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• W2770299250 abstract "The diversity of plant mating systems has inspired many researchers including Darwin (1876) to ponder why and how these systems have evolved. In particular, mating via a combination of selfing and outcrossing (“mixed mating”) has classically been posed as a paradox; models considering the fundamental genetic parameters driving mating-system evolution—the automatic transmission advantage and inbreeding depression—predict evolutionary stability only of complete selfing or complete outcrossing. In brief, because selfers and outcrossers both transmit copies of genes through pollen but selfers transmit twice as many through seed, selfers have an automatic advantage at the gene-level compared to outcrossers (Fig. 1A). Consequently, selfing should fix in the population unless the relative reduction in fitness of inbred vs. outbred progeny (inbreeding depression) outweighs the 50% transmission advantage, in which case outcrossing should be fixed. Yet numerous studies show that species exhibit mixed mating (Fig. 2). Many researchers (including us) have approached studying the evolution of mixed mating by asking, “Why might selfing persist despite high inbreeding depression?” (Fig. 2, section II). Interestingly, data also show that mixed mating and even high rates of outcrossing (>0.8) are common in self-compatible populations where inbreeding depression is below 0.5 (Fig. 2, sections IV and V). Here, we turn the original question around to ask, “Why might outcrossing persist in populations despite relatively low inbreeding depression?” and consider constraints posed by pollinator mutualists. Comparison of fitness between selfers and outcrossers at the gene level considering transmission advantage, persistent pollinators, and pollen discounting. Alleles are represented as small circles within an individual, and different individuals have differently colored alleles. Arrows indicate transmission to offspring. (A) Selfers have an automatic 3:2 transmission advantage at the gene level because they pass three allele copies (two through selfed seed, one through pollen export; shown in blue) to the next generation for every two alleles passed by outcrossers (one through seed, one through pollen export; shown in yellow). (B) If pollinators are highly abundant, outcross pollen delivery may overwhelm or occur before self-pollen deposition. By effectively enforcing outcrossed seed production, pollinators could “erase” the transmission advantage of selfing. (C) Under pollen discounting, a negative relationship between the amount of pollen exported and that available for self-fertilization eliminates or reduces the transmission advantage. All three scenarios are relevant only where there is sufficient transfer of pollen by pollinators. Relationship between inbreeding depression and primary selfing rate (i.e., corrected for early inbreeding depression; selfing rate = 1 - outcrossing rate) for 39 hermaphroditic, angiosperm species (N = 48 populations). Gray lines divide the graph into sections corresponding to populations considered primarily outcrossing (I, IV), mixed mating (II, V) or primarily selfing (III, IV) and with inbreeding depression greater than (I, II, III) or less than (IV, V, VI) the classic boundary line predicting whether selfing should evolve. Orange dots in sections IV and V highlight the apparent conundrum of species with relatively low inbreeding depression (<0.5) but that are either mixed mating (V) or considered to be primarily outcrossing (IV). Even assuming underestimation of reported values of inbreeding expression by 50%, 23% of all populations shown would still reside in sections IV and V. Adapted from Winn et al. (2011). Understanding the evolution of selfing given high inbreeding depression is perhaps best explained considering outcross pollen limitation. The reproductive assurance hypothesis posits that unreliable pollinators or low mate availability leave plants no better fitness option but to self, given the alternative of making fewer or even no seeds. A number of excellent models incorporate outcross pollen limitation (Goodwillie et al., 2005), and empirical studies support components of the reproductive assurance hypothesis (Busch and Delph, 2012). While this hypothesis is well accepted as an important driver of the evolution of selfing and the maintenance of mixed mating, it is one-sided in shedding light on mating system evolution because it does not explain moderate to high levels of outcrossing when inbreeding depression is low. We proffer that an explanation for persistent outcrossing given low inbreeding depression may lie in viewing the evolution of selfing through the lens of mutualism breakdown (Sachs and Simms, 2006) and the potential difficulties for self-compatible plants in divesting from their mutualist pollinators. Conflict could arise from the evolution of higher autonomous selfing rates because, while autonomously selfing plants are less reliant on their pollinator mutualists, there are ecological conditions where pollinators may remain strongly reliant on the plant for pollen and nectar. The resulting asymmetry would effect continued outcross pollen delivery, significantly slowing the progression of mutualism abandonment by the plant and thus evolution to high selfing. Notably, the asymmetry should be greatest where pollinators are abundant. Yet, pollen limitation is often seen as ubiquitous. Despite this perception, conditions with abundant pollinators providing adequate outcross pollen may be common. Indeed, Knight et al. (2006) revealed clear publication bias for reporting pollen limitation and that, when measured over a plant's lifetime, the magnitude of pollen limitation on average is actually low, especially for monocarpic species, which constitute half of the species inhabiting the seemingly paradoxical state space of moderate to high outcrossing levels with low inbreeding (Fig. 2, sections IV and V). This “persistent pollinator” hypothesis therefore predicts that outcrossing will be maintained where pollinators effectively block selfing, erasing the automatic transmission advantage via seed production (Fig. 1B). Holsinger (1991) similarly recognized the importance of pollinator abundance in explaining mixed mating in the absence of inbreeding depression. Under high pollen export rates, pollen discounting, the trade-off between using one's pollen to self-fertilize ovules and the opportunity for outcrossing, reduces the transmission advantage, stabilizing mixed mating (Fig. 1C). Otherwise, under pollen limitation, complete selfing always evolves. Tests of pollen discounting remain rare, in large part because they are so difficult to do. The results from the handful of test on pollen discounting have been inconsistent (Busch and Delph, 2012). Thus, we are left with mixed-mating species that have no to low inbreeding depression and similarly low to no pollen discounting (e.g., Ipomoea purpurea, Rausher et al., 1993). For some species, it may be that inbreeding depression is simply underestimated or is low because