Self- and Cross-Fertilization in Plants. I. Functional Dimensions Author(s): David G. Lloyd and Daniel J. Schoen Source: International Journal of Plant Sciences, Vol. 153, No. 3, Part 1 (Sep., 1992), pp. 358- 369 Published by: The University of Chicago Press Stable URL: http://www.jstor.org/stable/2995676 . Accessed: 18/02/2014 15:23 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp . JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. The University of Chicago Press is collaborating with JSTOR to digitize, preserve and extend access to International Journal of Plant Sciences. http://www.jstor.org This content downloaded from 131.212.205.195 on Tue, 18 Feb 2014 15:23:21 PM All use subject to JSTOR Terms and Conditions Int. J. Plant Sci. 153(3):358-369. 1992. ? 1992 by The University of Chicago.All rightsreserved. 1058-5893/92/5303-0010$02.00 SELF-AND CROSS-FERTILIZATION IN PLANTS. 1. FUNCTIONALDIMENSIONS DAVID G. LLOYD AND DANIEL J. SCHOEN Plant and MicrobialSciences, University of Canterbury,Private Bag, Christchurch,New Zealand; and Biology Department,McGill University, Montreal,Quebec H3A IBI, Canada Many functional-ecological, morphological,and physiological-factors affect the occurrenceof self- fertilization.Six modes of self-pollinationare distinguished. These differin whetherthey utilize specialized flowers,whether they involve the transferof pollen within or between flowers,whether they are auton- omous or mediated by vectors, and their timing relative to opportunitiesfor outcrossing.The various modes of selfing are subject to differentstructural constraints. Prepotency, the preferentialsuccess of cross-pollenin achievingfertilizations when it competes with self-pollen,influences the frequencyof self- fertilizationin some species. The amount of self-fertilizationmay depend on environmentalconditions and the vector species visiting each flower and may vary among the flowers of one plant. To gain informationon the prevalenceof autonomous self-pollination,66 species for which the degreesof self- compatibilityand autofertility(seed set in isolation) have been published were surveyed. Partiallyself- incompatiblespecies (in which the seed set is lower after self-pollinationthan after separateoutcrosses) have on average lower autofertilitythan self-compatiblespecies (in which self- and cross-pollinations succeed equally well), but some partially self-incompatiblespecies have considerableautofertility and some self-compatiblespecies have none. A number of featuresof floral morphologyand phenologyare associatedwith high AutofertilityIndices. Introduction The functional approach to the study of self- The comparisonof self-and cross-fertilization and cross-fertilizationcontrasts with the genetic is the centraltopic of floralbiology. Following one in emphasizing the operation of pollination thediscovery by Knight(1799) and Darwin (1868, mechanisms and aspects of the naturalhistory of 1876)that cross-fertilization is advantageousbe- flowers.Functional studies of mating systems ex- causeit producessuperior progeny, there was a amine ecological, morphological,and physiolog- periodof intenseactivity in pollinationbiology ical perspectives. They have continued from the in the later decadesof the nineteenthcentury. last century to the present day with little change Flowerstructures that encouragecross-fertiliza- and currentlyconstitute a useful but ratherstatic tion and reduce self-fertilizationwere studied aspect of mating systems. In recent years, many widely.After considerable debate during this pe- topics of floral ecology have been rejuvenatedby riod, it was also acknowledgedthat some plants innovative studies of reproductive strategiesfor areadapted to regularself-fertilization and have deployingadaptive mechanisms,but the new par- floralsyndromes that contrast strongly with those adigm has had hardly any impact on the tradi- associatedwith outcrossing(see Darwin[1876] tional topic of cross- versus self-fertilization. andHenslow [1879] for divergent viewpoints and We believe that functional aspects of self-fer- Miuller's[1883] brilliant resolution of the issue). tilization have been underemphasizedand offer Floralbiology became popular again in the sec- unrealized opportunities to increase our knowl- ond halfof the twentiethcentury. In this period, edge of the evolution and selection of mating sys- geneticstudies have dominatedcomparisons of tems. A number of major functional factors, in- self- and cross-fertilization.The geneticstudies cludingprepotency, pollen discounting,the effects have provided much-neededempirical