceo-Gomez et al. 2016a). For instance, conspecific pollen grains may
be locally adapted to succeed in highly competitive stigmatic
environments (large and diverse HP loads) resulting in enhanced pollen
performance (i.e. higher pollen germination and pollen tube growth;
Ashman \& Arceo-Gomez 2013, Moreira-Hernandez \& Muchhala 2019).
Analogous perhaps, to the effects of conspecific pollen competition on
the evolution of pollen tube growth rates (Mazer et al. 2010). Such
local adaptation of male gametophytes (pollen) could lead to lower HP
effects in plants typically exposed to high levels of HP transfer.
However, if varying degrees of history/intensity of exposure lead to
geographic mosaics of selection on stigmatic HP tolerance or conspecific
pollen performance is yet to be determined.

\emph{III. Recipient mating system} - Plant populations can vary
substantially in their degree of selfing versus outcrossing, which has
implications for their genetic diversity and architecture across their
distribution range (e.g. Barrett \& Husband 1990, Tamaki et al. 2009,
Ness et al. 2010, Hargreaves \& Eckert 2014). For instance, a recent
study showed large interpopulation mating system variation in 105
species across 44 families (Whitehead et al. 2018). Furthermore,
numerous studies have demonstrated that self-pollen is typically less
competitive, as germination and pollen tube growth is slower compared to
outcross pollen (e.g., Weller \& Ornduff 1977, Aizen \& Searcy 1990,
Cruzan \& Barrett 1993, Kruszewski \& Galloway 2006). Since both of
these components of the pollination process (pollen germination and tube
growth) are commonly affected by the presence of HP (Morales \& Traveset
2008, Ashman \& Arceo-Gomez 2013), self-pollen may be more susceptible
to HP effects compared with outcross pollen (Arceo-Gomez \& Ashman
2014b). If this is the case, then population susceptibility to HP
effects may covary with a population's mating system (Fig. 2c). To my
knowledge, this prediction has not been explored for any species. For
instance, a hand pollination experiment in \emph{Mimulus guttatus} , a
species with high interpopulation mating system variation (Ivey \& Carr
2005), showed that HP has stronger effects when competing against self-
compared to outcross conspecific pollen (Arceo-Gomez \& Ashman 2014b).
Specifically, HP reduced self-pollen tube growth by an additional 32\%
compared with outcross pollen (Arceo-Gomez \& Ashman 2014b).
Among-population variation in the degree of selfing can also take place
as a result of breakdown in self-incompatibility systems (e.g. Reinartz
\& Les 1994, Nasrallah et al. 2004, Busch \& Schoen 2008, Encinas-Viso
et al. 2020). It has been proposed that HP effects may depend on
self-incompatibility mechanisms in the HP recipient, since
self-incompatible plants could co-opt mechanisms involved in rejection
of self-pollen to reject HP (e.g. Hiscock \& Dickinson 1993, Murfett et
al. 1996, Bedinger et al. 2011). In this case, styles of
self-incompatible populations would be predicted to be more tolerant to
the negative effects of HP receipt compared with populations where
self-incompatibility mechanisms have broken down or are less effective
(Ashman \& Arceo-Gomez 2013). Thus, variation not only in the mating
system (ratio of self/outcross pollen), but in the strength of
self-incompatibility mechanisms, could mediate variation in the outcome
of HP interactions in nature. Furthermore, in mixed-mating populations
(plants that receive self and outcross pollen), HP receipt may have the
potential to influence realized mating system by favoring outcross
pollen grains (i.e. HP has greater effects on self-pollen; Arceo-Gomez
and Ashman 2014b), or if increased selfing provides reproductive
assurance in the face of high HP receipt (Ashman et al. 2020). Both of
these mechanisms could ultimately influence mating system evolution and
genetic diversity in plant populations. Thus, HP receipt could have
far-reaching consequences that go beyond what has been proposed, but
these intriguing ideas remain untested.

\textbf{Geographic mosaics of selection.}

Despite the seemingly large spatial variation in the intensity and
effects of HP receipt the potential role of HP transfer interactions as
a force generating geographic mosaics of selection is mostly unknown
(but see Kay \& Schemske 2008, Hopkins \& Rausher 2012, Arceo-Gomez et
al. 2016a). HP receipt can act as a selective force driving the
evolution of floral strategies that mitigate female (Morales \& Traveset
2008) and male fitness costs (conspecific pollen loss; Moreira-Hernandez
\& Muchhala 2019). Examples include adaptations to enhance pollen
placement (e.g. Armbruster et al. 1994. Minnaar et al. 2019a), shifts in
flowering phenology (e.g. Waser 1978) and adaptations to minimize
pollinator sharing such as flower trait divergence (e.g. Hopkins \&
Rausher, 2012), pollinator specialization (Muchhala et al. 2010) and
increased selfing (e.g. Fishman \& Wyatt, 1999). Specifically, Ashman
and Arceo-Gomez (2013) proposed two main evolutionary strategies to
mitigate female fitness effects, i.e. tolerance or avoidance of HP
receipt. Although these strategies were proposed as a means to explain
among-species variation in HP receipt (Ashman \& Arceo-Gomez 2013),
plants within the same species that are exposed to different HP transfer
environments may experience the same evolutionary pressures and
outcomes. For instance, Hopkins and Rausher (2012) showed evidence for
divergent selection pressures on flower color in \emph{Phlox
drummondii}populations as a result of HP transfer from \emph{Phlox
cuspidata.}Selective pressure on genes that affected floral pigmentation
occurred only in sympatric \emph{Phlox} populations to prevent
hybridization (i.e. HP avoidance; Hopkins \& Rausher 2012), or maybe
even direct HP effects on reproductive success (e.g. stigma clogging),
thus generating spatial mosaics of selection. In a similar study, Kay
and Schemske (2008) found pollen-pistil incompatibilities had evolved
only in sympatric populations of two \emph{Costus} species, and not in
isolated populations, thus providing evidence for geographic mosaics of
selection on HP tolerance strategies (also see Arceo-Gomez et al.
2016a). Furthermore, \emph{Mimulus guttatus} growing in serpentine seeps
in California showed an increase in flower longevity as an adaptive
response to minimize effects of high levels of HP receipt with
increasing co-flowering diversity (Arceo-Gomez \& Ashman 2014a). In this
case, population-level differences in HP receipt likely led to changes
in the adaptive value of flower longevity hence influencing spatial
patterns of floral evolution (Arceo-Gomez \& Ashman 2014a). Evolutionary
adaptations that minimize male fitness costs have also been shown and
these include traits that enhance accuracy in pollen placement (e.g.
Muchhala \& Potts 2007, Armbruster et al. 2014), increase in pollinator
specialization (e.g. Muchhala et al. 2010) and floral constancy
(Moreira-Hernandez \& Muchhala 2019). Nonetheless, evidence of
within-species variation in these male-driven evolutionary responses
across a species' distribution range is still limited. In addition to HP
tolerance and avoidance strategies, selection can favor mechanisms that
increase the degree of autonomous self-pollination in order to
preemptively minimize HP effects (e.g. Fishman \& Wyatt 1999, Randle et
al. 2018). For instance, Fishman and Wyatt (1999) demonstrated that
selection favored selfing and selfing-related traits only
in\emph{Arenaria uniflora~} populations that grew in sympatry with
congeneric \emph{A. glabra.} They further\emph{~} show that HP transfer
rather than pollinator competition was the main driver of selection
(Fishman \& Wyatt 1999). Thus, HP transfer not only has the potential
for generating geographic mosaics of selection in floral traits, but
also on patterns of mating system evolution.

