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 from sexual selection. One consequence of post-fertilization selection among pollen genotypes, however, is variance in male reproductive success: the phenomenon in which geneticists modelling sexual selection are most interested. It is crucial to note that male fitness in plants (if defined as the number of offspring surviving to reproduce) is determined both by the number of fertilized ovules which are not aborted and by the relative size they attain (when seed size influences seedling survivorship). The latter is determined by the pattern of investment exhibited by maternal individuals: the phenomenon with which zoologists modelling parent-offspring conflict are most concerned. Since seed abortion is the most extreme manifestation of both poor maternal investment and mate choice, components of parent-offspring conflict and sexual selection in angiosperms are inextricably entwined. Below, I argue that the offspring characters that influence seed weight or quality due to their effects on maternal investment are identical to those traits which determine male reproductive success after fertilization. A conceptual link Table 1. Comparison of the methods and qualitative results of parent-offspring conflict and sexual selection population genetic models. The parent-offspring conflict models consistently show that population mean fitness may decline due to decreasing female fecundity as selfishness spreads. The sexual selection models diverge from this conclusion.

Evolution of traits Dynamic us. Means by which - Parent-offspring W conflict us. considered singly non-dynamic population fitness sexual selection Genetic model Evolving trait(s) or simultaneously Assumptions model may decline Author

Parent-offspring 1 locus/2 allele ‘Conflictor’ gens Only I trait Monogamy Nondynamic Reduced female Parker & conflict Search for expressed in offspring considered Interbrood competition fecundity as MacNair evolutionary increase solicitation of for maternal resources selfishness spreads (1978) stable strategy and acquisition of Siblings not affected at (ESS) maternal resourses random with respect to genotype Future full-sibs affected by offspring selfishness Parent-offspring 2 locusESS Offspring selfishness Singly Monogamy Non-dynamic Reduced female Stamps, d d., conflict Maternal Sequential production of fecundity (1978) countermeasures two offspring Solicitation costs considered Parent-offspring 1 locus/2allele ESS Conflictor genes Only 1 trait Polygamy Non-dynamic Reduced female MacNair & conflict considered Inter-brood competition fecundity Parker (1978) cn Future hallkibs affected Population mean 5 by offspring selfishness fitncss lower than z for monogamy & Parent-offspring I locus/2 allele ESS Offspring sdfishness Only 1 trait Monogamy Nondynamic Reduced female Metcalf & E conflict considered Simultaneous production fccundity Stamps (1979) of offspring Parent-offspring 1 locus/2 allele ESS Offspring selfishness only 1 trait Single and multiple Nondynamic Reduced female Parker & conflict considered paternity broods fccundity MacNair Intra-brood competition (1979) Solicitation costs borne by selfish individual only or by entire brood or costs non-existent Parent-offspring 2 locus ESS Offspring selfishness Singly Polygamy Nondynamic Reduced female MacNair & conflict Two types of maternal Intra-brood and Inter- fecundity Parker (1979) countermeasures brood competition considered

Parent-offspring I locus/2 alleles ‘Overconsumer’ genes, Only I trait Multiple paternity in Nondynamic Reduced maternal Law & Cannings conflict Derive conditions for expressed in the considered angiosperms inclusive fitness (1984) spread of rare endosperm of Intra-brood competition (not necessarily overconsumer dcveloping seeds, Siblings are not affected reduced fecundity) alleles increase maternal by selfishness at random investment with respect to genotype

No solicitation costs Downloaded from https://academic.oup.com/biolinnean/article/30/2/115/2676958 by guest on 27 September 2021 September 27 on guest by https://academic.oup.com/biolinnean/article/30/2/115/2676958 from Downloaded Parent4iipring 1 locus/2 alleles ESS Resource-garnering Only I trait Multiple paternity in Nondynamic Reduced female Qyeller (1984) conAict -genes e5Tprcsscd-m considered plants fecundity parental, offspring, at a time Intra-brood competition gametophytic, or Siblings are affected by endosperm tissue selfishness at random with respect to genotype Parent-offspring I locusESS Investment per offspring Singly and Outcrossing, annual, Nondynamic Reduced maternal Bull (1985) conflict Evolution of investment jointly hermaphroditic fecundity and 2 modelled as a angiosperms reduced mean P parental trait and as Sequential production of fitness of m an offspring trait z offspring individual familia ci Environmental variance affects phenotypes Constant and varying environmental variance considered Sexual selection Polygenic model Sex-limited male Jointly Polygyny Dynamic Reduced mean male Lande (1981) Derivation of secondary sexual No male investment viability evolutionary character Assortive mating Sexual selection equilibria Female mating generates a genetic compensates for preferences not under correlation between the sub-optimal direct selection preference and the viability male trait Sexual selection ealitative non- Tendency for females to Jointly POlYiPY Non-dynamic Reduced female Heisler (1981) genetic model mate polygynously No male investment fecundity Test of ‘sexy son’ Females which mate hypothesis polygynously produce fewer offspring than monogamously mated females Sonsof polygynously mated females have higher reproductive success than sonsof monogamous females Sexual selection Polygenic model Sex-limited male Jointly Polygyny Dynamic Reduced male Kirkpatrick secondary sexual Male trait inflluences viability under ( 1985) character male viability, mating certain conditions Haploid 2 locus/2 Three types of female success and fecundity allele model preference Female mating preference affects the viability of her sons and fecundity There is genetic covariance between the male trait and the female preference Two cases of fertility

