Trends in Ecology & Evolution
ReviewPlant mating systems in a changing world
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)
References (83)
- et al.
Biological invasions as disruptors of plant reproductive mutualisms
Trends Ecol. Evol.
(2006) Do alien plant invasions really affect pollination success in native plant species?
Biol Conserv.
(2007)Interactive effects of habitat modification and species invasion on native species decline
Trends Ecol. Evol.
(2007)- et al.
A comparative analysis of pollen limitation in flowering plants
Biol. J. Linn. Soc.
(2000) Erratic pollination, high selfing levels and their correlates and consequences in an altitudinally widespread above-tree-line species in the high Andes of Chile
Acta Oecol.
(2006)Extensions of models for the estimation of mating systems using n independent loci
Heredity
(2002)Pollination biology and the evolution of mating systems in flowering plants
Evol. Biol.
(1996)Plant reproductive susceptibility to habitat fragmentation: review and synthesis through a meta-analysis
Ecol. Lett.
(2006)- et al.
Flower performance in human-altered habitats
Complex responses within a desert bee guild (Hymenoptera: Apiformes) to urban habitat fragmentation
Ecol. Appl.
(2006)
The effects of forest fragmentation on bee communities in tropical countryside
J. Appl. Ecol.
The interplay of pollinator diversity, pollination services and landscape change
J. Appl. Ecol.
Global warming and the disruption of plant–pollinator interactions
Ecol. Lett.
How does climate warming affect plant-pollinator interactions?
Ecol Lett.
Genetic consequences of habitat fragmentation in plant populations: susceptible signals in plant traits and methodological approaches
Mol. Ecol.
Allee effect and self-fertilization in hermaphrodites: reproductive assurance in demographically stable populations
Evolution
Is self-fertilization a dead end? Revisiting an old hypothesis with genetic theories and a macroevolutionary approach
Am. J. Bot.
Genetic constraints on floral evolution: a review and evaluation of patterns
Heredity
Evolutionary analysis of a key floral trait in Aquilegia canadensis (Ranunculaceae): genetic variation in herkogamy and its effect on the mating system
Evolution
The evolutionary enigma of mixed mating systems in plants: occurrence, theoretical explanations, and empirical evidence
Annu. Rev. Ecol. Evol. Syst.
Reproductive assurance and the evolution of uniparental reproduction in flowering plants
Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands
Science
Interspecific pollen transfer: magnitude, prevalence and consequences for plant fitness
Crit. Rev. Plant Sci.
Genetic resource impacts of habitat loss and degradation: reconciling empirical evidence and predicted theory for neotropical trees
Heredity
To self, or not to self…A review of outcrossing and pollen-mediated gene flow in neotropical trees
Heredity
Genetic diversity and outcrossing rate between undisturbed and selectively logged forests of Shorea curtisii (Dipterocarpaceae) using microsatellite DNA analysis
Int. J. Plant Sci.
Pollination processes and the Allee effect in highly fragmented populations: consequences for the mating system in urban environments
New Phytol.
Reproductive biology of the dry forest tree Enterolobium cyclocarpum (Guanacaste) in Costa Rica: a comparison between trees left in pastures and trees in continuous forest
Am. J. Bot.
Effects of forest fragmentation and flowering phenology on the reproductive success and mating patterns of the tropical dry forest tree Pachira quinata
Conserv. Biol.
Effects of dry tropical forest fragmentation on the reproductive success and genetic structure of the tree Samanea saman
Conserv. Biol.
Effects of forest fragmentation on pollinator activity and consequences for plant reproductive success and mating patterns in bat-pollinated bombacaceous trees
Biotropica
Plant mating systems and assessing population persistence in fragmented landscapes
Aust. J. Bot.
Genetic differentiation in isolated populations of Hakea carinata (Proteaceae)
Aust. J. Bot.
Impacts of forest fragmentation on the mating system and genetic diversity of white spruce (Picea glauca) at the landscape level
Heredity
Self- and cross-fertilization in plants. II. The selection of self-fertilization
Int. J. Plant Sci.
Self-fertilization and the escape from pollen limitation in variable pollination environments
Evolution
Plant population dynamics, pollinator foraging, and the selection of self-fertilization
Am. Nat.
A quantitative synthesis of pollen supplementation experiments highlights the contribution of resource reallocation to estimates of pollen limitation
Am. J. Bot.
Pollen limitation meets resource allocation: towards a comprehensive methodology
New Phytol.
Expanding the limits of the pollen-limitation concept: effects of pollen quantity and quality
Ecology
Bateman's principle and plant reproduction: the role of pollen limitation in fruit and seed set
Bot. Rev.
Cited by (442)
A global synthesis of the patterns of genetic diversity in endangered and invasive plants
2024, Biological ConservationReproductive strategy of an invasive buzz-pollinated plant (Solanum rostratum)
2023, South African Journal of BotanySoybean dependence on biotic pollination decreases with latitude
2023, Agriculture, Ecosystems and EnvironmentCurrent management practices do not adequately safeguard endangered plant species in conservation collections
2023, Biological Conservation
- *
Authors indicated with an asterisk are listed in order of contribution; all others are listed alphabetically.