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Maternal Effects in PlantsAuthor(s): Deborah A. Roach and Renata D. WulffSource: Annual Review of Ecology and Systematics, Vol. 18 (1987), pp. 209-235Published by: Annual ReviewsStable URL: http://www.jstor.org/stable/2097131Accessed: 29/05/2009 08:31

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Anti. Rev. Ecol. Svst. 1987. 18:209-35 Copyright ? 1987 bY Annuiiial Reviews Inc. All rights reserved

MATERNAL EFFECTS IN PLANTS

Deborah A. Roach

Department of Zoology, Duke University, Durham, North Carolina 27706

Renata D. Wulif

Escuela de Biologia, Universidad Central de Venezuela, Apartado 47114, Caracas, Venezuela

INTRODUCTION

Maternal effects in plants were recognized as long ago as 1909 (32). Recent evidence, primarily over the last 15-20 years, shows that maternal effects can contribute substantially to the phenotype of an individual, and as we show, this has important consequences for the interpretation and design of both ecological and genetic studies. Following a discussion of the consequences of maternal effects and an analysis of the different ways these effects can be estimated, we review the evidence for maternal effects from the fields of physiological ecology, crop science, and quantitative genetics. We do not review all of the literature because that would be a monumental task; rather, we focus on representative studies from each of these fields. It is our contention that despite evidence that maternal effects can have a large influence on offspring phenotype, few detailed studies have identified the specific causes of maternal effects, particularly in natural populations.

MATERNAL EFFECTS: DEFINITIONS AND CAUSES

Variation in an individual's phenotype may be determined not only by the genotype and environment of that individual but also by maternal effects, i.e. the contribution of the maternal parent to the phenotype of its offspring beyond the equal chromosomal contribution expected from each parent. We distinguish three different classes of maternal effects: cytoplasmic genetic,

209 0066-4162/87/11 20-0209$02.00

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endosperm nuclear, and maternal phenotypic (Figure 1). Cytoplasmic genetic maternal effects are derived from the fact that organelles such as plastids and mitochondria can be directly transferred from the maternal plant to the offspring during ovule formation and development, and this transmission is independent of nuclear genes. Molecular and quantitative genetic studies have shown that cytoplasmic factors contribute to heritable variation in both qualitative and quantitative traits in plants. Discussions of cytoplasmic maternal effects in this paper are limited to identifying the general phenomenon and do not focus on the details of transmission, which have been reviewed elsewhere (63, 164).

A second class of maternal effects in plants originates via the endosperm (Figure 1). During angiosperm development, multiple fertilization usually results in 3N endosperm with two nuclei from the maternal and only one from the paternal parent. Although the endosperm is not always triploid, with the single exception of the Onagraceae, it always contains more doses of maternal than paternal genes (177). The endosperm contains enzymes important for germination (72) and is also the source of nutrients for the developing embryo. As a consequence of the differential dosage of male and female genes, the female parent may have a more important role in determining the characteristics of this nutrient source.

A third class of maternal effects is phenotypic, resulting from the environment or genotype of the maternal parent. These influences may occur via structure or physiology (Figure 1). The tissues immediately surrounding the developing embryo and endosperm are all maternal. These tissues, the integuments of the ovule and the wall of the ovary, eventually form the seed coat, fruit, and accessory seed structures such as the hairs, awns, and barbs. Such structures are important determinants of seed dormancy, dispersal, and

I MATERNAL GENERATION OFFSPRING GENERATION

CYTOPLASMIC CYTOPLASMIC DNA DIRECT TRANSMISSION DNA

EONMEV R PHYSIOLOGY ENVIRONMENT i MATERNAL I OFFSPRING 1F- I

NUCLEAR - HENOTYPE STRUCTURE PHENOTYPE NUCLEAR I GENOTYPE GENOTYPE

ENDOSPERM ENDOSPERM NUCLEAR I NUCLEAR DOSAGE I DOSAGE

Figure 1 Path diagram showing maternal effects and other influences on the phenotype during the ofitspring generation. Solid arrows represent nmaternal effects.