selection considered Downloaded from https://academic.oup.com/biolinnean/article/30/2/115/2676958 by guest on 27 September 2021 September 27 on guest by https://academic.oup.com/biolinnean/article/30/2/115/2676958 from Downloaded 120 S. J. MAZER must be forged between parent-offspring conflict and sexual selection approaches so that analytical models may be constructed which: (a) describe the evolution of ‘male’ and ‘female’ polygenic traits which influence seed size and the probability of abortion, (b) incorporate fertility selection, viability selection, sexual selection and kin selection, and (c) forestall premature attempts to interpret specific developmental traits in plants as maternal countermeasures to selfish offspring. Downloaded from https://academic.oup.com/biolinnean/article/30/2/115/2676958 by guest on 27 September 2021

CONFLICT OF INTEREST AMONG INTERACTING INDIVIDUALS Kin selection theory predicts that heritable traits enabling an individual to garner resources at the expense of its present or future siblings will be favoured by selection unless the genetic cost to the siblings of this ‘selfishness’ exceeds some function of B/r, where B is the benefit gained by the selfish individual (Trivers, 1974) and r represents the standard coefficient of relationship (Wright, 1922; Hamilton, 1964; Uyenoyama & Feldman, 1980). Simply interpreted, the intensity of inter-sib or parent-offspring conflict should be inversely related to the value of r between interacting individuals. The genetic ‘cost’ of selfishness depends on the number of siblings influenced by selfish behaviour and the value of r among sibs. In plants, maternal individuals may bear seeds fathered by many pollen donors (Ellstrand, 1984), and neighbourhood structure may result in local inbreeding. Consequently, the coefficient of relationship between pairs of seeds developing concurrently within and among fruits may vary among pairs. Multiple paternity and inbreeding complicate the prospects of specifying the point of divergence between the genetic interests of a maternal plant and her offspring. There has been no direct documentation of parent-offspring or inter-sibling conflict in plants; the morphological or ‘behavioural’ features of plants which may be viewed as manifestations of such conflict are not easily identifiable. Recently, however, there have been several theoretical discussions of conflict in plants (Charnov, 1979, 1983; Nakamura, 1980; Kress, 1981; Cook, 1981; Westoby & Rice, 1982; Queller, 1983, 1984; Law & Cannings, 1984; Willson & Burley, 1983; Bull, 1985). These authors have observed that in plants, as in animals, a genetic conflict of interests exists among siblings, between parents and their offspring, and between the maternal and paternal components of the genome. Accordingly, these authors raise the possibility that maternal ‘countermeasures’ have evolved in response to offspring ‘selfishness’. A ‘selfish’ offspring is defined as one capable of acquiring maternal resources at the expense of its siblings and to a degree that reduces the inclusive fitness of its mother. A countermeasure is any trait expressed in the maternal plant which allows it to allocate resources in a way that increases its fitness at the expense of the inclusive fitness of any selfish offspring, Parent-offspring conflict exists when maternal plants maximize their fitness through the production of seeds that are on average smaller than that which maximizes the fitness of any individual offspring. Such a situation may arise because maternal fitness and offspring fitness are functions of different variables. Maternal fitness is a function of fecundity and the mean fitness of individual offspring. Assuming that seed weight is positively correlated with performance (Black, 1958a,b; Twamly, 1967; Williams, Black & Donald, 1968; Carleton & PARENT-OFFSPRING CONFLICT/SEXUAL SELECTION IN PLANTS 121 Cooper, 1972; Dolan, 1984; Stanton, 1984), maternal fitness may be expressed as : w, a (fecundity) (seed weight). Maternal fitness is considered to be independent of the coefficient of relationship between pairs of developing seeds. This fact yields the expectation that, unless the production of variable seeds is advantageous for other reasons (e.g. frequency-dependent selection), maternal fitness is maximized by an equable Downloaded from https://academic.oup.com/biolinnean/article/30/2/115/2676958 by guest on 27 September 2021 distribution of resources among progeny. In contrast, the inclusive fitness of an individual offspring depends upon its own size as well as the degree of relatedness between itself and the siblings with which it shares maternal resources: w, a (seed weight) (r). Kin selection theory predicts that offspring fitness increases with preferential investment unless the cost to siblings exceeds the appropriate function of B/r. Under conditions in which small seeds are favoured for their dispersal or germination characteristics (Black & Wilkinson, 1963; Carleton & Cooper, 1972; Cooper, Ditterline & Welty, 1979; Hendrix, 1984), parent and offspring may converge with respect to ‘optimal’ seed weight. In addition, the maintenance of seed dimorphisms in some inbreeding species suggests that the production of variable seeds is favourable under certain conditions. The assumption that large seeds are more successful than small seeds is required for further discussion of parent-offspring conflict.