Changes in HP transfer dynamics as a result of changes in community
species composition (e.g. Arceo-Gomez \& Ashman 2014a, Johnson \& Ashman
2019) can further contribute to generate selection mosaics via diffuse
selection (e.g. Iwao \& Rausher 1997; Stinchcombe \& Rausher 2001). For
instance, Iwao and Rausher (1997) proposed that diffuse co-evolution
would occur if, 1) susceptibility to different selective pressures (e.g.
HP donors) are genetically uncorrelated, 2) the presence/absence of one
species (e.g. HP donor) does not mediate the incidence of effects caused
by another, and 3) the fitness effects of one species (e.g. HP donor) do
not depend on the presence/absence of another. So far, we know that at
least one of these conditions is likely violated in the context of HP
receipt. Specifically, Arceo-Gomez and Ashman (2011) showed that the
fitness effects of HP receipt can strongly depend on the number and
identity of HP donor species present on the stigma (violating condition
three). Furthermore, it is possible that HP recipient susceptibilities
to different HP donor species will be correlated if they all depend on
the efficiency of recipient's self-incompatibility system, that is,
self-compatible plants may be similarly susceptible to a wide array of
HP donors (violating condition one; Hiscock \& Dickinson 1993, Murfett
et al. 1996). It has also been shown that the presence of one species
can cause a rearrangement of HP interactions in the community, mediating
the incidence of HP effects from other species, and thus violating
condition two sated above (Johnson \& Ashman 2019, Daniels \&
Arceo-Gomez 2020). In other words, the effects and responses to
selection via one HP donor are likely non-independent of the
presence/absence of other HP donors in the community, thus setting the
stage for diffuse selection (e.g. Stinchcombe \& Rausher 2001). While
the role of multispecies interactions in mediating diffuse evolutionary
processes is a topic of ongoing study (Johnson \& Stinchcombe 2007), the
potential importance of diffuse selection via HP transfer interactions
has been entirely overlooked. Nevertheless, the above evidence suggests
that the potential for within-species variation in HP receipt to act as
a driver of microevolutionary processes is strong. Yet, its contribution
to generating geographic mosaics of selection remains largely
unexplored.

\textbf{Community-level variation in patterns of HP receipt}

The average intensity and diversity of HP that plants receive not only
vary among populations of the same species but can vary among entire
plant communities. Recent studies on HP transfer networks have shown
that community-wide patterns of HP transfer can vary spatially (e.g. Tur
et al. 2016, Johnson \& Ashman 2019). For instance, a study across nine
sand dune plant communities in the Yucatan showed large variation in
average HP proportion (2.3\% - 20.8\%) and HP richness (2.3 - 5.5 HP
donor species) that plants receive across communities (Parra-Tabla et
al. 2020). A recent global study also showed that patterns of HP receipt
(likelihood and intensity) correlate with latitudinal and altitudinal
biodiversity gradients, suggesting that plants growing in highly diverse
regions of the world are more likely to engage in HP transfer
interactions (Arceo-Gomez et al. 2019a). Although it is evident that
patterns of HP receipt vary across large spatial scales most studies to
date have been limited to evaluate patterns of HP receipt within single
communities (e.g. McLernon et al. 1996, Montgomery \& Rathcke 2012, Fang
\& Huang 2013, Arceo-Gomez et al. 2016b). Wide differences in pollinator
species composition across regions around the globe may further
contribute to global trends in HP receipt (Arceo-Gomez et al. 2019a).
For example, large vertebrate pollinators common in tropical regions
(e.g. bats and hummingbirds; Bawa 1990) can carry larger and more
diverse HP loads (e.g. Borgella et al. 2001, Muchhala \& Jarrin 2002,
Muchhala \& Thomson 2012) compared with invertebrate pollinators (e.g.
beetles, bees, flies, butterflies) that are common in temperate areas
(e.g. Barrett \& Helenum 1987). These global differences in HP carriage
and receipt may thus contribute to observed global patterns of floral
diversification by imposing a wide-range of selective pressures via male
(Moreira-Hernandez \& Muchhala 2019) and female fitness (Morales \&
Traveset 2008, Ashman \& Arceo-Gomez 2013). For instance, it has long
been proposed that enhancing pollinator floral constancy is a strong
force driving divergent evolution, but how much of this is due to HP
avoidance versus competition for pollinator visitation is less known
(e.g. Waelti et al. 2008; also see Moreira-Hernandez \& Muchhala 2019).
In fact, the pollination literature has largely overlooked the potential
contribution of post-pollination process (via HP transfer) to outcomes
of pollinator-mediated selection. HP receipt has been shown to influence
the evolution of morphological traits (e.g. flower color and size;
Armbruster et al. 1994, Muchhala \& Thomson 2012, Hopkins \& Rausher
2012), physiological processes (e.g. Kay \& Schemske 2008), mating
systems (e.g. Fishman \& Wyatt 1999, Randle et al. 2018) and flowering
phenology (Waser 1978). Thus, differences in HP receipt mediated by
variation in plant and pollinator community composition among geographic
regions across the globe may have the potential to generate evolutionary
hostspots (Thompson 1999) and contribute to shape global patterns of
plant biodiversity.

