Evolution and Ecology of Plant Mating Systems

Abstract

The mating system provides a description of the distribution of mating unions in a population; in hermaphrodites, such as most flowering plants, this amounts to the rate of self‐fertilisation versus outcrossing. Selfing has evolved numerous times in flowering plants, probably because selfers transmit an extra copy of their genes to their seed progenies and/or because they can reproduce in the absence of mates. Nevertheless, selfed progenies tend to be less fit, and selfing detracts from an individual's outcrossing potential. As a result, most plants avoid selfing via a number of physiological, morphological or phenological adaptations. The mating system also has important implications for the genetic structure of individuals and populations: selfing individuals show reduced heterozygosity, reduced effective recombination and reduced effects of genetic conflict and populations of selfers tend to be more genetically differentiated from one another than do those of outcrossers.

Key Concepts

  • The mating system describes and quantifies the distribution of mating unions in a population; in hermaphroditic plants, the mating system typically refers to the selfing or outcrossing rates.
  • Self‐fertilisation confers an automatic selective benefit because selfed progenies carry two copies of a parent's genome rather than just one. An important possible cost of self‐fertilisation is inbreeding depression, where selfed progenies have lower fitness than their outcrossed counterparts.
  • Self‐fertilisation can be costly because pollen used up in selfing is unavailable for competition to sire outcrossed progenies; this is known as pollen discounting. Similarly, self‐fertilised ovules are unavailable for outcrossing (seed discounting), also constituting a cost.
  • Self‐fertilisation may be advantageous when mates or pollinators are scarce because it provides reproductive assurance by allowing uniparental reproduction.
  • Inbreeding depression can be caused by either overdominance, where heterozygotes have an advantage over both corresponding homozygotes, or partial dominance, where fitness is reduced on one homozygote by the expression of deleterious recessive alleles.
  • Plants avoid self‐fertilisation through physiological self‐incompatibility reactions, the spatial separation of the sexual functions within and/or among flowers (herkogamy or dicliny) or the temporal separation of the sexual functions (dichogamy).

Keywords: self‐fertilisation; inbreeding depression; recombination; self‐incompatibility; flowering plants; hermaphrodite; siring success; dioecy; floral morphology

Figure 1. The evolutionary geneticist and statistician, Ronald Fisher (a), first saw that a mutation increasing the selfing rate in an otherwise outcrossing hermaphrodite population would enjoy an automatic fitness advantage because selfers would transmit two copies of its genes to the next generation through their selfed seeds, whereas outcrossing individuals would only transmit a single copy (b). Fisher's simple analysis assumes that selfed and outcrossed seeds have equal fitness and that selfing individuals continue to transmit genes by outcrossing through their pollen.
Figure 2. A diagram from Charles Darwin's book ‘The Effects of Cross‐ and Self‐fertilization in the Vegetable Kingdom’, published in 1876. The diagram shows the average heights of selfed and outcrossed progenies of the plant Ipomaea purpurea over 10 generations. The shorter height of selfed plants indicates inbreeding depression. Darwin concluded from his numerous experiments that ‘plants abhor perpetual self‐fertilisation’. Reproduced from Darwin 1876.
Figure 3. The evolution of selfing is typically followed by the evolution of reduced flower size. The flowers of the highly selfing species Capsella rubella (a) are much smaller than those of its near relative C. grandiflora (b). Within the highly variable Californian dune species Camissonia cheiranthifolia (c), flower size likely varies positively with the outcrossing rate. (a, b) Photos courtesy of T. Slotte, (c) Courtesy of C.G. Eckert.
Figure 4. The flowers of the aquatic perennial herb Sagittaria latifolia are either male (top three open flowers in the inflorescence shown) or female (bottom three open flowers). Individuals in some populations (as in the image) are monoecious, with both male and female flowers on the same plant. Other populations are dioecious, with male and female flowers on different plants. Photo courtesy of M. Dorken.
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Further Reading

Barrett SCH (2002) The evolution of plant sexual diversity. Nature Reviews Genetics 3: 274–284.

Barton NH and Charlesworth B (1998) Why sex and recombination? Science 281: 1986–1990.

Charlesworth D (2006) Evolution of plant breeding systems. Current Biology 16: R726–R735.

Hiscock SJ and McInnis SM (2003) The diversity of self‐incompatibility systems in flowering plants. Plant Biology 5: 23–32.

Lloyd DG (1979) Some reproductive factors affecting the selection of self‐fertilization in plants. American Naturalist 113: 67–79.

Vogel S (1996) Christian Konrad Sprengel's theory of the flower: the cradle of floral ecology. In: Lloyd DG and Barrett SCH (eds) Floral Biology: Studies on Floral Evolution in Animal‐pollinated Plants, pp. 44–62. New York, NY: Chapman and Hall.

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Pannell, John R, and Voillemot, Marie(Jan 2017) Evolution and Ecology of Plant Mating Systems. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0021909.pub2]