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-Gómez 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.