\textbf{Future directions}

Despite the fact that the study of HP receipt has a history of at least
40 years (Kanchan \& Jayachandra 1980), we are just starting to unravel
the complexity of its delivery (e.g. Fang \& Huang 2013, Tur et al.
2016) and its effects (e.g. Muchhala et al. 2010, Arceo-Gomez \& Ashman
2011, Arceo-Gomez et al. 2019b). Thus, much remains to be done in order
to fully understand its ecological and evolutionary implications in
natural communities. Here I outline a few avenues of future research
that may help uncover the importance of HP in generating geographic
mosaics of selection and its contribution to shaping patterns of plant
diversity across local and global spatial scales.

\textbf{Within-species variation in HP receipt and effects}

First, future studies should more widely evaluate the variation in the
intensity of HP receipt for one or multiple species across their
geographic distributions. So far, very few studies have documented
changes in the dynamics of HP receipt for a single species across
spatial scales (e.g. compared to changes in pollen transfer network
structure), and the spatial scales studied tend to be small (two or very
few communities; e.g. Arceo-Gomez \& Ashman 2014a, Arceo-Gomez et al.
2018; but see Waites \& Agren 2004). So far, we have very little
empirical evidence of the extent of within-species variation in HP
receipt across natural communities. Such studies would constitute an
important first in advancing our understanding of the relevance of
geographic mosaics of HP transfer interactions in nature, as well as of
its potential ecological and evolutionary consequences. Second, studies
that evaluate the mediators of HP transfer dynamics (conspecific flower
density, plant and pollinator community composition) and the
directionality of their effects (increase or decrease HP receipt) are
key if we aim to understand the underlying drivers generating geographic
variation in HP interactions. This can be achieved via experimental
studies, where flower density and plant and pollinator community
composition are manipulated in the lab (e.g. Thomson et al. 2019) or
field conditions (e.g. de Waal et al. 2015, Bruckman \& Campbell 2016,
Brosi et al. 2017), or by taking advantage of existing natural variation
in the field (e.g. Arceo-Gomez \& Ashman 2014a, Albor et al. 2019). It
is also important to note that while some sources of variation are
expected to vary inconsistently across the landscape (e.g. conspecific
density and spatial arrangement) others may vary in a more predictable
manner (e.g. species diversity, resource availability). This latter more
predictable type of variation (i.e. geographic gradients) could then be
used to formulate and test specific predictions regarding the role of
these drivers in mediating variation in HP transfer interactions. For
instance, we could expect an increase in HP receipt with increasing
co-flowering diversity and a decrease in HP effects with increasing
resource availability. The importance of these mediators in influencing
HP transfer dynamics should also be evaluated singly and in combination
(e.g. de Waal et al. 2015, Thomson et al. 2019). This is becoming more
feasible with the development of powerful analytical techniques that
allow for simultaneous evaluation of multiple independent variables
(e.g. structural equation modeling; Albor et al. 2019).

Third, when evaluating HP effects, it is important that we move beyond
effects in species-pairs and start incorporating the complexity of HP
interactions within natural communities by acknowledging the intricacies
of HP loads (e.g. Arceo-Gomez et al. 2011) and the diversity of
co-flowering species involved (e.g. Fang \& Huang 2013, Arceo-Gomez et
al 2019b). Along these same lines, it is also important to design
studies that help understand how effects revealed by greenhouse
experiments may reflect expected outcomes in the field (e.g. Briggs et
al. 2016), and how these effects vary across a wide range of
environmental (Celaya et al. 2015) and biotic conditions (e.g.
Arceo-Gomez et al. 2016a). Such tests are necessary in order to gain a
more complete understanding of the causes and consequences of HP receipt
in natural communities and how these may contribute to generate
geographic mosaics of selection.

\textbf{Adaptive responses}

Evaluation of the potential adaptive responses to within-species
variation in HP receipt across the landscape (Arceo-Gomez \& Ashman
2014a, Arceo-Gomez et al. 2016a, Moreira-Hernandez \& Muchhala 2019)
remains a promising field of study. Here, several avenues of research
exist. First, studies that evaluate the potential for plant populations
to adapt to different HP transfer regimes (e.g. Hopkins \& Rausher 2012,
Arceo-Gomez et al. 2016a). This can be achieved by evaluating the
potential for natural selection on traits associated with HP tolerance
or avoidance strategies under different HP transfer environments (e.g.
Hopkins \& Rausher 2012, Tong \& Huang 2016), and/or via reciprocal
transplant experiments that evaluate patterns of local adaptation
(Arceo-Gomez \& Ashman 2014a). Hand-pollination studies that evaluate
population-level variation in HP effects under controlled conditions
would also be valuable to elucidate the potential for the evolution of
HP tolerance strategies in nature (e.g. Arceo-Gomez et al. 2016a, Tong
\& Huang 2016). Furthermore, few studies have measured traits and
fitness in communities of varying species composition (Johnson \&
Stinchcombe 2007), thereby assessing the potential role of diffuse
selection on species evolutionary trajectory as a response to HP
receipt.

Second, it is also important to design these studies in a way that we
can separate adaptive responses from the male (pollen) and female
(style/stigma) perspectives in order to fully assess the adaptive
potential of plants to HP effects. Such studies would also help to
pinpoint the exact mechanisms mediating HP tolerance and avoidance. For
instance, although several mechanisms/traits conferring HP tolerance
have been proposed such as longer styles or dry stigmas (reviewed in
Ashman \& Arceo-Gomez 2013), to date very few studies have attempted to
test these predictions (Tong \& Huang 2016, Arceo-Gomez et al. 2019b).
Thus, our understanding of the potential traits and mechanisms
conferring HP tolerance is still very limited. Third, there is also
evidence indicating that HP receipt may play an important role in mating
system evolution and in altering the genetic architecture of plant
populations, with so far unknown consequences (Arceo-Gomez \& Ashman
2014b). For instance, higher levels of outcrossing as a result of
greater HP receipt (Arceo-Gomez \& Ashman 2014b), could increase genetic
diversity and the rate of evolutionary change within populations (Hughes
et al. 2008). An increase in genetic diversity could also help generate
and maintain species diversity at the community-level via effects on
population-level fitness (Vellend \& Geber 2005, Hughes et al. 2008). In
spite of these tantalizing possibilities, to my knowledge, this very
promising avenue of research remains unexplored. Thus, studies that link
within-species variation in patterns of HP receipt, outcrossing rates
and levels of genetic diversity across populations with patterns of
species diversity across communities could offer transforming insights
on the role of HP receipt in shaping patterns of diversity not only
across spatial, but across biological scales (from genes to
communities).

