Ecology and Evolution of Plant Mating

R E V I E W S Ecologyand evolution of plant mating Spencer C.H. Barrett and Lawrence D. Harder exin flowering plants is Plants exhibit complex mating patterns the relative frequency of selfing complicated by three dis- because of their immobility, and outcrossingl. There are im- tinctive features of their hermaphroditism and reliance on vectors portant biological reasons why the S biology. First, being sessile, for pollen transfer. Research on plant evolution of selfing, in particular, plants require vectors to transfer mating attempts to determine who mates has attracted so much attention. male gametes (pollen) between with whom in plant populations and First, the effects of selfing and out- individuals. This reliance promotes how and why mating patterns become crossing on fitness through in- the evolution of diverse floral adap evolutionarily modified. Most theoretical breeding depression and heterosis tations associated with the particu- models of mating-system evolution have are well established2J. Second, the lar agents responsible for pollen focused on the fitness consequences frequency of outcrossing is the dispersal (animals, wind, water). of selfing and outcrossing, stimulating most important determinant of Animals are most commonly em- considerable empirical work on the population genetic structure, af- ployed as pollinators because ecology and genetics of inbreeding fecting both genetic diversity within their behavioural flexibility can depression. Less attention has been given populations and genetic differen- be manipulated by plant traits. to how the mechanics of pollen dispersal tiation among them4. Finally, the Second, most plants are hermaph- influence the transmission of self and acquisition of selfing profoundly in- rodite and so are capable of self- outcross gametes. Recent work on the fluences floral evolution, affecting ing, sometimes at the expense of relation between pollen dispersal and floral design and sexual resource outcrossing. Third, owing to the mating suggests that many features allocations. Each of these aspects modular construction of plants, of floral design traditionally interpreted of the biology of selfing and out- male and female gametes are pack- as anti-selfing mechanisms may function crossing has stimulated consider- aged in a bewildering array of to reduce the mating costs associated able theoretical and empirical structural and temporal combi- with large floral displays. work during the past decade. nations at the flower, inflorescence, Recognition of the significance plant or population level, despite of selfing for mating-system evolu- the basic hermaphroditic condi- Spencer Barrett is at the Dept of Botany, tion prompted development of tion. Because of vector-mediated University of Toronto, Toronto, Ontario, specific tools for measuring the Canada M5S 382; Lawrence Harder is at the relative frequency of selfing and gamete transfer and elaborate sex- Dept of Biological Sciences, University of Calgary, ual systems, plant mating can be Calgary, Alberta, Canada T2N lN4. outcrossing. Since Brown and highly promiscuous, with individ- Allard first demonstrated the util- uals mating with many sexual part- ity of allozyme markers to esti- ners including themselves. mate mating parameters 25 years Pollination is fundamental among the complex ecologi- ago, estimation of the proportion of offspring produced by cal interactions that generate mating patterns because it selfing, s, or its complement, the female outcrossing rate determines mating opportunities by establishing the dis- (t= 1 -s), has become routine for many botanists. It is impor- persion of pollen grains among flowers. Despite the obvious tant to recognize that s and [portray selfing and outcrossing functional link between pollination and mating, research on through female function and only depict the proportions of these basic aspects of plant reproduction has followed separ- successful gametes involved in selfing and outcrossing ate paths during most of this century, with surprisingly little when referring to a population average of all phenotypesQ. cross-fertilization. Most pollination studies have been eco- This approach has few parallels with work on animal mating logical, with little consideration of how patterns of pollen systems, probably because of the contrasting sexual sys- transport might influence mating and plant fitness. In con- tems (hermaphroditism versus dioecy) that predominate in trast, mating-system studies have been dominated by popu- the two groups. Notwithstanding this difference, many ani- lation genetic and theoretical approaches, paying scant mals do not appear to maintain sufficient allozyme variation attention to how the proximate ecological factors governing to enable quantitative analysis of mating parameters rel- pollen dispersal influence mating. In recent years, the iso- evant to their reproductive biology (e.g. incidence of extra- lation of pollination and mating-system biology has begun to pair copulations in ‘monogamous’ birds), hence the de- break down, with the publication of theoretical and empiri- velopment of alternative genetic markers, such as DNA cal studies emphasizing both the ecological aspects of plant fingerprinting techniques in behavioural ecology. Although mating and the fitness consequences of different mating pat- such techniques are also likely to provide powerful new terns. Here, we review some of these recent developments insights into aspects of plant mating, particularly concern- to illustrate why, following Darwin’s early lead, plant mating ing male reproductive success, allozymes continue to be the continues to be one of the most active fields of enquiry in eve main source of genetic markers for analysing selfing. lutionary biology. These developments involve advances in Two types of data are required to describe accurately determining the proximate mechanisms governing mating, the mating system of a plant population: (1) measures of fer- measuring mating complexity, and understanding the genetic tility, and (2) estimates of the kinds of mating events that and evolutionary consequences of different mating strategies. occurs. Fertility involves the relative contribution of individuals to the next generation through male and female gametes. The incidence of selfing and outcrossing and their Mating events are usually classified according to whether measurement seeds originate from outcrossing, selfing or apomixis. Among In contrast to its zoological counterpart, the study of outcrossed progeny, it is also possible to estimate the de plant mating systems has been dominated by comparison of gree of biparental inbreeding, how often progeny are full TREE vol. II, no. 2 February 1996 0 1996, Elsevier Science Ltd 73 R E V I E W S sibs, and the number of male parents represented in a seed cropg. Despite rapid progress in the use of genetic markers, Box 1. The evolution of plant mating systems it is worth noting that we are still some way from being able Fisher11 demonstrated that, all else being equal, a gene causing self- to determine for any plant population the basic mating in- fertilization will increase in frequency each generation, because, on formation of who has mated with whom and how often. DNA average, selfers contribute more gene copies to the next generation markers with high allelic variation, such as microsatellite than outcrossers: loci, seem to offer the best hope for achieving this goallo. Average gene contribution Ecology and evolution of selfing Outcrosser Selfer The fundamental issues involved in the evolution of selfing were elegantly identified in Fisher’s early treatment” of Ovule parent 1 1 Pollen parent 1 2a the transmission advantage of a selfing gene. His work pro- Total 2 3b vided the basic insight into why most later genetic models of mating-system evolution predict that selfing will be un- %ontribution diminished by pollen discounting. conditionally favoured if selfed progeny have at least half bcontribution diminished by inbreeding depression. the fitness of outcrossed progeny (Box 1). Several aspects This three to two average bias in gamete transmission, which arises of plant reproduction oppose this siring advantage of self- because a selfer sires its own seeds and seeds on outcrossers, has pollination, either by reducing it directly through pollen dis- been termed the automatic selection advantage of self-fertilization. counting or through inequalities in the fates of selfed and Not all plants self, indicating that strong forces operate to prevent outcrossed progeny resulting from inbreeding depression the spread of selfing genes. Fisher’s argument requires that selfing and outcrossing involve distinctly separate pools of pollen. In contrast, (Box 1). The most thoroughly studied selective force main- when pollen involved in selfing diminishes the pool available for out- taining outcrossing is substantial inbreeding depression in crossing (pollen discounting), a selfer’s siring advantage is reduced selfed progeny, which arises largely from the expression of proportionately. Holsinger*’ demonstrated theoretically that pollen dis- recessive deleterious alleles in homozygous indivlduaW. counting alone is sufficient to explain both why selfing does not always evolve, and the occurrence of mating systems that include a mixture of The evolution of selfing should generally be accompanied selling and outcrossing. The few empirical studies of pollen discount- by changes in the incidence and intensity of factors oppos- ing suggest that its

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