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Maternal Investment and Male Reproductive Success in Angiosperms

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Maternal Investment and Male Reproductive Success in Angiosperms Biological Society of the Linnean Society (1987), 30: 115-133 Maternal investment and male reproductive success in angiosperms: parent-offspring Downloaded from https://academic.oup.com/biolinnean/article/30/2/115/2676958 by guest on 27 September 2021 conflict or sexual selection? SUSAN J. MAZER Department of Botany, University of Calzfornia, Davis, California 95616, U.S.A. Received 31 January 1986, accepted for publication 22 October 1986 It is possible to interpret components of seed development in angiosperms from the perspective of parent-offspring conflict (a special case of kin selection) or sexual selection. Available parent- offspring conflict models predict the evolution of traits determining the outcome of competition among related individuals soliciting maternal resources. In such models, ‘selfishness’ may spread even if it reduces female fecundity and thus population mean fitness may decline. These models are limited, however, because most of them do not simultaneously consider selection among maternal genotypes varying in the tendency to respond to their offspring. Available sexual selection models, in contrast, do consider the joint evolution of polygenic male traits (influencing viability, mating success and fecundity) and female preferences (influencing the mating success of different male phenotypes). These models have shown that male traits may evolve that are non-optimal with respect to viability. Only one recent sexual selection model explicitly incorporates direct fecundity selection upon females; this model concludes that fecundity will be maximized at equilibrium. Hence population mean fitness may decline due to reduced male viability but not due to diminished female fecundity. Available sexual selection models, however, are limited because they do not consider the effects of interactions among relatives. The assumptions and qualitative results of the two types of models are compared and discussed in the context of seed development. Differential allocation of maternal resources among genetically distinct developing seeds may be viewed from the perspective of either. Because the results of the available models of parent-offspring conflict and sexual selection are not wholly consistent and because data confirming the genetic basis of maternal patterns of investment or differential male reproductive success are scant, it is not clear which set of conclusions is most appropriate to apply to plants. To achieve the generality towards which mathematical approaches aspire, new models concerning the evolution of traits influencing resource allocation in plants must incorporate the components of both parent-offspring conflict and sexual selection. KEY WORDS:-Gametophytic competition ~ kin selection - parent-ffspring conflict - parental investment - resource allocation - sexual selection. CONTENTS Introduction .................. 116 Parent-offspring conflict and sexual selection: two views of male reproductive success . 116 Conflict ofinterest among interacting individuals ......... 120 Criteria for parent-offspring conflict in plants ........... 121 Identification of maternal countermeasures in plants ......... 122 Identification of resource-garnering ability ........... 123 Selection on maternal investment and resource-garnering ability: components of fitness . 124 Fecundity selection ................ 124 Viability selection ................ 125 I15 0024-4066/87/020115 + 19 SOS.OO/O 0 1987 The Linnean Society of London 116 S. J. MAZER The joint evolution of discrimination and RGA .......... 125 Selfishness us. countermeasures or male competition us. female choice? ..... 126 Discussion: The evolution of resource-garnering ability- analogy to sexual selection. .............. 128 Acknowledgements ................. 130 References. ................... 130 INTRODUCTION Animal behaviourists, plant ecologists and theorists have argued that resource Downloaded from https://academic.oup.com/biolinnean/article/30/2/115/2676958 by guest on 27 September 2021 limitation in natural populations has led to inter-sibling and parent-offspring conflict over maternal resources when there is a genetic ‘conflict of interest’ relating to resource allocation (Trivers, 1974; Charnov, 1979; Westoby & Rice, 1982; Queller, 1983; Willson & Burley, 1983; Law & Cannings, 1984). With respect to plants, Willson & Burley (1983) note that some components of seed development (e.g. the likelihood of ovule fertilization or abortion, or seed size achieved) may be interpreted as manifestations of parent-offspring conflict and/or sexual selection (see also Janzen, 1977; Charnov, 1979, 1983; Stephenson & Bertin, 1984; Willson & Burley, 1983). The primary