MATERNAL EFFECTS IN PLANTS 211

germination traits, and variation in these traits can carry over to influence the mature phenotype of an individual.

CONSEQUENCES OF MATERNAL EFFECTS

Selection Studies Maternal effects are generally considered 'troublesome' sources of error in the sense that they are non-Mendelian and reduce the precision of genetic studies. In fact, the actual influence of maternal effects on the response to selection will depend on the type of maternal effect involved. Environmental maternal effects will increase the amount of environmental noise and thus slow the response to selection. The amount of genetic covariation between consecutive generations will be further reduced if environmental maternal effects persist for several generations (3, 89) or if there are substantial interactions between maternal effects and the environment (3, 150).

Cytoplasmic or nuclear genetic maternal effects will inflate the amount of genetic variance but may slow the response to selection if the trait is completely under maternal control. Naylor (120) constructed a model to compare the response to selection for a population in which fitness differentials in offspring are under complete maternal control vs a population with no maternal effects and complete offspring genetic control of fitness. Both models reached similar equilibria with stabilizing selection, but the maternal control model showed a slower response.

Variation in an offspring trait may also be under the dual control of both maternal and offspring genotype. The response to selection for such a trait will depend on the correlation between the different effects. If there is a negative correlation between maternal and offspring effects, then the response to selection will be slowed (38, 170, 179). Despite the fact that many traits probably are under dual control, the consequences of this are rarely considered in selection studies.

The consequences of maternal effects for the response to selection may be further complicated by the correlation between maternal and offspring environments. If there is a high positive correlation between successive environments, then maternal effects will be advantageous to individual offspring, particularly if offspring do better in an environment resembling the parental environment (92).

Ecological Studies Variation in seed, seedling, and adult traits caused by maternal effects can have important consequences for the ecology of an individual. Seed size, for example, is a trait for which a large maternal effect has been demonstrated (see Evidence), and which has important ecological consequences. Studies

212 ROACH & WULFF

have shown an effect of seed size on germination characteristics (23, 34, 39, 182, 185), on seedling size (14, 136, 153, 184, 188), and on adult plant size and competitive ability (14, 39, 142, 154, 189). Variation in other maternally derived traits can similarly result in size hierarchies and differential fitness of individuals within a population. Thus, our understanding and identification of maternal effects has important consequences for our understanding of plant distributions both within and between populations and communities.

Maternal effects may complicate ecological studies, many of which are designed to identify the environmental factors determining the survival, reproduction, and distribution of individual species. In these studies, it may be difficult, if not impossible, to identify the environmental factors determining success if the important events took place during the previous generation via maternal effects. If maternal effects do contribute to the traits of interest, then a complete ecological understanding of the variation may require a multiple generation study and a separation of genetic and environmental maternal effects.

Maternal effects may also complicate the interpretation of common garden studies. Phenotypic variation among plants in a common garden experiment is generally attributed to genetic differentiation (24). Using tillers or cuttings for these types of studies can introduce a bias from within generation carry-over effects of the home environment (85). In a similar way, maternal effects will result in maternal carryover effects if seeds are used in these experiments (7). The environment under which the seeds were matured, i.e. the maternal environment, may influence the growth of individuals in the common garden. In order to minimize this error, seed plants must be grown in a common garden for one (121) or several generations (7). However, persistent maternal effects may still exist (3, 131).

METHODS FOR ESTIMATING MATERNAL EFFECTS Genetic Studies DIFFERENCES IN RECIPROCAL CROSSES The most direct quantitative evidence for unequal contribution by maternal and paternal parents to the phenotype of offspring is through reciprocal crosses in which pairs of individuals serve as both maternal and paternal parent. A number of different reciprocal crossing designs may be used (for reviews see 26, 49, 106); the most common is the complete diallel. Reciprocal pairs have similar nuclear genetic contributions, and any difference in performance of reciprocal pairs will be due to a maternal (or perhaps a paternal) effect. The relative importance of maternal and paternal effects can be determined by comparing the relative amount of variation between maternal and paternal half-sib families. Variance between family groups will be similar if there are no parental influences beyond the


equal chromosomal contributions, and maternal effects will be indicated if there are greater differences between maternal families than paternal families (106, 165). Paternal effects have been found only in a few species (164). For dioecious plants, where it is not possible to use the same individual as both male and female parent, the best method for detecting non-nuclear effects is a North Carolina Type-II design in which all possible matings are made between males and females (28, 106).