\textbf{Pre-conditions for selection}

It would also be important to conduct studies that evaluate whether the
pre-conditions for HP receipt to exert natural selection on traits that
minimize HP effects in natural communities are met (i.e. opportunity for
selection). One such condition for instance would be that HP transfer
dynamics are relative stable over time (Ashman \& Arceo-Gomez 2013). If
HP transfer dynamics are highly stochastic over the years, or over
shorter periods of time, this would strongly limit the opportunity for
selection on traits that minimize HP effects in a population. To my
knowledge, the only study to date that has evaluated temporal stability
in patterns of HP receipt has found good support for this pre-condition
(Fang et al. 2019). Specifically, they showed constant patterns of HP
receipt (HP load size and diversity) in up to 34 insect-pollinated
species over three consecutive years. This result suggests that HP
receipt may not vary stochastically over time and that HP tolerance or
avoidance strategies could evolve in such communities (Fang et al.
2019). However, further research is necessary to determine whether this
is the case for other communities or if patterns of HP remain constant
over longer periods of time.

Another important test of the pre-conditions for natural selection would
be to evaluate how variance in HP receipt is structured spatially at
different hierarchical levels of biological organization (populations,
plants and individual flowers). For instance, from an evolutionary
perspective we can expect that the fraction of total variance that is
accounted for by within and among population differences in HP receipt
would be more directly related to the potential for natural selection to
act on traits that minimize HP effects (see Herrera 2002, Arceo-Gomez et
al. 2016c). On the other hand, a higher degree of within-plant
variability will greatly reduce the opportunity for selection on such
traits (Herrera 2002), as flowers within the same plant will experience
very different HP transfer regimes. Although a few studies have
evaluated how variance in conspecific pollen deposition is partitioned
among biological levels of organization (e.g. Herrera 2002, Arceo-Gomez
et al. 2016c), to my knowledge no study has evaluated how much of the
variance in HP receipt is accounted for by within- versus among-plant,
and among-population differences. Studies that partition the variability
in HP receipt at the scale of populations and below (individual plants
and flowers) are needed in order to gain a better understanding for the
opportunity of selection in natural communities. Such studies can also
provide insights into the factors underlying variation in HP receipt at
different spatial scales. For instance, greater among-population
variance would suggest that community-level attributes such as
conspecific flower density (e.g. de Waal et al. 2015, Thomson et al.
2019), or changes in co-flowering (e.g. Arceo-Gomez \& Ashman 2014a) and
pollinator community composition (e.g. Johnson \& Ashman 2019) are key
determinants of HP receipt. Greater among plant variance, on the other
hand, may indicate that within-species variation in intrinsic plant
traits (e.g. flower size; Arceo-Gomez et al. 2016b) or spatial
structuring within a site may play a more important role (Bruckman \&
Campbell 2016, Thomson et al. 2019). If greater variance in HP receipt
is observed among flowers within the same plants, then stochastic
pollination events may be more important (Herrera 2002, Fang \& Huang
2013, Arceo-Gomez et al. 2016b).

\textbf{Conclusions}

The drivers of variation discussed here may not be exhaustive, however,
they illustrate the high potential for geographic variation in the
intensity and effects of HP transfer interactions as well as in the
evolutionary responses to HP receipt. So far, the study of
pollinator-mediated plant-plant interactions has been almost entirely
dominated by studies of pre-pollination interactions even though their
outcomes are influenced by plant-plant interactions that take place on
the stigma after pollen has been deposited. Therefore, it is paramount
that we fully evaluate the causes, consequences and context-dependency
of HP transfer interactions in order to gain a more complete
understanding of the role that plant-pollinator interactions play in
generating and organizing plant biodiversity. It is also important to
acknowledge that the number of studies documenting patterns of HP
receipt is still limited and strongly biased towards temperate systems
(Arceo-Gomez et al. 2019a; Fig. 3). Studies on HP transfer dynamics in
highly diverse regions such as in Africa and South America are largely
underrepresented (Fig. 3; Arceo-Gomez et al 2019a). Biases in studies of
HP receipt are not only geographical but also phylogenetic as large
groups of plants have also been poorly represented in these studies
(e.g. monocotyledons; Arceo-Gomez et al. 2019a). Thus, there is an
urgent need to evaluate patterns of variation in HP receipt at larger
spatial and phylogenetic scales. Knowledge of wide-scale patterns of HP
receipt may help uncover its potential role in shaping patterns of plant
diversity at a global scale.

\textbf{Acknowledgments}

The author thanks R. Raguso and V. Parra-Tabla for comments on an
earlier version of this manuscript. GAG was supported by NSF DEB
1931163. The author has no conflict of interests to declare.

\textbf{Author contributions}

GAG conceptualized the ideas and wrote the manuscript.

\textbf{References}

Aizen, M. A. et al. 1990. Among\selectlanguage{english}-and within\selectlanguage{english}-flower comparisons of pollen
tube growth following self\selectlanguage{english}-and cross\selectlanguage{english}-pollinations in \emph{Dianthus
chinensis} (Caryophyllaceae).~\emph{American Journal of Botany}
.\emph{~77} : 671-676.

Albor, C. et al. 2019. Taxonomic and functional diversity of the
co\selectlanguage{english}-flowering community differentially affect \emph{Cakile
edentula}pollination at different spatial scales.~\emph{Journal of
Ecology} .~\emph{107} : 2167-2181.

Andonian, K. et al. 2012. Geographic mosaics of plant--soil microbe
interactions in a global plant invasion.~\emph{Journal of Biogeography}
.~\emph{39} : 600-608.

