Review
Plant mating systems in a changing world

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There is increasing evidence that human disturbance can negatively impact plant–pollinator interactions such as outcross pollination. We present a meta-analysis of 22 studies involving 27 plant species showing a significant reduction in the proportion of seeds outcrossed in response to anthropogenic habitat modifications. We discuss the evolutionary consequences of disturbance on plant mating systems, and in particular whether reproductive assurance through selfing effectively compensates for reduced outcrossing. The extent to which disturbance reduces pollinator versus mate availability could generate diverse selective forces on reproductive traits. Investigating how anthropogenic change influences plant mating will lead to new opportunities for better understanding of how mating systems evolve, as well as of the ecological and evolutionary consequences of human activities and how to mitigate them.

Section snippets

Human activities influence plant-pollinator interactions

Human activities have dramatically altered natural habitats in myriad ways with potentially significant consequences for plant and animal inhabitants. Although anthropogenic change has caused much concern regarding the fate of biodiversity, human perturbations have also provided opportunities for scientists to study ecology and evolution in action. In some cases, these unplanned experiments have been exploited to gain a better understanding of fundamental problems in ecology and evolution,

Evidence that human disturbance reduces outcrossing in plant populations

We exhaustively searched the literature for studies that compare the proportion of seeds outcrossed (t), as estimated from marker gene analysis, between populations in disturbed and relatively undisturbed habitats. We found 22 studies representing 27 species and 11 families (Table 1, Figure 1). Overall, t is significantly lower in disturbed habitats (paired t-test, P < 0.0001) and sometimes substantially lower 22, 23. We would expect the effect of disturbance on t to be more pronounced among the

Anticipating mating system evolution in human-disturbed habitats

The reductions in outcrossing in disturbed habitat illustrated in Figure 1 most likely represent short-term responses by populations to changes in pollination environment rather than evolved changes in the mating system. However, chronic outcross pollen limitation in disturbed habitats selects for selfing as a means of reproductive assurance 33, 34, 35 but the evolutionary consequences of anthropogenic effects on plant mating systems has rarely been considered. Outcross pollen limitation (PLx)

Anthropogenic pollen limitation might yield diverse outcomes for mating system evolution

The evolutionary response of plant populations to anthropogenic PL is likely to depend on the extent to which PL is caused by reduced pollinator visitation versus reduced number or density of conspecific pollen donors (mates). These two situations can occur independently 50, 51, 52 but will often co-occur because pollinators are attracted to higher flowering plant density 25, 53 and habitat perturbation can diminish both flowering plant density and pollinator populations. The contribution of

Conclusions

We have argued that many of the ways in which humans disturb natural habitats are likely to disrupt plant–pollinator interactions, with consequent outcross pollen limitation, and that the ecological context of anthropogenic PL can generate diverse selective forces on plant mating systems. In many cases, we expect an evolutionary shift towards higher frequencies of self-fertilization, although the selective forces and traits involved are likely to vary with the nature of the disturbance. There

Acknowledgments

We thank the National Evolutionary Synthesis Center (NESCent) for supporting the “Understanding the Paradox of Mixed Mating Systems” working group from which this paper emerged; Jon Auman, Karen Henry, Hilmar Lapp and Jeff Sturkey at NESCent for logistic support; Paula Jean Tonsor for the pollination treatment artwork (Box 1); Joe Hereford for enjoyable discussions; Mark van Kleunen for comments on the manuscript; the United States National Science Foundation for grants to SK NSF DEB 0324764;

Glossary

Autofertility (AF)
capacity of a plant to produce seed by spontaneous (autonomous) self-pollination when isolated from pollinators, usually measured by caging
Autogamy (a)
transfer of self pollen between anthers and stigmas within the same flower
Autonomous autogamy
spontaneous self-pollination without pollinator activity caused by close proximity of dehiscing anthers and receptive stigmas
Competing or simultaneous selfing (c)
occurs during the time when outcrossing also occurs
Delayed selfing (d)

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