infor- of selfingon the outcrossed seed production,and mationon severalaspects of self- and cross-fer- reproductive assurance, remain entirely or al- tilization,including frequencies of self-fertiliza- most entirelyunstudied (Lloyd 1992; Schoen and tion(Barrett and Eckert 1990), the expression and Lloyd 1992). Moreover, self-pollination is not a causesof inbreedingdepression (Charlesworth and single unvaryingprocess that occurs in the same Charlesworth1987; Barrettand Charlesworth manner in all species that practice any selfing 1991),and the geneticstructures of outcrossing (Lloyd 1979). On the contrary, self-pollination and selfingpopulations (Brown 1990; Hamrick occurs in several fundamentally different ways, and Godt 1990;Ritland 1990). The theoretical which we describe as the "modes" of self-polli- effectsof the matingsystem on the geneticstruc- nation. There have been few attempts to deter- turesof regularlyselfing and outcrossingpopu- mine their relativefrequencies experimentally. In lations have also been analyzedwidely (Brown addition, a number of operational factors can 1990;Ritland 1990). cause the amount of self-fertilization to vary within a population, including environmental Manuscriptreceived March 1992; revisedmanuscript received conditions and differentpollinator species; these May 1992. too have rarelybeen examined. 358 This content downloaded from 131.212.205.195 on Tue, 18 Feb 2014 15:23:21 PM All use subject to JSTOR Terms and Conditions LLOYD & SCHOEN-FUNCTIONAL DIMENSIONS OF SELF- AND CROSS-FERTILIZATION 359 In this and the following articles we examine erties of cross-fertilizationand the genetic prop- these major functional dimensions of self- and erties of self-fertilization.The distinctive nature cross-fertilizationand attempt to integratethem of geitonogamyhas led to its being the only mode with genetic approachesto the subject. This ar- of chasmogamous selfing that was distinguished ticle introduces functional aspects of self- and traditionally(Kemer 1895). A certain amount of cross-fertilizationby describingthe variousmodes geitonogamy is virtually inevitable in self-com- by which selfing occurs and the ecological, mor- patible plants that produce a number of flowers phological, and physiological factors that influ- at anthesis at the same time. Geitonogamy is ence their frequencies.It also reviews published probablythe most widespread mode of self-pol- work on spontaneousself-pollination to examine lination, but it may never achieve the predomi- functional factors that contribute to variation in nance that the autonomous modes acquirein ha- the frequency of self-fertilization. The two fol- bitually selfing species. It would be even more lowing articlespresent a phenotypic model of the important but for the fortunate and still largely selection of self-fertilization(Lloyd 1992) and de- unexplained habit shared by virtually all flower scribe and illustrateexperimental procedures for visitors of visiting only a fractionof the available estimating the selective forces and partitioning flowerson a plant before moving to the next plant the full complement of self-fertilizationinto its (Frankieet al. 1976; Kadmon and Shmida 1992; component modes (Schoen and Lloyd 1992). Robertson 1992). Charles Darwin (1859, 1876) recognized the Modesof self-pollination importanceof geitonogamy when he arguedthat trees are likely to be self-pollinated more fre- CLEISTOGAMY quently than other plants because they display In morphologicalterms, the most distinctmode more flowersat one time. Darwin postulatedthat of selfingis cleistogamy(Kuhn 1867; Lord 1981), this could explain the higher frequencyof species which occurs in closed flowers that are structur- with separatesexes among the trees of the United ally specialized for self-fertilizationand do not Kingdom, New Zealand, and the United States outcross.Cleistogamy differs from all othermodes (but not Australia) than among other plants of of selfing in several respects. It is the only mode the same regions. A century later, Arroyo (1976) that occurs in morphologically distinct flowers. proposedthat the occurrenceof geitonogamymay Hence, it can be recognized immediately and its be an important factor in the selection of self- frequencycan be measured simply by counting incompatibility as well as separate sexes. the numbers of cleistogamously and chasmoga- A few recent studies have examined the rela- mously produced seeds. Morever, cleistogamy is tionship between the frequency of geitonogamy uniqueamong modes of selfing(Schoen and Lloyd and flower number that