RECIPROCAL SPECIFIC EFFECTS The next level of analysis partitions maternal effects into the portion due to differences between reciprocal crosses, which is consistent across all crosses sharing a similar maternal parent, and that which is due to the interaction between progeny genotype and the maternal effect (73, 174). These interaction effects have been termed 'reciprocal specific effects' and can be distinguished using the techniques of Hayman (73) or Cockerham & Weir (27). They are sometimes attributed to interactions between cytoplasmic maternal effects and offspring nuclear effects. Without further detailed analysis, it is possible to argue they could also be due to an interaction of any other type of maternal effect (Figure 1) with offspring nuclear effects. An even more detailed analysis of a diallel cross, which allows separation of additive and dominance components of reciprocal differences, has been worked out (41, 179), but to our knowledge this level of detail has rarely been applied to studies in natural populations (for an exception see 74).

SEPARATING DIFFERENT TYPES OF MATERNAL EFFECTS It is important to be able to distinguish the different classes of maternal effects because they have different evolutionary consequences. A number of experiments have attempted to distinguish cytoplasmic effects from other types of maternal effects by their persistence over generations (10, 21). The problem is that environmental effects may also persist for more than one generation (3). A more definitive identification of cytoplasmic maternal effects can be made with specific crossing designs that repeatedly use the same maternal lineage. For example, Corey et al (31) used a male tester in crosses with reciprocal F1 hybrids to show a cytoplasmic maternal effect for seedling size in Arabi- dopsis.

Endosperm dosage maternal effects can be identified by their unequal contribution from male and female parent. Smith & Fitzsimmons (153) suggest that it is possible to identify an endosperm effect if one assumes that (a) at least two doses of factors are necessary to obtain, say, a heavy grain, and (b) a single dose has no effect on grain weight, and (c) the effect of three doses is equal to the effect of two doses. Their crossing scheme produced F1 hybrids between large- and small-seeded parental lines of flax, and then F2's

214 ROACH & WULFF

from permutations of crosses among the Fl's. They reasoned that the mean weight of F2 grains should equal the average of the parental lines if there were endosperm dosage effects on grain weight. Their results did not show any dosage effects. Using a different technique, Millet & Pinthus (115) tested endosperm genetic maternal effects on grain weight in Triticum aestivum from a comparison of self and reciprocal crosses of heavy- and light-seeded culti- vars. They reasoned, that the mean weight of the F2 should equal the average of the grain weights of the two selfed lines. These techniques have not been applied elsewhere, nor have their assumptions been tested.

Phenotypic maternal effects can be either genetic or environmental, and simple experimental designs can be used to separate these phenotypic effects. The most common technique is to clone individuals over different environments prior to crossing (25). The relative contribution of genetics and environment to the offspring phenotype can then be evaluated.

It is not possible to separate genetic and environmental maternal effects in a single generation. However, an approximate separation of these effects can be done with perennial species; this involves collecting seed over several years from the same maternal plant and calculating various covariances between seed weight and seedling size. Genetic and persistent environmental effects can then be separated from transient environmental effects (98, 112).

No study has ever considered all possible causes of maternal effects simultaneously. Thus, it is not possible to evaluate the relative importance of the different origins of maternal effects.