CRITERIA FOR PARENT-OFFSPRING CONFLICT IN PLANTS There are five major criteria for the existence of a genetic conflict of interest between parent and offspring over maternal investment. Although I refer to the phenomenon as ‘parent-offspring’ conflict, it should be recognized that in angiosperms the mechanisms by which resource allocation is controlled are poorly understood. The endosperm (neither ‘parent’ nor ‘offspring’) may play an important role in determining the delivery of resources from maternal plant to developing embryo. First, the parental plant and its offspring must be genetically non-identical. This is the case for strictly outcrossing species and for self-compatible but occasionally or frequently outcrossing individuals in a genetically heterogeneous population. This criterion allows the inclusive fitnesses of parents and offspring to be maximized by different patterns of resource allocation. Second, offspring must differ genetically from one another, so that each individual will ‘value’ its own genome to a greater degree than those of its siblings. The degree of genetic heterogeneity among seeds borne by a maternal plant depends on three features of the local population: (a) the genetic diversity of potential pollen donors, (b) the number and relative abundance of genetically distinct pollen donors which successfully fertilize available ovules, and (c) the degree of heterozygosity among pollen donors. Third, offspring must be capable of soliciting maternal investment at the expense of their siblings, and there must be additive genetic variance for this resource-garnering ability (RGA) or ‘selfishness’. The mechanism by which I22 S.J. MAZER some embryos (or endosperms) receive more nutrients than others is not clear. It is generally believed that developing seeds produce hormones which serve as a signal to the maternal plant. In response to these signals, which may vary in strength among seeds and fruits, the maternal plant differentially releases photosynthates and other nutrients to individual seeds or to groups of seeds held within individual fruits (Crane, 1964; Bollard, 1970; Stephenson & Bertin, 1984 and references therein). This ‘source-sink’ relationship among organs is central to discussions of parent-offspring interactions and the potential for conflict over Downloaded from https://academic.oup.com/biolinnean/article/30/2/115/2676958 by guest on 27 September 2021 maternal investment. It has been shown that genetically distinct parental plants pollinating the same female may achieve different rates of seed abortion or produce seeds of different weight (Schaaf & Hill, 1979; Marshall & Ellstrand, 1986; Mazer, Snow & Stanton, 1986). The genetic or chemical factor responsible for this differential success of gametophytes or fertilized ovules has not been identified; presumably, paternally derived alleles expressed in the pollen tube or embryo provide a hormonal cue to which the maternal plant responds with transport and delivery of nutrients. The maternal component of the endosperm or embryo may also vary among developing endosperms and result in some biochemical differentiation of the offspring, Alternatively, a genetic interaction between the maternal and paternal genomes may render some embryos more likely to survive than others. Finally, embryos may be inviable owing to lethal genes at loci other than those determining RGA. Fourth, resources must be limited. The prevalence of resource limitation of fruit and seed production is well known (Maun & Cavers, 1970, 1971; Willson & Price, 1980; Stephenson, 1981; Willson & Burley, 1983). The evolution of selfishness and countermeasures required that resource limitation results in a trade-off between fecundity and offspring viability. The fifth, and most critical, criterion is that the patterns of resource allocation that maximize inclusive fitness differ between the maternal plant and its offspring. Empirical data demonstrating this are particularly difficult to provide. One must show that there is a relationship between maternal investment pattern and maternal fitness, that there is a trade-off between seed size and seed number at the level of the whole plant and that offspring fitness is maximized by a seed weight larger than the mean weight of seeds produced by the plant with the highest maternal fitness.

