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.