Incompatibility and pollen competition in Alnus glutinosa: Evidence from pollination experiments

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  • Genetica 105: 259271, 1999. 2000 Kluwer Academic Publishers. Printed in the Netherlands. 259

    Incompatibility and pollen competition in Alnus glutinosa: Evidence frompollination experiments

    Wilfried Steiner & Hans-Rolf GregoriusInstitut fr Forstgenetik und Forstpflanzenzchtung, Universitt Gttingen, Bsgenweg 2, D-37077 Gttingen,Fed. Rep. Germany; Author for correspondence: (Fax: +49 / 551 / 398367;E-mail: gregorius@ufogen.uni-forst.gwdg.de)Received 1 March 1998 Accepted 6 August 1998

    Key words: Alnus glutinosa, incompatibility, pollen competition, pollination experiments

    Abstract

    Different types of incompatibility systems were found to operate simultaneously in Alnus glutinosa in the courseof numerous pollination experiments, including self-pollination and pollination with controlled pollen mixtures.Isozyme genetic markers were used to identify the pollen parent of each offspring from the mixed pollinationexperiments, thus allowing specification of the fertilization success of each pollen parent. In a first step, theseresults were compared with observations on in vitro pollen germination experiments. This comparison allowsfor exploration of the explanatory value of different germination media as models of germination conditions onstigmas. In most cases, the data suggest that the in vitro germination conditions resemble the fertilization conditionsin vivo, at least in the sense that they favor the same pollen parents. By providing a generic and operable definitionof the two basic types of incompatibility, eliminating (inability to fertilize ovules) and cryptic (resulting in loweredfertilization success of a pollen parent under competition), evidence was detected for the existence of both typesof incompatibility in Alnus glutinosa, where eliminating incompatibility occurred as self-incompatibility only.However, since this incompatibility seems to act primarily via pollen elimination, seed production is not likely tobe negatively affected in natural populations, even for comparatively large amounts of self-pollination.

    Glossary

    Cryptic incompatibility of a pollen parent; a pollenparent being opposed (see entry opposition) by somebut not by all ovule parents.Cryptic pollen deficiency of a pollen parent; a pollenparent being opposed (see entry opposition) by allovule parents.Cryptic self-fertility of a plant; self-pollen applied tostigmas under exclusion of cross-pollen inhibits fer-tilization, whereas a mixture of self- and cross-pollenresults in the formation of some progeny from self-fertilization.Eliminating incompatibility of a pollen parent; infer-tility with some but not with other ovule parents.Infertility of a pollen parent with the ovules of anovule parent; the proportion of unfertilized ovules in-creases with the share of the pollen parent among allpollen pollinating the ovule parent.

    Interference of two pollen types; the performance(germination and growth) of one pollen type is af-fected by the presence of the other; interference cantake place uni- and bilaterally.Opposition of an ovule parent to a pollen parent;the relative success of a pollen parent in fertilizing theovules of a plant is below average in competition withpollen from other plants.Pollen deficiency of a pollen parent; infertility of thepollen parent with all ovule parents.

    Introduction

    Generative reproduction in plants allows for variableforms of selection during the phase from the formationof gametes to their fusion in zygotes and the initialstages of seed development. Although this reproduc-tive phase normally covers only a comparatively small

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    portion of an organisms total life span, its overallselective potential may be considerable. Especially inlong-lived, highly iteroparous organisms like trees, itmay even exceed the potential for selection during theextensive vegetative phase.

    Effects of selection on mating processes (selectivemating) have long been discussed in the populationgenetics literature. They include aspects such as dif-ferential intensity and asynchrony of flowering as asource of differential mating participation and mat-ing preferences, segregation distortion as implied byselection during gamete formation, gametophytic se-lection, and early postzygotic incompatibility or se-lective embryo abortion. In fact, even the specificallycombinational effects of mating that appear, for ex-ample, in various prezygotic incompatibility relations,present themselves as a result of selection processesamong the potential mating partners of an individualor group of individuals. Differential mating successamong the potential mating partners defines the mat-ing preferences of the individual or group (Gregorius,1989). By combining a multitude of different formsand intensities of selection, the generative phase ofreproduction thus establishes a complex system ofselection mechanisms.