IDENTIFICATION OF MATERNAL COUNTERMEASURES IN PLANTS Accepting the above criteria, several authors have attributed a number of angiosperm features to the evolution of offspring selfishness or maternal countermeasures. These include the evolution of maternally derived integuments (Westoby & Rice, 1982; Queller, 1983), invasion of gametophytic tissue by paternal genes (double fertilization) (Charnov, 1983), haustoria (Queller, 1983), seed abortion, control over seed dormancy (Cook, 1981 ) , size of the pollen unit (Kress, 1981) and the maternally weighted genome of the endosperm (Westoby & Rice, 1982; Queller, 1983). While these suggestions are consistent with the predictions of kin selection theory, it is not a straightforward matter empirically to identify physiological or morphological traits as countermeasures which have evolved to maximize maternal inclusive fitness (Bull, 1985). PARENT-OFFSPRING CONFLICT/SEXUAL SELECTION IN PLANTS I23 Countermeasures may be empirically identified’by two criteria. First, one must demonstrate that specific morphological or physiological traits function both to limit the acquisition of resources by offspring and to increase maternal fecundity or to decrease the variance in investment per offspring. To do this, one must show that such traits do in fact lead to relatively equable investment among offspring even when some continue to provide cues soliciting investment. This is difficult to do for any plant species, for which the hypothetical ‘cues’ have not yet been identified. Second, one must establish the conditions under Downloaded from https://academic.oup.com/biolinnean/article/30/2/115/2676958 by guest on 27 September 2021 which alleles which preclude maternal plants from investing differentially in their offspring can spread in a population in which alleles for selfishness are widespread. That is, one must show that decreasing the variance in progeny weight or increasing fecundity is selectively advantageous to maternal individuals. Two major difficulties in identifying countermeasures against resource acquisition also constrain their evolution. These are the presence of strong environmental effects on seed weight and environment-specific selection on seed weight. Consider that seed weight may be determined by genes for maternal investment patterns as well as by genes influencing resource acquisition: if selection is to effect evolutionary change in these two traits through their effects on seed weight, phenotypic variation in seed weight must correspond to genotypic variation in these traits. In addition, for selection to effect evolutionary change in seed weight, seed weight must be heritable. A strong environmental component to variation in seed weight within or among individuals precludes high heritabilities of seed weight, maternal investment patterns and RGA. In addition, developmental effects on seed weight, including positional or phenological effects (Hocking, 1980; Schaal, 1980; Waller, 1982; Hendrix, 1984; Mazer et al., 1986) may preclude a high heritability of RGA. In spite of these difficulties it is necessary for theoretical models to consider the existence of maternal countermeasures because their presence and frequency will determine whether the genetic variation among offspring in RGA can result in phenotypic variation in seed size. In addition, parent-offspring conflict models must consider the joint evolution of countermeasures and selfishness (Bull, 1985). While these problems are not fatal to the notions that specific traits of seeds represent maternal countermeasures, they point to the need for: (1) the detection of heritable variation in maternal patterns of resource allocation among seeds, (2) field studies of the effects of this variation on maternal fitness, and (3) genetic models incorporating the evolution of offspring RGA and the ecological consequences of maternal investment patterns among developing seeds.

IDENTIFICATION OF RESOURCE-GARNERING ABILITY Based on the theoretical criteria above, the potential exists for parent- offspring conflict to occur. Evidence for genetic variation in RGA is supported by three lines of evidence. First, seed abortion is extremely common and is often non-random with respect to genotype (Moore, 1946; Brink, 1952; Henson & Tayman, 1961; Stickler & Wassom, 1963; Sayers & Murphy, 1966; Mogensen, 1975; Schaal, 1980; Willson & Price, 1980; Lee & Bazzaz, 1982; Pimienta & 124 S. J. MAZER Polito, 1882; Bawa & Webb, 1984). Second, the observation that seed size is influenced by paternal genotype (consistently across females) in some species implies that there exists additive genetic variance in embryo growth rates or RGA (Marshall & Ellstrand, 1986; Mazer et al., 1986). Finally, there is growing evidence that seed quality is affected by pollen composition (Mulcahy, 1971, 1974; Mulcahy & Mulcahy, 1975; Schemske & Pautler, 1984). If embryo growth and survival are determined largely by genetic interactions between the maternal and paternal contributions, directional selection upon genes for Downloaded from https://academic.oup.com/biolinnean/article/30/2/115/2676958 by guest on 27 September 2021 nutrient-garnering ability may be constrained (for evidence of interactions, see Brink, 1952; Bertin, 1982; Mazer et al., 1986). It has not been demonstrated unequivocally that there exists additive genetic variance in RGA. Below, however, I assume that this is possible.