Arceo\selectlanguage{english}-Gomez, G. and Ashman, T.L. 2011. Heterospecific pollen deposition:
does diversity alter the consequences?~\emph{New Phytologist}
,~\emph{192} : 738-746.

Arceo-Gomez, G. and Ashman, T.L. 2014a. Coflowering community context
influences female fitness and alters the adaptive value of flower
longevity in \emph{Mimulus guttatus} .~\emph{The American Naturalist}
,~\emph{183} : E50-E63.

Arceo-Gomez, G. and Ashman, T.L. 2014b. Heterospecific pollen receipt
affects self pollen more than outcross pollen: implications for
mixed\selectlanguage{english}-mating plants.~\emph{Ecology} ,~\emph{95} : 2946-2952.

Arceo\selectlanguage{english}-Gomez, G. et al. 2016a. Can plants evolve tolerance mechanisms to
heterospecific pollen effects? An experimental test of the adaptive
potential in \emph{Clarkia} species.~\emph{Oikos} ,~\emph{125} :
718-725.

Arceo\selectlanguage{english}-Gomez, G. et al. 2016b. Patterns of among\selectlanguage{english}-and within\selectlanguage{english}-species
variation in heterospecific pollen receipt: The importance of ecological
generalization.~\emph{American Journal of Botany} ,~\emph{103} :
396-407.

Arceo\selectlanguage{english}-Gomez, G. et al. 2016c. Patterns and sources of variation in
pollen deposition and pollen tube formation in flowers of the endemic
monoecious shrub \emph{Cnidoscolus souzae} (Euphorbiaceae).~\emph{Plant
Biology} ,~\emph{18} : 594-600.

Arceo\selectlanguage{english}-Gomez, G. et al. 2018. Variation in sampling effort affects the
observed richness of plant--plant interactions via heterospecific pollen
transfer: implications for interpretation of pollen transfer
networks.~\emph{American journal of botany} ~\emph{105} : 1601-1608.

Arceo-Gomez, G. et al. 2019a. Global geographic patterns of
heterospecific pollen receipt help uncover potential ecological and
evolutionary impacts across plant communities
worldwide.~\emph{Scientific reports} ,~\emph{9} : 1-9.

Arceo-Gomez, G., et al. 2019b. Interactive effects between donor and
recipient species mediate fitness costs of heterospecific pollen receipt
in a co-flowering community.~\emph{Oecologia} ,~\emph{189} : 1041-1047.

Armbruster, W.S. et al. 2014. Do specialized flowers promote
reproductive isolation? Realized pollination accuracy of three
sympatric\emph{Pedicularis} species.~\emph{Annals of Botany}
,~\emph{113} : 331-340.

Ashman, T\selectlanguage{english}-L. and Arceo\selectlanguage{english}-Gomez, G. 2013. Toward a predictive understanding
of the fitness costs of heterospecific pollen receipt and its importance
in co\selectlanguage{english}-flowering communities.~\emph{American Journal of Botany} ~100:
1061-1070.

Ashman, T-L., Arceo-Gomez, G., Bennett, J.M. and Knight, T.M., 2020. Is
heterospecific pollen receipt the missing link in understanding pollen
limitation of plant reproduction?~\emph{American Journal of Botany} ,
107: 845-847.

Ashman, T.L. et al. 2020. Pollen on stigmas as proxies of pollinator
competition and facilitation: complexities, caveats and future
directions.~\emph{Annals of Botany} ,~\emph{125} : 1003-1012.

Barrett, S.C. and Helenurm, K. 1987. The reproductive biology of boreal
forest herbs. I. Breeding systems and pollination.~\emph{Canadian
Journal of Botany} ,~\emph{65} : 2036-2046.

Barrett, S.C. and Husband, B.C. 1990. Variation in outcrossing rates
in\emph{Eichhornia paniculata} : the role of demographic and
reproductive factors.~\emph{Plant Species Biology} ,~\emph{5} : 41-55.

Bascompte, J. et al. 2003. The nested assembly of plant--animal
mutualistic networks. \emph{Proceedings of the National Academy of
Sciences} , 100: 9383-9387.

Bawa, K.S. 1990. Plant-pollinator interactions in tropical rain
forests.~\emph{Annual review of Ecology and Systematics} , 21: 399-422.

Bedinger, P.A. et al. 2011. Interspecific reproductive barriers in the
tomato clade: opportunities to decipher mechanisms of reproductive
isolation.~\emph{Sexual Plant Reproduction} ,~\emph{24} : 171-187.

Borgella Jr, R. et al. 2001. Species Richness and Pollen Loads of
Hummingbirds Using Forest Fragments in Southern Costa
Rica.\emph{Biotropica} ,~\emph{33} : 90-109.

Briggs, H.M. et. al. 2016. Heterospecific pollen deposition
in\emph{Delphinium barbeyi} : linking stigmatic pollen loads to
reproductive output in the field.~\emph{Annals of Botany} ,~\emph{117} :
341-347.

Brosi, B.J. et al. 2017. Experimental species removals impact the
architecture of pollination networks. Biology letters, 13: 20170243.

Bruckman, D. and Campbell, D.R. 2016. Pollination of a native plant
changes with distance and density of invasive plants in a simulated
biological invasion.~\emph{American journal of botany} ,~\emph{103} :
1458-1465.

Busch, J.W. and Schoen, D.J. 2008. The evolution of self-incompatibility
when mates are limiting.~\emph{Trends in plant science} ,~\emph{13} :
128-136.

Campbell, A.W. et al. 2001. The importance of light intensity for pollen
tube growth and embryo survival in wheatx maize crosses.~\emph{Annals of
Botany} ,~\emph{87} : 517-522.

Carstensen, D.W. et al. 2014. Beta diversity of plant-pollinator
networks and the spatial turnover of pairwise interactions.~\emph{PLoS
One} ,~\emph{9} : 112903.

Celaya, I.N. et al. 2015. Negative effects of heterospecific pollen
receipt vary with abiotic conditions: ecological and evolutionary
implications.~\emph{Annals of botany} ,~\emph{116} : 789-795.

Chapin, F.S. et al. 1987. Plant responses to multiple environmental
factors.~\emph{Bioscience} ,~\emph{37} : 49-57.