Environmental Studies The general methodology used to study environmental maternal effects is to place plants under different environmental conditions and to observe traits expressed in the offspring generation. These studies measure an environmental carryover effect and involve variables of the environment including light, nutrients, temperature, water, and growth substances. Most studies examine the effect of only one of these environmental variables at a time, except in studies done in natural populations in which case the "environment" is not specifically identified. Environmentally induced genetic changes may occur as a result of these environmental effects (36, 42, 80), but these effects are rare and we do not include them in our definition of environmental maternal effects. Instead, we consider environmental effects as transient influences that endure one generation or, with diminishing effect, into the second generation.

It is often difficult to separate environmental effects acting directly on the seed from those acting on the mother and then the seed. In this paper, maternal effects include all influences that take place before seed dispersal. In other words, we include as maternal effects all effects that occur after embryo formation but before seed dispersal.


EVIDENCE FOR MATERNAL EFFECTS

Maternal Effects on the Seed

SEED SIZE AND MINERAL COMPOSITION

Genetic studies A large maternal effect on seed size, identified through differences between reciprocal crosses, has been found in Zea mays (43), Brassica campestris (150), Raphanus raphanistrum (110), and a number of other species (180, reviewed by 2). Most of these studies unfortunately have not separated possible sources of the maternal effects, not even at the basic level of genetic versus environmental contributions. In one of the few studies that has separated phenotypic maternal effects into genetic and environmental components, Antonovics & Schmitt (6) showed that both components had effects on propagule weight in Anthoxanthum odoratum, but that environmental maternal effects predominated. In the only other genetic study of maternal effects with a noncultivated species in a natural population, Roach (135) showed reciprocal differences due to maternal effects on seed size in Gera- nium carolinianum.

Genetic studies with cultivated plants have shown that maternal cytoplasm may directly influence seed size. For example, in crosses between small- and large-seeded flax varieties, Smith & Fitzsimmons (153) found reciprocal differences in seed weight. Curiously, parents producing small seeds had a larger maternal effect than did those that produced large seeds. Persistence of these differences into the F2 and F3 hybrids indicated that the effects were due to maternal cytoplasm. In order to show cytoplasmic maternal effects definitively, multiple generation studies such as this need to be done. Con- clusions about the presence of cytoplasmic maternal effects have sometimes been prematurely reported in the literature. For example, Chandraratna & Sakni (21) showed a maternal effect on grain weight in rice, and a model constructed by them assumed that this maternal effect was due to cytoplasmic inheritance. However, the authors acknowledge that later generation crosses would be needed to show cytoplasmic inheritance definitively.

Genetic studies of cultivated species have also demonstrated various types of maternal effects on the mineral composition of seeds. Reciprocal differences, suggesting large maternal effects, have been found for seed chemistry in pearl millet (16), seed oil in Lupinus (180), fatty acid content in maize (137), and protein content in dry beans (101) and soybeans (149), but not in Brassica campestris (150). In the case of dry beans, and in most cases with soybeans, these differences did not persist into the F2, suggesting that these are noncytoplasmic maternal effects. Cytoplasmic maternal effects may ex- plain reciprocal differences in oil content in sunflowers, for it has been

216 ROACH & WULFF

hypothesized that oil synthesis may occur primarily in mitochondria or chlo- roplasts (57). Unfortunately, a multiple-generation study was not done to confirm this conjecture.

Environmental Studies Evidence for environmental phenotypic maternal effects may be inferred from studies in natural populations in which variation in seed size has been reported both among and within plant populations. Within populations the major source of variation is among individual plants (155, 162, 172); thus, either genetic or microenvironmental factors are an important influence on the size of seeds produced. In these studies, variability in seed size has been correlated with environmental factors such as drought (144), temperature (113), and grazing (34).

Studies in which single environmental factors have been examined, under controlled conditions, have shown that the effects on seed weight of maternal environmental conditions depend on the timing of the treatment. Sionit & Kramer (151) found a decrease in seed weight in soybeans in response to water stress when the stress was applied during pod formation and filling, but no similar response occurred when the stress was applied at other stages of development. Decreased water availability for the mother plant results in decreased seed weight in a number of other species (114, 140, 183, 187), probably a result of decreased rates of photosynthesis and changes in seed maturation time.