SELECTION ON MATERNAL INVESTMENT PATTERNS AND RESOURCE-GARNERING ABILITY: COMPONENTS OF FITNESS Fecundity selection Consider a population of annual, hermaphroditic, randomly mating adult plants. Assume that, as females, individuals exhibit additive genetic variation in their tendency to discriminate among offspring that vary in their RGA. Also assume that, as males (pollen donors), individuals vary in the additive effects of the RGA alleles they transmit to their progeny. Assuming a high heritability of both traits and discrete generations, how might selection operate over the entire life cycle of these individuals? When pollen grains arrive at a receptive stigma, there is competition among them to gain access to ovules, those with the highest rates of germination, pollen tube growth and/or fertilization ability having the advantage. Paternally derived alleles for rapid germination, rapid pollen tube growth and high RGA may be genetically linked or phenotypically correlated (Mulcahy, 197 1, 1974; Mulcahy & Mulcahy, 1975; Tanksley, Zamir & Rick, 1981), but I will restrict the following discussion to pollen-derived genes which influence the allocation of maternal resources following syngamy. Once fertilization has occurred, maternal plants which discriminate among high- and low-RGA offspring will allocate more resources to those offspring which solicit them most effectively. Under the assumptions of this model, selection for alleles effecting high RGA occurs during seed development only in discriminating maternal plants. As seeds mature, there will be selective abortion of those offspring that have obtained resource levels below a minimum threshold (as proposed by Lloyd, 1980; Lloyd, Webb & Primack, 1980). On average, in discriminating maternal plants, these offspring will be those exhibiting low values of RGA. Within the seed crops of discriminating females, the increased investment in vigorous embryos and/or abortion of ineffectual embryos results in two features of the F, generation. First, if abortion rates are high, the weight of the surviving seeds may be larger (but their numbers lower) than in the F, generation produced by non-discriminating maternal plants. Alternatively, seed crops may simply be more variable, reflecting a pattern of differential investment. Second, the frequency or total biomass of offspring bearing genes for high RGA will be PARENT-OFFSPRING CONFLICT/SEXUAL SELECTION IN PLANTS 125 higher among the progeny produced by discriminating females than by non- discriminating females. It is not sufficient to measure the fitness of discriminating and non- discriminating maternal plants solely in terms of their fecundity. Since maternal fitness is a function of both fecundity and mean offspring fitness, it is necessary to complete the life cycle by examining the performance of the offspring produced by these adults. In so doing, progeny performance is included as a component of the fitness of the adults of the PI generation. Instead of defining a Downloaded from https://academic.oup.com/biolinnean/article/30/2/115/2676958 by guest on 27 September 2021 generation of natural selection as occurring from zygote to zygote, I have considered it as a process occurring from adult to adult.

Viability selection It is possible that the progeny of discriminating females compensate for their potentially low numbers with superior germination and juvenile survivorship. If large or variable progeny achieve high enough rates of survivorship, then the number of F, adult individuals derived from discriminating PI females will be greater than the number derived from non-discriminating mothers. In this case, the ‘countermeasures’ of the non-discriminating females would not confer upon them a selective advantage in spite of their immediate effects upon fecundity. Also, since RGA alleles are neutral in non-discriminating females but favoured in discriminating females, the intuitive result of this selection process would be an increase in the frequency of RGA alleles in the F, generation. These intuitive conclusions are consistent with the parent-offspring models in which genes for selfishness spread when they result in relatively successful ‘over-consumer’ genotypes and in which the average fecundity of maternal individuals may decrease. However, these models do not simulate the joint evolution of the two traits: the tendency to discriminate in favour of ‘over-consumer’ progeny and the ability of offspring to garner resources.

THE JOINT EVOLUTION OF DISCRIMINATION AND RGA The simultaneous evolution of these two traits in plants involves interactions between them which may result in a non-intuitive evolutionary outcome. It is difficult to explore the probable outcome of these interactions without an analytical model. Consider, however, the following possibilities. (a)The large but less numerous progeny of discriminating females do not have survivorship rates sufficient to increase their frequency relative to the progeny of non-discriminating females. The change in the frequency of discriminating females between the PI and F, generations will be negative or zero. (b) The viability of the large or variable progeny of discriminating females is sufficiently high that their abundance relative to the progeny of non- discriminating females at adulthood increases between generations. In both cases, since discriminating PI females will have favoured high-RGA offspring, the frequency of high-RGA alleles will have increased. Is it possible that these high-RGA offspring can compensate for their low numbers (in case (a)) by exhibiting superior reproductive success as pollen donors to other members of the F, generation? If so, discriminating maternal plants may I26 S. J. MAZER produce progeny with higher survivorship, lower maternal fecundity (since they too will tend to discriminate) and higher paternal success than non- discriminating individuals. Maternal fitness might then be defined in terms of a third variable, the male reproductive success of the progeny: w, ac (fecundity) (seed weight) (male reproductive success of progeny). The paternal success of the progeny produced by discriminating females relative to the progeny of non-discriminating females will depend upon three Downloaded from https://academic.oup.com/biolinnean/article/30/2/115/2676958 by guest on 27 September 2021 components of the population: the frequency of discriminating pollen recipients in the F, generation, the relative fecundity of the non-discriminating recipients, and the frequency of other pollen donors with high RGA. The advantage of resource-garnering ability is frequency-dependent. The critical question is whether the trade-off between maternal fecundity and paternal success is sufficient to allow the spread of alleles which result in a reduction in population mean maternal fecundity.