Cosacov, A. et al. 2008. Variation of pollinator assemblages and pollen
limitation in a locally specialized system: the
oil-producing\emph{Nierembergia linariifolia} (Solanaceae).~\emph{Annals
of botany} ,~\emph{102} : 723-734.

Cruzan, M.B. and Barrett, S.C. 1993. Contribution of cryptic
incompatibility to the mating system of \emph{Eichhornia
paniculata}(pontederiaceae).~\emph{Evolution} ,~\emph{47} : 925-934.

Daniels, J.D. and Arceo-Gomez, G. 2020. Effects of invasive\emph{Cirsium
arvense} on pollination in a southern Appalachian floral community vary
with spatial scale and floral symmetry.~\emph{Biological Invasions}
,~\emph{22} : 783-797.

Davis, M.A. et al. 2000. Fluctuating resources in plant communities: a
general theory of invasibility.~\emph{Journal of ecology} ,~\emph{88} :
528-534.

de Waal, C. et al. 2015. Relative density and dispersion pattern of two
southern African Asteraceae affect fecundity through heterospecific
interference and mate availability, not pollinator visitation
rate.~\emph{Journal of Ecology} ,~\emph{103} : 513-525.

Eaton, D.A. et al. 2012. Floral diversity and community structure
in\emph{Pedicularis} (Orobanchaceae).~\emph{Ecology} ,~\emph{93} :
S182-S194.

Emer, C. et al. 2015. The impact of the invasive alien
plant,\emph{Impatiens glandulifera} , on pollen transfer
networks.~\emph{PloS one} ,~\emph{10} : 0143532.

Encinas\selectlanguage{english}-Viso, F. et al. 2020. The loss of self\selectlanguage{english}-incompatibility in a
range expansion.~\emph{Journal of Evolutionary Biology} .
https://doi.org/10.1111/jeb.13665

Fang, Q. and Huang, S.Q. 2013. A directed network analysis of
heterospecific pollen transfer in a biodiverse community.~\emph{Ecology}
,~\emph{94} : 1176-1185.

Fang, Q. et al. 2019. Multi\selectlanguage{english}-year stigmatic pollen\selectlanguage{english}-load sampling reveals
temporal stability in interspecific pollination of flowers in a
subalpine meadow.~\emph{Oikos} ,~\emph{128} : 1739-1747.

Feng, H. et al. 2000. Effect of enhanced ultraviolet-B radiation on
pollen germination and tube growth of 19 taxa in
vitro.~\emph{Environmental and Experimental Botany} ,~\emph{43} : 45-53.

Fishman, L. and Wyatt, R. 1999. Pollinator\selectlanguage{english}-mediated competition,
reproductive character displacement, and the evolution of selfing
in\emph{Arenaria uniflora} (Caryophyllaceae).~\emph{Evolution}
,~\emph{53} : 1723-1733.

Gandon, S. and Nuismer, S.L. 2009. Interactions between genetic drift,
gene flow, and selection mosaics drive parasite local
adaptation.~\emph{The American Naturalist} ,~\emph{173} : 212-224.

Gomulkiewicz, R. et al. 2000. Hot spots, cold spots, and the geographic
mosaic theory of coevolution.~\emph{The American Naturalist}
,~\emph{156} : 156-174.

Hanoteaux, S. et al. 2013. Effects of spatial patterns on the
pollination success of a less attractive species.~\emph{Oikos}
,~\emph{122} : 867-880.

Hargreaves, A.L. and Eckert, C.G. 2014. Evolution of dispersal and
mating systems along geographic gradients: implications for shifting
ranges.~\emph{Functional ecology} ,~\emph{28} : 5-21.

Hegland, S.J. and Boeke, L. 2006. Relationships between the density and
diversity of floral resources and flower visitor activity in a temperate
grassland community.~\emph{Ecological Entomology} ,~\emph{31} : 532-538.

Herrera, C.M. 1988. Variation in mutualisms: the spatiotemporal mosaic
of a pollinator assemblage.~\emph{Biological Journal of the Linnean
Society} ,~\emph{35} : 95-125.

Herrera, C.M. 1995. Microclimate and individual variation in
pollinators: flowering plants are more than their
flowers.~\emph{Ecology} ,~\emph{76} : 1516-1524.

Herrera, C.M. 2002. Censusing natural microgametophyte populations:
variable spatial mosaics and extreme fine\selectlanguage{english}-graininess in
winter\selectlanguage{english}-flowering\emph{Helleborus foetidus}
(Ranunculaceae).~\emph{American Journal of Botany} ,~\emph{89} :
1570-1578.

Hiscock, S.J. and Dickinson, H.G. 1993. Unilateral incompatibility
within the Brassicaceae: further evidence for the involvement of the
self-incompatibility (S)-locus.~\emph{Theoretical and Applied Genetics}
,~\emph{86} : 744-753.

Hopkins, R. and Rausher, M.D. 2012. Pollinator-mediated selection on
flower color allele drives reinforcement.~\emph{Science} ,~\emph{335} :
1090-1092.

Hughes, A.R. et al. 2008. Ecological consequences of genetic
diversity.~\emph{Ecology letters} ,~\emph{11} : 609-623.

Ivey, C.T. and Carr, D.E. 2005. Effects of herbivory and inbreeding on
the pollinators and mating system of \emph{Mimulus
guttatus}(Phrymaceae).~\emph{American Journal of Botany} ,~\emph{92} :
1641-1649.

Iwao, K. and Rausher, M.D. 1997. Evolution of plant resistance to
multiple herbivores: quantifying diffuse coevolution.~\emph{The American
Naturalist} ,~\emph{149} : 316-335.

Johnson, A.L. and Ashman, T.L. 2019. Consequences of invasion for pollen
transfer and pollination revealed in a tropical island
ecosystem.~\emph{New Phytologist} ,~\emph{221} : 142-154.

Johnson, M.T. and Stinchcombe, J.R. 2007. An emerging synthesis between
community ecology and evolutionary biology.~\emph{Trends in ecology \&
evolution} ,~\emph{22} : 250-257.

Kaiser-Bunbury, C.N. et al. 2017. Ecosystem restoration strengthens
pollination network resilience and function.~\emph{Nature} ,~\emph{542}
: 223-227.