Growth substances applied to the maternal plant may also affect seed size, particularly if applied during the time of seed development and maturation. Hormone content in seeds varies during development and may have a regula- tory role in directing the movement of assimilates toward the seed (12). Hormone content of seeds also varies with environmental factors; for example, the concentration of abscisic acid is increased by water stress, decreased by low temperatures, and affected by the mineral nutrition of the parent plant (91). Moreover, seed weight correlates with endogenous ABA content (147). The role of hormones in seed development is poorly understood, and although several stages of seed growth and development are correlated with changes in hormone levels (46), these changes may not necessarily indicate differences in hormone action or be the cause of differences in rate of seed growth (64).

Exposure of the parent plant to different temperatures affects the size of seeds produced in several species (3, 22, 47, 187). These effects have usually been ascribed to differences in assimilate supply. However, since temperature affects both the rate of dry matter accumulation in the seed and its period of development, maximum seed weight is not necessarily attained at the temperature favoring the highest accumulation of dry matter (173). Daylength


also affects seed weight, as for example in Chenopodium rubrum (30). In this case, photoperiodic treatment extremely early in development affected seed weight. In contrast, photoperiodic effects on seed dormancy usually occur only at later stages of seed development (65).

The effect of maternal resources on seed size has been studied by various methods. In many species, seed size increases with increased nutrient supply (64, 125, 181, 187). In some cases, there is an interaction between maternal genetic and maternal environmental effects (105). In other species, seed weight remains stable despite increased nutrient supply and increased plant growth (53). Similarly, in some species, partial shading during certain stages of development may influence seed weight (88, 126), but in other species, shading may have no effect on final seed weight if the period of seed development is also increased (48). Environmental factors, such as grazing, may result in the removal of leaves, inflorescences, or seeds from the maternal plant. Studies have shown that partial defoliation of the maternal plant may lead to a decrease (107, 156) in mean seed weight, to no effect (100, 182), or to an increase (187). Sometimes a more intense defoliation may increase rather than reduce mean seed weight (105). Leaf removal may affect carbohydrate supply and may also have major effects on hormonal and nutrient supply and on translocation patterns. The removal of flowers or developing seeds has often been shown to increase seed size (48, 59, 108), most probably by removing reproductive sinks.

While in many cultivated species the seed concentration of different minerals is markedly affected by the external supply to the parent plant (117), in wild plants the elemental composition of seeds seems to remain relatively stable. In Senecio sylvaticus (167) and in Senecio vulgaris (53), seeds produced by plants grown in a range of nutrient treatments maintained remark- ably constant mineral nutrient concentration; so did seeds of Grevillea leucopteris collected from plants grown in a wide variety of soil types (84). In Abutilon theophrasti, five minerals were tested; only nitrogen concentration showed a significant increase in the seed in response to an increase in parental nutrient status (125). These results suggest that, in species not artificially selected, seed quality may be relatively buffered against the variation in parent supply. Given that nutrient supply to the maternal plant may affect not only seed chemistry but also seed coat structure and hormone content (64), and given that nitrogen in seeds is stored mainly in the form of proteins, several of which may have a major role as defense against predators (118), more detailed studies are needed on the response of noncultivated species to the nutrient supply to the maternal plant.

There is some evidence that nutrient treatments applied to the maternal plant can influence the nutritional quality of seeds, and that genotypes vary in

218 ROACH & WULFF

response to this treatment. In a study of the effect of foliar urea sprays on grain protein percentage and grain yield, Altman et al (4) found an increase in percentage protein in the seed with increased nitrogen application. They also found a maternal genotype by nitrogen treatment interaction, suggesting this type of maternal effect has both a genetic and an environmental component.