SELFISHNESS VS. COUNTERMEASURES OR MALE COMPETITION VS. FEMALE CHOICE? This analysis recalls components of the controversial ‘sexy son’ hypothesis, in which there is a postulated compensatory advantage to females that choose to mate with ‘attractive’ males (that reduce their fecundity) because their offspring will bear the genes of their fathers, and thus themselves be successful as fathers (Weatherhead & Robertson, 1979; Heisler, 1981; but see Kirkpatrick, 1985). The preceding description has used vocabulary introduced earlier in the context of parent-offspring conflict; I propose now that many components of this process are identical to the critical features of sexual selection. Furthermore, since the available sexual selection models explicitly incorporate two critical features ignored by the parent-offspring models-the joint evolution of the two traits and a normal phenotypic distribution of these traits-it is appropriate to consider their results in the context of seed development. Strictly speaking, sexual selection involves two components: (a) female preference, during mating, for males bearing particular traits and/or (b) competition (generally among males) for mates (Darwin, 187 1; Fisher, 1930). In animals, such traits may not increase the fitness of the individuals (generally males) bearing them in any activities other than those associated with reproduction. It has been suggested that sexual selection for male traits occurs in plants (Bateman, 1948; Janzen, 1977; Willson, 1979), but most recent empirical studies have focussed upon the adaptive significance of pollen competition, inflorescence size, floral display, flower/fruit ratio, amd attractiveness to pollinators (Willson & Rathcke, 1974; Mulcahy & Mulcahy, 1975; Lloyd & Webb, 1977; Willson & Price, 1977; Stepehenson, 1979; Willson, Miller & Rathke, 1979; Bawa, 1980; Schemske, 1980; Queller, 1983). Evolution of these traits involves differential success of individuals or their gametes prior to fertilization. Most processes effecting successful pollen dispersal and fertilization are more accurately identified as intra-sexual competition than as female preference. Differential pollen tube growth rates offer an ambiguous case; growth rates may depend upon maternal stylar tissue (Marshall & Ellstrand, 1986). Post-fertilization female choice of offspring bearing ‘male’ traits has not been explicitly identified in plants (but see Bertin, 1982; Stephenson & Bertin, PARENT-OFFSPRING CONFLICT/SEXUAL SELECTION IN PLANTS I27 1984; Bookman, 1984; Bawa & Webb, 1984; for discussions and evidence that this might occur). In the case outlined above, maternal plants do not choose mates directly. Rather, they preferentially invest in or ‘choose’ the offspring of males bearing alleles for high RGA. As in models of sexual selection, the ‘preference’ (the tendency to discriminate) determines the evolution of the ‘male trait’ (high RGA) . In sexual selection theory, if the preference becomes genetically correlated with the male trait, two possibilities arise: first, that of a stable Downloaded from https://academic.oup.com/biolinnean/article/30/2/115/2676958 by guest on 27 September 2021 equilibrium in which female fecundity is not maximized (the ‘sexy son hypothesis’) and second, that of an unstable ‘runaway’ process. First, can a stable equilibrium be reached in which females with relatively low fecundity will be favoured due to their preference for pollen donors which bear genes rendering them successful in reproduction-the ‘sexy son’ hypothesis? Kirkpatrick (1985) concludes, based on a quantitative genetic model, that this is not possible. However, the assumptions of his model-and those of similar sexual selection models (Lande, 1981 ; Kirkpatrick, 1982)-do not wholly correspond to those outlined in five major ways: (1) Recent quantitative genetics models of sexual selection assume an optimum phenotype under viability selection for a male-limited trait (in this case, RGA) subject to sexual selection (Lande, 1981 ; Kirkpatrick, 1982, 1985). In these models, as in the process outlined above, the process of ‘mate choice’ is frequency dependent. That is, the relative reproductive success of a male of a given RGA phenotype depends upon the value of his phenotype relative to other males in the population. In available selection models, however, the relationship between genotype and viability is not frequency dependent, whereas in the process I have described for plants, it is. Assuming that offspring viability is correlated with seed weight, the viability of an offspring with a specific RGA genotype depends upon both the tendency to discriminate exhibited by the maternal plant in which it develops and the RGA phenotypes of its simultaneously developing siblings relative