populations are small, such that drift leads to fixation of deleterious alleles and constrains adaptive evolution more generally. But for others, we maintain that ecological forces may be at play, and in considering the evolution of selfing as a form of mutualism breakdown, we place the emphasis on the (in)ability of plants to abandon their persistent pollinators for the shift to complete selfing to emerge. When pollinators are limiting, this breakdown reduces to the case of reproductive assurance because of pollinator abandonment. But, under conditions of high pollinator abundance, we speculate that high selfing is possible only when autonomous selfing ability evolves in concert with traits that enable self-compatible plants to avoid their persistent pollinators, self-pollinate, and regain their transmission advantage. To understand the evolution of complete selfing from mixed mating, we then need to ask: What traits might coevolve with autonomous selfing ability to enable plants to avoid their pollinators? And what might constrain them from being able to do so? We see two routes: escape or hide. One way plants could escape is through shifting the timing of autonomous selfing during a flower's lifespan. Lloyd (1979) defined the occurrence of selfing at three times across the floral lifespan that can alter the likelihood of selfed seed set relative to the opportunity for outcross pollen delivery. “Prior” selfing occurs before this opportunity, while “competing” occurs at the same time, and “delayed” happens afterward. Delayed selfing is widely seen as a mechanism of reproductive assurance and will result in higher rates of selfing when pollinators are absent, but only prior selfing allows for high rates of selfing when pollinators are abundant. Consequently, higher selfing rates could evolve under high outcross pollen receipt and low inbreeding depression when there is variation in floral traits that permits prior selfing. However, the evolution of complete selfing would still be constrained, if, for example, the mechanism of prior selfing promotes sexual conflict between male and female functions (sensu Barrett, 2002). Alternatively, plants could escape by offsetting timing of flowering from pollinators’ phenologies, but clear ecological and physiological limits exist that would leave some populations “stuck” as mixed maters. For example, the earliest (or latest) flowering species within a community may be the main food resource for the pollinator community, visited by newly emerging (or late season) pollinators to a greater degree than species that flower midseason. Or, the quality of growth conditions can physiologically limit how much earlier (or later) a plant population can flower to avoid pollinators, especially for those that already bloom on the tails of the growing season. In ephemeral habitats, flowering and pollinator emergence may be triggered by the same environmental cues, making it difficult for plants to avoid pollinator visitation. Indeed, long-term data from areas experiencing climate change suggest that shifts in bee emergence keep pace with shifts in plant species’ phenology (Bartomeus et al., 2011). While coshifting phenologies are a boon to reproduction for species that require pollinators for seed set, this scenario sets up red queen-like conditions for self-compatible plants that could otherwise gain fitness benefits through selfing. That is, although earlier flowering plants may be favored initially because they can realize higher selfing rates, selection subsequently favors earlier emerging pollinators that track their floral resource but again enforce outcrossing. Rather than run, plants could hide. Because pollinators typically favor larger floral displays and greater rewards, only “unattractive” plants may be able to realize higher selfing rates. Thus, we might expect correlated selection on selfing ability and (un)attractive traits where pollinators are abundant. This scenario provides perhaps another way to look at “selfing syndrome” evolution (Sicard and Lenhard, 2011). Still, plants may be constrained by how much attraction can be reduced. For example, even large decreases in floral attractiveness may not deter pollinators if the plant serves as their main resource. Nectar investment can be eliminated completely, but pollen investment can only drop so much before self-pollination fails to function effectively. That the evolution of selfing may be thwarted by persistent pollinators is an idea that seems so simple but has not been explicitly addressed. We note that this scenario would not apply to self-incompatible species and is specific to conditions of negligible pollen limitation and pollen discounting. We also assume that sibling competition is of minimal importance (e.g., Schmitt and Ehrhardt, 1987) and acknowledge that other forces such as economics of reduced floral investment may be at play. A key expectation is that for self-compatible species under those conditions and free from the negative genetic consequences of selfing, it is not enough for the capacity to self to evolve—it must be selected in concert with traits related to pollinator avoidance that influence the realized individual selfing rate. Although selection on individual selfing rate per se and its connection to floral traits has previously been suggested (Johnston et al., 2009), studies remain to be done. These could involve using experimental arrays of individuals that vary in autonomous selfing ability and either timing of selfing, flowering time, or attractive traits placed under different pollination conditions. In addition, we might predict that high selfing can more readily evolve in species where genetic correlations tie selfing ability to pollinator-avoidance traits along the axis of selection. We further envision a modeling framework that accounts for reciprocal dynamics of the plant–pollinator mutualism to help identify when mutualism breakdown, and thus the evolution of complete selfing, should occur. For example, models of mating system evolution could explicitly consider the cost-to-benefit ratio of participation in the mutualism for both plants and pollinators, plant and pollinator abundance, and the joint evolution of plant and pollinator traits (e.g., Holland and DeAngelis, 2010; Lepers et al., 2014). Ultimately, we encourage greater discussion about the importance of pollination biology in constraining plant mating-system evolution, also emphasized by others (e.g., Johnston et al., 2009; Devaux et al., 2014). We advocate looking beyond outcross pollen limitation and considering conditions where we might otherwise expect the automatic transmission advantage to favor the evolution of complete selfing. The authors thank M. O. Johnston, C. Devaux, and E. Porcher for helpful discussions and P. Diggle and three anonymous reviewers for valuable feedback on an earlier version of this perspective." @default.
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• W2770299250 title "Persistent pollinators and the evolution of complete selfing" @default.
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