objective of this paper is to illustrate that neither approach as thus far developed provides a satisfying model for the evolution of these traits in plants. The evolution of traits influencing resource allocation to and resource acquisition by developing seeds may legitimately be modelled using a parent-offspring conflict or sexual selection approach. Law & Cannings ( 1984) offer a parent-offspring model for the evolution of ‘over-consumer’ alleles expressed in developing seeds. At present, however, there are no models available which treat selective events occurring during seed development as sexual selection among competing males. This bias is probably due to the traditional view that sexual selection occurs prior to fertilization. This view is justified for animals, in which the most obvious episodes of male-male combat and female choice occur before mating. In plants, however, opportunities for male competition and female choice exist from the time of pollen dispersal until seed dehiscence. Surprisingly, the conclusions of the parent-offspring conflict models applied to animals and plants are at variance with those of the sexual selection models applying to animals (see Table 1). The contradictions appear to be due to differences in the assumptions of and methods employed in each type of model. The purpose of this paper is thus twofold: first, to discuss specific traits of developing seeds in the context of parent-offspring conflict and sexual selection, and second, to explore with respect to plants, the assumptions, results and limitations of the available models of these processes. PARENT-OFFSPRING CONFLICT AND SEXUAL SELECTION: TWO VIEWS OF MALE REPRODUCTIVE SUCCESS Animal behaviourists interested in parental investment have developed population genetic models of traits influencing the solicitation and allocation of resources among interacting related individuals-the parent-offspring conflict models (Charlesworth, 1978; MacNair & Parker, 1978, 1979; Parker & MacNair, 1978, 1979; Stamps, Metcalf & Krishnan, 1978; Metcalf & Stamps, 1979; Stamps & Metcalf, 1980). Zoologists interested in the consequences’ of variance in male reproductive success have built models of sexual selection PARENT-OFFSPRING CONFLICT/SEXUAL SELECTION IN PLANTS 117 (Darwin, 1859, 1871; Fisher, 1930; O’Donald, 1962, 1967, 1973, 1977, 1980; Charnov, 1979; Lande, 1981 ; Kirkpatrick, 1982, 1985; Bateson, 1983). Sexual selection models predict the evolution of traits influencing male reproductive success through intra-sexual competition and female choice. They have shown that autosomal male-limited traits may evolve when a strong female preference for them exists even if these traits cause reduced viability. One model (Kirkpatrick, 1985) has shown that maternal fecundity will be maximized at equilibrium even when female preferences exist for males which lower the Downloaded from https://academic.oup.com/biolinnean/article/30/2/115/2676958 by guest on 27 September 2021 fecundity of the matings in which they participate. In contrast, parent-offspring conflict models have shown that, under some conditions, paternally derived alleles for ‘selfishness’ may spread when rare even if they do reduce the fecundity of individuals bearing selfish offspring (Blick, 1977; MacNair & Parker, 1978, 1979; Law & Cannings, 1984). It seems that the geneticists employing these two approaches have effectively worked in isolation without concern for the fact that they are modelling related phenomena. The similarities between the two approaches become especially apparent when one considers the features of maternal investment in plants. Questions concerning the allocation of maternal resources among simultaneously developing seeds may be couched in terms of parent-offspring conflict or in terms of sexual selection among competing pollen donors. As mentioned above, there is one element of the process of sexual selection as described by Darwin for animals (1859, 1871; see also Fisher, 1930) which might be modified in its application to plants. Male plants (or their gametophytes: pollen grains) may compete merely for access to females (i.e. stigmas), but many of the events affecting male reproductive success in plants may occur afh pollination or fertilization (Stephenson & Bertin, 1984; Bawa & Webb, 1984). Seed-bearing individuals may effectively determine their mates by discriminating among genetically distinct pollen grains, pollen tubes or fertilized ovules. This is not ‘female choice’ as defined by Darwin; these selective processes involve discrimination among male gametes or sired ovules, not among parental diploid genotypes. The inclusion of post-fertilization selection as a component of sexual selection is a controversial proposal. One might insist that all post-zygotic selection be considered as viability selection (or natural selection), distinct
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