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-Gómez
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).
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 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-Gómez 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.
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-Gómez 2013, Arceo-Gómez 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-Gómez 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-Gómez
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-Gómez et al. (2016a)
showed evidence indicating that Clarkia xantiana populations vary
in their level of HP tolerance according to their history of exposure to
HP. Specifically, 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-Gómez 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-Gómez 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-Gómez 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.
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-Gómez 2013), self-pollen may be more susceptible
to HP effects compared with outcross pollen (Arceo-Gómez & 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 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-Gómez & Ashman 2014b).
Specifically, HP reduced self-pollen tube growth by an additional 32%
compared with outcross pollen (Arceo-Gómez & 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-Gómez 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-Gómez
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.