Kanchan, S. and Chandra, J. 1980. Pollen allelopathy---a new
phenomenon.~\emph{New Phytologist} ,~\emph{84} : 739-746.

Kay, K.M. and Schemske, D.W. 2008. Natural selection reinforces
speciation in a radiation of neotropical rainforest
plants.~\emph{Evolution: International Journal of Organic Evolution}
,~\emph{62} : 2628-2642.

Kay, K.M. et al. 2019. Experimental sympatry reveals geographic
variation in floral isolation by hawkmoths.~\emph{Annals of botany}
,~\emph{123} : 405-413.

King, C. et al. 2013. Why flower visitation is a poor proxy for
pollination: measuring single\selectlanguage{english}-visit pollen deposition, with implications
for pollination networks and conservation.~\emph{Methods in Ecology and
Evolution} ,~\emph{4} : 811-818.

Kruszewski, L.J. and Galloway, L.F. 2006. Explaining outcrossing rate
in\emph{Campanulastrum americanum} (Campanulaceae): geitonogamy and
cryptic self-incompatibility.~\emph{International Journal of Plant
Sciences} ,~\emph{167} : 455-461.

Kunin, W.E. 1997. Population size and density effects in pollination:
pollinator foraging and plant reproductive success in experimental
arrays of \emph{Brassica kaber} .~\emph{Journal of Ecology} , 85:
225-234.

Lankinen, A. 2001. In vitro pollen competitive ability in Viola
tricolor: temperature and pollen donor effects.~\emph{Oecologia}
,~\emph{128} : 492-498.

Lush, et al. 1998. Directional guidance of \emph{Nicotiana alata} pollen
tubes in vitro and on the stigma.~\emph{Plant Physiology} ,~\emph{118} :
733-741.

McLernon, S.M. et al. 1996. Heterospecific pollen transfer between
sympatric species in a midsuccessional old\selectlanguage{english}-field
community.~\emph{American Journal of Botany} ,~\emph{83} : 1168-1174.

Mazer, S.J. et al. 2010. The joint evolution of mating system and pollen
performance: predictions regarding male gametophytic evolution in
selfers vs. outcrossers.~\emph{Perspectives in Plant Ecology, Evolution
and Systematics} ,~\emph{12} : 31-41.

Minnaar, C. et al. 2019a. Intraspecific divergence in floral\selectlanguage{english}-tube length
promotes asymmetric pollen movement and reproductive
isolation.~\emph{New Phytologist} ,~\emph{224} : 1160-1170.

Minnaar, C. et al. 2019b. Plant--pollinator interactions along the
pathway to paternity.~\emph{Annals of Botany} ,~\emph{123} : 225-245.

Mitchell, R. J. et al. 2009. New frontiers in competition for
pollination. Annals of botany, 103: 1403-1413.

Montgomery, B.R. and Rathcke, B.J. 2012. Effects of floral
restrictiveness and stigma size on heterospecific pollen receipt in a
prairie community.~\emph{Oecologia} ,~\emph{168} : 449-458.

Morales, C.L. and Traveset, A. 2008. Interspecific pollen transfer:
magnitude, prevalence and consequences for plant fitness.~\emph{Critical
Reviews in Plant Sciences} ,~\emph{27} : 221-238.

Moreira-Hernandez, J.I. and Muchhala, N. 2019. Importance of
pollinator-mediated interspecific pollen transfer for angiosperm
evolution.~\emph{Annual Review of Ecology, Evolution, and Systematics}
,~\emph{50} : 191-217.

Muchhala, N. et al. 2010. Competition drives specialization in
pollination systems through costs to male fitness.~\emph{The American
Naturalist} ,~\emph{176} : 732-743.

Muchhala, N. and Jarrin\selectlanguage{english}-V, P. 2002. Flower Visitation by Bats in Cloud
Forests of Western Ecuador1.~\emph{Biotropica} ,~\emph{34} : 387-395.

Muchhala, N. and Potts, M.D. 2007. Character displacement among
bat-pollinated flowers of the genus \emph{Burmeistera} : analysis of
mechanism, process and pattern.~\emph{Proceedings of the Royal Society
B: Biological Sciences} ,~\emph{274} : 2731-2737.

Muchhala, N. and Thomson, J.D. 2012. Interspecific competition in
pollination systems: costs to male fitness via pollen
misplacement.~\emph{Functional Ecology} ,~\emph{26} : 476-482.

Murfett, J. et al. 1996. S RNase and interspecific pollen rejection in
the genus Nicotiana: multiple pollen-rejection pathways contribute to
unilateral incompatibility between self-incompatible and self-compatible
species.~\emph{The Plant Cell} ,~\emph{8} : 943-958.

Nasrallah, M.E. et al. 2004. Natural variation in expression of
self-incompatibility in Arabidopsis thaliana: implications for the
evolution of selfing.~\emph{Proceedings of the National Academy of
Sciences} ,~\emph{101} : 16070-16074.

Ness, R.W. et al. 2010. Mating-system variation, demographic history and
patterns of nucleotide diversity in the tristylous plant\emph{Eichhornia
paniculata} .~\emph{Genetics} ,~\emph{184} : 381-392.

Olesen, J.M. and Jordano, P. 2002. Geographic patterns in
plant--pollinator mutualistic networks.~\emph{Ecology} ,~\emph{83} :
2416-2424.

Parra\selectlanguage{english}-Tabla, V. et al. 2020. Pollen transfer networks reveal alien
species as main heterospecific pollen donors with fitness consequences
for natives.~\emph{Journal of Ecology} . 10.1111/1365-2745.13520.

Phillips, R.D. et al. 2020. Niche Perspectives on Plant--Pollinator
Interactions. Trends in Plant Science 25: 779-793.

Randle, A.M. et al. 2018. Shifts to earlier selfing in sympatry may
reduce costs of pollinator sharing.~\emph{Evolution} ,~\emph{72} :
1587-1599.

Rathcke, B. 1983. Competition and facilitation among plants for
pollination.~In Real L. \emph{Pollination biology} , Academic
Press,~pp\emph{305} -329.

