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-Gómez 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-Gómez (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-Gómez 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 Phlox drummondiipopulations as a result of HP transfer from Phlox cuspidata.Selective pressure on genes that affected floral pigmentation occurred
only in sympatric 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 Costus species, and not in isolated
populations, thus providing evidence for geographic mosaics of selection
on HP tolerance strategies (also see Arceo-Gómez et al. 2016a).
Furthermore, 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-Gómez & 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-Gómez & 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 inArenaria uniflora populations that grew in sympatry with
congeneric A. glabra. They further 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-Gómez & 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-Gómez 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-Gómez 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.