to its own (since maternal plants can presumably respond only to differences among offspring with respect to solicitation cues). Since seed size depends on factors other than genes for RGA, there is not a simple relationship between RGA and viability. The regression of RGA genotypic values on seed size phenotypic values is a function of the frequency distributions of the tendency to discriminate and RGA values. While viability selection on phenotypic variation in seed size is independent of population gene frequencies, the absolute fitnesses of RGA genotypes are not. Thus, an optimum value of RGA with respect to viability cannot be specified because there is no inherent absolute fitness associated with a given value of RGA independent of the maternal environment. This is in contrast to the sorts of male traits undergoing viability and sexual selection in available genetic models. Traits such as tail size in birds do not exhibit frequency-dependent viability selection. (2) In Kirkpatrick’s ( 1985) sexual selection model, fecundity depends largely on the male with whom a female chooses to mate because of resources offered by the male. In plants, however, assuming equal resource availability among maternal plants, the fecundity of a mating depends primarily upon the maternal individual’s tendency to abort developing seeds and upon the distribution of RGA among her mates. In addition, in the process I have described, fecundity I28 S. J. MAZER (a maternal trait) is an inverse function of mean offspring viability. In Kirkpatrick’s model, maternal fecundity and the viability of male offspring are both determined primarily by the male genotype. (3) Female preferences are subject to fertility selection in Kirkpatrick’s model; his result is that they evolve to ‘optimum’ fertility. As long as the correlation between the male character and the female preference is imperfect, the available genetic variance allows each trait to evolve toward its own optimum. Female preferences evolve to optimize female fertility while the male trait evolves to Downloaded from https://academic.oup.com/biolinnean/article/30/2/115/2676958 by guest on 27 September 2021 optimize viability, sexual and fertility selection. In animals, then, both the female and the male traits undergo direct selection on fecundity, but only the male trait undergoes viability selection. In plants, in contrast, the tendency to discriminate (female preference) is itself also directly subject to viability selection, because seed size is a character determined by a number of genes that include the genes for discrimination. In other words, seed size is in part determined by the preference trait. Since seed size is affected by both fertility selection and viability selection (as is the male trait, RGA), it is not clear that maternal investment must evolve to maximize fertility. (4) The consequence of family structure cannot be inferred from the sexual selection models. According to the parent-offspring conflict models, the degree of relatedness among competing offspring should directly affect the evolution of RGA (i.e ‘selfishness’). While the breeding system of a plant population will in part determine the distribution of RGA and the value of r among simultaneously developing seeds, this variable is not incorporated into the sexual selection models. (5) Strong interactions between maternal and paternal contributions to seeds may affect seed size and viability (Schaaf & Hill, 1979; Mazer et al., 1986; Mazer, 1987). Also, maternal effects may far exceed paternal effects in several components of seed yield (Mazer et al., 1986). The importance of sexual selection upon traits subject to strong maternal effects and interactions are not considered in available models of sexual selection. For these reasons, it is not clear that Kirkpatrick’s conclusions concerning the demise of the ‘sexy son’ hypothesis apply to the evolution of RGA. The second major conclusion derived from sexual selection theory that may be applied to plants is this: there may be conditions under which a dynamic process similar to the ‘runaway’ process thought to occur among animals can also occur in plants, resulting in maladaptive properties of seed size as well as clutch size (Fisher, 1930; Lande, 1981). That is, if high RGA is viewed as a male trait yielding pollen donors successful in producing seeds, can RGA evolve to a point where mean seed viability is reduced owing to a correlation between high RGA and larger than optimal seeds (from both the offspring’s and the mother’s point of view)? If there is an optimal seed size with respect to viability above which individual fitness decreases, there may exist phenotypic values of RGA which are disadvantageous to the developing seeds which exhibit them.