DORMANCY AND GERMINATION

Genetic studies The primary control of seed dormancy and germination is through the maternal tissues surrounding the embryo (109). In particular, control is via the seed coat (93) or other structures such as the lemma and palea (82). A maternal effect on germination may also occur via an endosperm dosage effect (Figure 1), because the endosperm, which contains a larger maternal than paternal component, contains a number of enzymes important for germination (43, 72). Garbutt & Witcombe (60) showed, in Sinapis arvensis, that the seed coat (of maternal origin) controls dormancy. The embryo genotype only affects dormancy when there is a nondormant seed coat type. No study has ever addressed the relative importance of maternal tissues and endosperm to germination patterns.

Genetic studies have shown a large maternal effect on germination percentage in Zea mays (43) and Anthoxanthum odoratum (145). In studies with Dactylis (123) and Lolium perenne (76), maternal effects found for germination percentage were due perhaps to cytoplasmic or cytoplasmic interaction effects, but in neither case were multiple generation studies done to confirm this. Reciprocal differences for seed longevity in soybeans are due to noncytoplasmic maternal effects, for the differences decreased in later generations (96).

In addition to influencing the rate or timing of germination, maternal effects can also influence the sensitivity of seeds to environmental conditions. In a study with Zea mays, a maternal effect was found for sensitivity to cold during germination (17).

Environmental studies Seeds of different populations or geographical origin have often been found to vary in germination requirements and in degree of dormancy (11, 40, 113, 127, 129, 168). For example, in a study on Poa trivialis, Hilton et al (81) found that the germination response to red/far-red ratios was related to the light quality to which the seeds were exposed during maturation in their natural habitats. Microclimate and site may also be important determinants of seed germination patterns. In a study of germination inhibition, in Chenopodium bonus-henricus, Dorne (40) showed that whereas the excised embryo was never dormant, germination of intact seeds was dependent on seed coat thickness. The seed coat became thicker and


contained more polyphenols with increasing elevation, and this was reflected in reduced germination. Moreover, plants transplanted to different elevations showed a direct influence of the new environment on seed coat inhibition of germination. Common garden experiments suggest that much of the variation in germination requirements among populations may be environmentally induced (40, 121, 127). But the importance of this to within-population variation in seed dormancy is not clear because few studies have been done in natural populations (but see 87).

The effects of specific environmental conditions on seed germination requirements have been recently reviewed (64-66). As a general rule, the lower the temperature during seed development, the higher the levels of dormancy (130, 168) during the seed maturation period (139); this is also true if applied only during vegetative development (141). Generalizations about the effects of maternal temperatures on seed germination are difficult, however, because there may be considerable genetic variability in the response to maternal conditions. When clones of Plantago lanceolata were grown to maturity at two different thermoperiods, the overall effect of higher maternal temperature was a decrease in seed weight and an increase in the rate and percentage of germination. However, seed families differed in their germination response to maternal temperatures (as indicated by significant interactions between family and maternal treatment) as well as in the degree to which the response to germination temperature depends on the temperature conditions during seed maturation (as indicated by significant three-way interactions between family and germination temperature and maternal temperature (3). The existence of genetic variability in the response to maternal temperatures was also shown for pure lines of wild oats (138) and for different wheat genotypes (128).

Daylength and light quality during seed development have been found to affect germination in several species (reviewed by 65, 66), and the photoperiodic treatments have been found to be most effective during the later stages of seed development. Light quality effects are most probably mediated by the phytochrome system. For example, in Arabidopsis thaliana, exposure of plants during seed development to light with a low red/far-red ratio resulted in seeds with low germination percentage in the dark, while exposure to light with a high red/far-red ratio resulted in seeds with high dark germination percentage (62, 111). This suggests that the active form of phytochrome, induced by the light treatment during seed development, persists and acts in the dry seed. These effects are probably perceived by the developing seed itself. When developing buds are selectively illuminated with a fiber light, the receptor for the red light stimulus is shown to be localized in the developing seed and not in the vegetative parts of the plant (62). Even in vitro cultured ovules are sensitive to red and far-red light (163). Since light transmitted by chlorophyll-containing tissues will be enriched at the far-red end of the

220 ROACH & WULFF

spectrum (152), seeds located in different portions of the inflorescence or the canopy may be exposed to different red/far-red ratios during development. The light-filtering properties of the maternal tissues surrounding the seeds could be responsible for this light sensitivity. In an extensive study of many different species, Cresswell & Grime (35) found that the chlorophyll content of the investing structures was negatively correlated with the capacity of seeds to germinate in the dark.