Reinartz, J.A. and Les, D.H. 1994. Bottleneck\selectlanguage{english}-induced dissolution of
self\selectlanguage{english}-incompatibility and breeding system consequences in \emph{Aster
furcatus} (Asteraceae).~\emph{American Journal of Botany} ,~\emph{81} :
446-455.

Robertson, C. 1895. The philosophy of flower seasons, and the
phaenological relations of the entomophilous flora and the anthophilous
insect fauna. The American Naturalist, 29: 97-117.

Ruane, L.G. and Donohue, K. 2007. Environmental effects on
pollen--pistil compatibility between \emph{Phlox cuspidata} and \emph{P.
drummondii} (Polemoniaceae): implications for hybridization dynamics.
American journal of botany, 94: 219-227.

Sargent, R.D. and Ackerly, D.D. 2008. Plant--pollinator interactions and
the assembly of plant communities. Trends in Ecology \& Evolution, 23:
123-130.

Searcy, K.B. and Macnair, M.R. 1990. Differential seed production
in\emph{Mimulus guttatus} in response to increasing concentrations of
copper in the pistil by pollen from copper tolerant and sensitive
sources. Evolution, 44: 1424-1435.

Singer, M.C. and McBride, C.S. 2012. Geographic mosaics of species'
association: a definition and an example driven by plant--insect
phenological synchrony.~\emph{Ecology} ,~\emph{93} : 2658-2673.

Spigler, R.B. and Chang, S.M. 2008. Effects of plant abundance on
reproductive success in the biennial \emph{Sabatia
angularis}(Gentianaceae): spatial scale matters.~\emph{Journal of
Ecology} ,~\emph{96} : 323-333.

Stinchcombe, J.R. and Rausher, M.D. 2001. Diffuse selection on
resistance to deer herbivory in the ivyleaf morning glory, Ipomoea
hederacea.~\emph{The American Naturalist} ,~\emph{158} : 376-388.

Tamaki, I. et al. 2009. Interpopulation variation in mating system and
late\selectlanguage{english}-stage inbreeding depression in \emph{Magnolia stellata}
.~\emph{Molecular Ecology} ,~\emph{18} : 2365-2374.

Thompson, J.N. 1999. Specific hypotheses on the geographic mosaic of
coevolution.~\emph{The American Naturalist} ,~\emph{153} : S1-S14.

Thompson, J.N. and Cunningham, B.M. 2002. Geographic structure and
dynamics of coevolutionary selection.~\emph{Nature} ,~\emph{417} :
735-738.

Thomson, J.D. et al. 1982a. The effect of a foreign pollen on ovule
development in \emph{Diervilla lonicera} (Caprifoliaceae). \emph{New
Phytologist} , 90: 777-783.

Thomson, J.D. et al. 1982b. Behavior of bumble bee pollinators
of\emph{Aralia hispida} Vent. (Araliaceae).~\emph{Oecologia} ,~\emph{54}
: 326-336.

Thomson, J.D. et al. 2019. Effects of spatial patterning of co-flowering
plant species on pollination quantity and purity.~\emph{Annals of
Botany} ,~\emph{123} : 303-310.

Toju, H. and Sota, T. 2006. Imbalance of predator and prey armament:
geographic clines in phenotypic interface and natural
selection.~\emph{The American Naturalist} ,~\emph{167} : 105-117.

Tong, Z.Y. and Huang, S.Q. 2016. Pre\selectlanguage{english}-and post\selectlanguage{english}-pollination interaction
between six co\selectlanguage{english}-flowering \emph{Pedicularis} species via heterospecific
pollen transfer.~\emph{New Phytologist} ,~\emph{211} : 1452-1461.

Torang, P. et al. 2010. Habitat quality and among-population
differentiation in reproductive effort and flowering phenology in the
perennial herb \emph{Primula farinosa} . \emph{Evolutionary Ecology} ,
24: 715-729.

Tur, C. et al. 2016. Evaluating the effects of pollinator\selectlanguage{english}-mediated
interactions using pollen transfer networks: evidence of widespread
facilitation in south Andean plant communities.~\emph{Ecology Letters}
,~\emph{19} : 576-586.

Vellend, M. and Geber, M.A. 2005. Connections between species diversity
and genetic diversity.~\emph{Ecology Letters} ,~\emph{8} : 767-781.

Waelti, et al. 2008. Floral odour and reproductive isolation in two
species of \emph{Silene} . \emph{Journal of evolutionary biology} , 21:
111-121.

Waites, A.R. and Agren, J.O.N. 2004. Pollinator visitation, stigmatic
pollen loads and among\selectlanguage{english}-population variation in seed set in \emph{Lythrum
salicaria} .~\emph{Journal of Ecology} ,~\emph{92} : 512-526.

Waser, N.M. 1978. Competition for hummingbird pollination and sequential
flowering in two Colorado wildflowers.~\emph{Ecology} ,~\emph{59} :
934-944.

Waser, N.M. et al. 1996. Generalization in pollination systems, and why
it matters.~\emph{Ecology} ,~\emph{77} : 1043-1060.

Weller, S.G. and Ornduff, R. 1977. Cryptic self-incompatibility
in\emph{Amsinckia grandiflora} . \emph{Evolution} , 31: 47-51.

Whitehead, M.R. et al. 2018. Plant mating systems often vary widely
among populations. \emph{Frontiers in Ecology and Evolution} , 6: 38.

\textbf{Figure 1.} Four predicted sources of within-species variation in
HP receipt across spatial scales depicted here as two populations.
Examples of studies providing supporting evidence for the role of each
source of variation in mediating HP transfer dynamics are presented.

\textbf{Figure 2} Three predicted sources of within-species variation in
the intensity of HP effects across spatial scales depicted here as two
populations. Examples of studies providing supporting evidence for the
role of each source of variation in mediating HP effects are presented.

\textbf{Figure 1}\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/image1/image1}

\end{center}
\end{figure}

\textbf{Figure 2}\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/image2/image2}

\end{center}
\end{figure}

\textbf{Figure 3} Global distribution of 26 studies (red circles) that
have evaluated the intensity of HP receipt for 245 plant species across
temperate and tropical regions between 1986 and 2017 (modified from
Arceo-G\selectlanguage{ngerman}ómez et al. 2019a).\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/image3/image3}

\end{center}
\end{figure}

\selectlanguage{english}
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