DISCUSSION: THE EVOLUTION OF RGA-ANALOGY TO SEXUAL SELECTION The construction of a model which describes the evolution of RGA should include many of the same components as models of sexual selection in which males provide neither resources nor parental care to their offspring. Pollen PARENT-OFFSPRING CONFLICT/SEXUAL SELECTION IN PLANTS 129 donors provide only genes which, in turn, influence the likelihood of abortion, the seed size achieved (and the correlated consequences for sporophytic vigor), and the performance of offspring as adult pollen donors. If paternal effects upon seed abortion and size in nature (Schaaf & Hill, 1979; Marshall & Ellstrand, 1986; Mazer el al., 1986) are due to genes which determine resource acquisition, then it seems reasonable to suggest that quantitative variation in seed size reflects polygenic control of RGA. It is possible that differences in seed size Downloaded from https://academic.oup.com/biolinnean/article/30/2/115/2676958 by guest on 27 September 2021 among siblings are due to differences in metabolic efficiency and not to differences in resource allocation. I have assumed that this is not the case. It may furthermore be supposed that the tendency for maternal sporophytes to be discriminating or ‘choosy’ is also under polygenic control. The potential existence in wild species of additive genetic variance in both RGA and the tendency to discriminate makes it difficult intuitively to predict the evolutionary outcome of selection on phenotypic variation in seed weight in natural populations. This problem is analogous to those found in discussions and models of sexual selection in the following ways. First, the survival and size attained by a developing offspring is a function of its RGA as well as the tendency to discriminate exhibited by the maternal sporophyte in which it develops. This property of offspring success is analogous to that of male mating success in discussions of sexual selection; the success of a given male may depend upon both its intrinsic competitive ability and upon the frequency of females which choose to mate with him. It may be disturbing to some to consider the number and performance of seeds fathered by specific pollen donors as analogous to the mating success of male animals. As I emphasize above, however, after fertilization pollen donors do not engage in intra-sexual competition independent of maternal plants. The view that male mating success in plants is achieved directly through the number and size of the seeds they father is an accommodation that does not invalidate the proposed analogy. Second, the tendency of maternal sporophytes to discriminate among their developing offspring when resources are limiting is analogous to female choice in animals. Individuals of most species of seed plants probably simultaneously develop the offspring of several pollen donors. The proposed ability of seed- bearing plants to abort seeds of ‘poor genetic quality’ (defined here as low RGA) provides an opportunity for them to choose mates on the basis of some quality criterion. The success of this analogy depends upon the existence of a mechanism which allows maternal plants to assess the genetic quality of young embryos fathered by genetically distinct pollen donors-a controversial suggestion at best. Potential cues available for assessment may include pollen tube growth rates as correlates of sporophytic success (Mulcahy, 1974), hormone production, or metabolic rates of developing seeds. If there is additive genetic variance in the tendency to discriminate, the trait may be open to the same patterns of selection as female choice as described in models of sexual selection in animals (O’Donald, 1980; Lande, 1981 ) . Third, selection may operate to favour maternal plants on the basis of seed quality, not seed quantity. It is often assumed that, in plants, the number of seeds produced is a good measure of a maternal plant’s absolute fitness. As described above, however, the force of sexual selection may be in opposition to that of fecundity selection and/or viability selection. 130 S. J. MAZER The analogy between the evolution of RGA and the evolution of male traits in the context of sexual selection is not wholly satisfying because sexual selection models do not directly address the component of kin selection involved in the allocation of maternal resources among simultaneously developing offspring. Likewise, parent-offspring conflict models do not fully describe the selective forces involved in seed development because they do not resolve the opposing forces of mate selection and fecundity selection. There are two additional shortcomings of the available parent-offspring models. First, these models posit Downloaded from https://academic.oup.com/biolinnean/article/30/2/115/2676958 by guest on 27 September 2021 only the existence of females which either do or do not invest differentially among their offspring in response to variation in solicitation cues (those without or with countermeasures, respectively). They do not allow for continuous variation in the pattern of maternal investment (but see Bull, 1985). Second, unless either a quantitative genetic model with a genetic correlation between RGA and maternal discrimination, or a two-locus model with linkage disequilibrium between RGA and discrimination is built, parent-offspring models cannot include the role of genetic correlation- the phenomenon which generates the most interesting properties of the sexual selection models. Significantly, the two types of models appear to yield conflicting conclusions with regard to the evolution of traits which reduce female fecundity (Table 1). Parent-offspring conflict models support the view that traits can evolve in spite of their effects on fecundity (Blick, 1977; Stamps et al., 1978); sexual selection models have led to the conclusion that fecundity will always be maximized (Kirkpatrick, 1982, 1985). A harmonization of these two approaches is essential before it will be possible to construct models which incorporate kin selection, fecundity selection, viability selection and sexual selection in a way that yields meaningful predictions concerning the outcome of selection on RGA and maternal discrimination in plants.

ACKNOWLEDGEMENTS I thank J. A. Stamps for many lively discussions on parent-offspring conflict in plants. A. V. Hedrick, R. R. Nakumara, R. Law, A. L. Snow, M. L. Stanton, D. C. Queller and two anonymous reviewers read a previous version of this paper and provided many much-appreciated and insightful criticisms and suggestions for improvement. Mark Kirkpatrick generously provided a copy of his unpublished manuscript. I owe special thanks to John D. Damuth and to I. Lorraine Heisler who offered many timely and thoughtful discussions and insights.

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