The effects of maternal nutrient supply and hormone level on dormancy and germination have been recently reviewed (64, 65). Although for many species, a positive correlation is found between increased nutrient supply and germination percentage, an increase in nitrogen fertilization can result in an accumulation of germination inhibitors in the fruits (86). The effects of growth substances vary according to the time of application and often interact with other environmental factors such as photoperiod (68). The interpretation of these effects is difficult because we know little about what fraction of these hormones are translocated from the mother plant, what fraction is synthesized in the seed itself, and how growth substances are degraded during seed drying (12).

Many other environmental factors may affect seed germination. For example, exposure of the parent plants to drought stress during seed development decreased the duration of primary dormancy in wild oats (140), and growth of Plantago lanceolata under elevated atmospheric CO2 con- centrations increased germination percentages ( 186). In both studies however, considerable variation occurred in the responses among families, suggesting that genetic variability in the response of seed germination to maternal environmental conditions may be widespread.

Many of the environmental effects on seed dormancy could be due to changes in the structure or permeability of the seed coats. Photoperiodic treatments had a significant effect on the permeability of Ononis sicula seeds (67), and the addition of minerals and growth substances has been found to alter seed coat structure in several species (reviewed by 64). In a study with soybeans, Nooden et al (122) found that seed coat permeability was increased by the addition of minerals and cytokinins. Since drought decreases the production of cytokinins in the root and mineral flux to the shoot (5), water stress may induce the production of more impermeable seeds. Variation in other accessory seed structures has been less studied, but it is known that pappus length in Leontodon hispidus is altered by seasonal changes in the environment (58).

Given the numerous effects of maternal environmental conditions on seed dormancy, it is not surprising that the timing of dispersal influences seed germination requirements. During the growing season, environmental conditions change, and this is reflected by a change in the quality of offspring


produced at different times (8, 136). In Frasera caroliniensis, for example, seeds that overwintered on the parent plant required warm stratification in addition to the cold stratification required by seeds collected earlier in the season (9). As a result, in late maturing seeds, germination was spread over several seasons.

WITHIN-PLANT EFFECTS ON SEED SIZE, DORMANCY, AND GERMINATION

Single plants may produce seeds differing in size and germination requirements. These effects range from the production of clearly dimorphic seeds such as the aerial and subterranean achenes in Emex spinosa (176), or the achenes produced by disk and ray flowers in many Compositae, to a continuous variation in seed size associated with position of a seed on a mother plant during development. Positional effects and their effects on seed structure and dormancy have recently been reviewed (64, 65, 148). In the classic example of Aegilopsis ovata, Datta et al (37) found that the grains produced in the upper portions of the spikelet were more dormant and weighed less than those produced in the lower portions of the spikelet. Similar effects have been described for Rumex (19, 107, 108). More recent examples include the variability in structure, germination requirements, and dispersal ability of ray and disk achenes in Heterotheca latipholia (171), the differences in size and germination requirements between aerial and subterranean propagules in Amphicarpea bractata (146), and the variability in size and dormancy of seeds produced at different positions in the umbel in Pastinaca sativa (79). It has been suggested that within-plant variability in seed size may be affected by the timing of fertilization or by the number of competing ovules per fruit (110). Silvertown (148) has proposed that the differential rates of ripening of the embryo and enveloping structures (somatic heterochrony) could account for many of the polymorphisms observed within plants.

As much as an eight-fold variation in seed weight was observed in single plants of Lomatium gravi (162), almost a six-fold variability in Raphanus raphanistrum (155), and about a two-fold variation in Pastinaca sativa (79) and in Desmodium paniculatum (187). In the latter species, within-plant variability is affected by nutrient supply. Seed size has often been found to vary with position on the plant or the infrutescence, as for example in Impatiens capensis (172), in wheat (132) and in many Umbelliferae (79), and with position in the fruit (155). This variation of seed weight with position in the pod is commonly found in legumes (142, 187) and is sometimes associated with variation in mineral content (83).