    The results on mating system characteristics of Al-nus glutinosa reported in the following highlight malegametophytic selection caused by pollen competitionfor fertilization. Pollen competition is understood hereas all aspects involved in the striving of pollen to fer-tilize the same ovule. Different factors may contributeto this kind of selection. (i) Pollen vigor basically de-termines the capacity of an individual pollen grain togerminate, grow, and fertilize; physiological consti-tution and genetic characteristics of the pollen or itsproducer may affect this capacity (see e.g., Mulcahy,Muleahy & Ottaviano, 1986, chapter on Gene ex-pression in pollen). Here, the conditions for selectionare shaped over the whole reproductive process fromthe beginning of gametophyte formation to the finalfertilization event, and these conditions strongly influ-ence the mating (fertilization) success of the differentpollen types.

    After pollination of the female flowers, (ii) femalemate choice, sexual selection, and prezygotic incom-patibility mechanisms become relevant. Interactionbetween female flower and pollen can lead to selectionamong the pollen present on a stigma. Especially incombination with incompatibility phenomena, femalerecognition and rejection processes are well known(for reviews, see de Nettancourt, 1977; McCubbin &

    Kao, 1996). Further selection conditions arise from(iii) malemale interactions in the sense of pollen in-terference (for example, via allelopathic substances).Several investigations have demonstrated that neigh-boring pollen on a stigma or pollen tubes in a style canmore or less directly influence each others germina-tion or pollen tube growth, thus resulting in selection(Marshall et al., 1996; Kanchan & Jayachandra, 1980;Murphy & Aarssen, 1989). Since these three factorsdo not act in isolation from each other, they are verydifficult to distinguish experimentally.

    Alnus glutinosa is monoecious and predominantlywind-pollinated. The female and male inflorescencesare well separated. Only in very rare cases couldinflorescences with male flowers at the bottom andfemale flowers at the top of the same inflorescencesbe observed. As the vast majority of inflorescenceson every tree do not comprise flowers of both sexualtypes, such combinations of sexes in one inflorescencecan be considered as malformations. No such inflores-cences were used in our experiments. The existence ofa self-incompatibility system in this species seems tobe likely despite some conflicting reports in the liter-ature (Johnsson, 1951; Weiss, 1964; Hagman, 1970,1975 report self-incompatibility in contrast to Heit-mller, 1957; Rohmeder & Schnbach, 1959 [p. 71];Holzer, 1961; Weisgerber, 1974). The repeated occur-rence of self-incompatibility hints at the existence ofa genetic mechanism that enables the species to se-lectively discriminate between self- and cross-pollen.Such mechanisms, however, may (probably to a lesserextent) also imply the possibility of selective fertiliza-tion among cross-pollen that differs in specific charac-teristics, thus defining more complex incompatibilityrelations.

    The present experimental approach is intended tocontribute to the clarification of these conflicting re-ports and to enable a more detailed analysis of theproblem of incompatibility in Alnus glutinosa. Takingthe possibility of (cryptic) incompatibility relationsshowing under pollen competition only into account,the majority of the pollination experiments are com-posed of pollen mixtures consisting of defined propor-tions of two pollen parents. The two pollen parents andthe ovule parent are chosen on the basis of isozymegenotypes that allow identification of the pollen par-ent of each offspring from the pollination experiment(the principle of this method goes back to Bateman,1956). Particular attention is given to an unambigu-ous and operational formulation of the basic types ofincompatibility relations in order to allow detection

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    of variants of incompatibility and of fertilization re-lations that do not fit into the common concepts ofincompatibility (for convenience, the relevant termsare compiled in a brief glossary at the end of thepaper).

    Materials and methods

    Tree material

    All pollination experiments were carried out on treesgrowing in two seed orchards (Jungviehweide andGahrenberg) of the Hessian Forest Research Institu-tion. All pollen parents except one were also chosenamong the seed orchard trees. The only exception isa planted roadside tree (ATW2) of unknown originand age. All seed orchard trees are named with theirofficial numbers consisting of clone name and rametnumber. As literature reports, the general possibilityof misclassification in seed orchards, different rametsof the same clone were treated as separate trees inour experiments. Neither pollen samples nor seed lotsfrom different ramets of the same clone were mixed,although electrophoretic data from isozymes were inaccordance with the

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