In summary, within-plant variation in seed size and dormancy emphasizes the sensitivity of these traits to environmental variation. Controlled environ-

222 ROACH & WULFF

ment studies have identified specific environmental factors that influence seed size and dormancy, but the importance of these specific environmental factors to variation in natural populations is not clearly understood.

Maternal Effects on Later Life Traits

SEEDLINGS

Genetic and environmental studies A large number of studies have been done with Lolium perenne, and the results showed that maternal effects can have a substantial influence on an individual's phenotype at the early seedling stage, and that these effects diminish over time (10, 44, 76-78, 159, 161). Up to the third leaf stage, leaf number, leaf size, and tiller number in L. perenne were predominantly under maternal control. At the fifth leaf stage, maternal effects were not present, or they were combined with offspring genetic effects. Similar studies with Dactylis have shown maternal effects for seedling growth rate, leaf area, and tiller number (123, 124). In these studies, cytoplasmic effects or interactions between cytoplasmic and nuclear effects were suggested as the cause of these maternal influences.

Cytoplasmic maternal effects on seedlings were identified in an experiment with Arabidopsis using male testers in crosses with reciprocal F, hybrids (31). Results indicated large and persistent maternal effects for seedling root length and plant weight, suggesting that these effects were due to cytoplasmic influences.

A number of studies have shown an indirect maternal effect on seedling size via seed size (1, 98, 104, 143, 154, 188). A positive correlation between seed and seedling size is evidence for a maternal effect in species for which seed size is under maternal control. In a study with tobacco, Van Sanford & Matzinger (169) suggested that the stability of seedJing weight over several environments was consistent with an indirect maternal effect via seed size. In other words, because of the dependence of early seedling growth on the materials stored in the seed, maternal effects on the seed had a larger influence than the immediate environment in determining the early juvenile phenotype. In a similar way, reciprocal differences in alfalfa for seedling height and forage yield were largely attributable to the correlation between seed size and the photosynthetic area of seedlings (18). In studies such as these, it is not possible to distinguish between genetic and environmental maternal effects because maternal genotypes were not randomized over environments. Although he could not completely deconfound genetic and environmental effects, using Phalaris tuberosa Latter (98) found that genetic and persistent environmental maternal effects on seed size subsequently influenced seedling weight and growth per tiller. Environmental maternal effects on seed size, on the other hand, influenced the time to emergence of


leaves and tillers and also seedling tiller number. Latter suggested that qualitative differences may exist between genetic and environmental effects of seed size: Whereas the genetic maternal effects might depend on differences in the levels of endogenous gibberellins and auxins, the environmental maternal effects may influence nutrient level and differences in embryo size (98).

Maternal effects may differ among even closely related species. In Lolium perenne, large genetic maternal effects were found for the rate of leaf appearance (44). In L. multiflorum, however, no maternal effect was found for this trait despite a maternal effect on leaf size (45). In the study with L. multiflorum, maternal effects contributed to variation in third leaf size, due to additive genetic maternal effects on leaf length and maternal interaction effects on leaf width. The pattern of maternal effects in this species was similar to studies with other Lolium species in that maternal effects were found for early leaf size but were absent at the sixth leaf stage.

Environmental maternal effects may also have a significant influence on the seedling phenotype. In Plantago lanceolata, exposure of the parent plant to different CO2 levels and temperature regimes affected seedling sizes and growth rates. However, families differed in both the extent and the direction in which seedling development was affected by maternal treatments (3, 186). The relationship between maternal treatments and seedling response is not always straightforward: In Senecio vulgaris the nutrient requirements of seedlings did not correlate with the nutrient conditions during seed maturation or with the nutrient content of the seeds (54).

There have been very few quantitative genetic studies of maternal effects for seedlings in natural populations. A study with G. carolinianum showed no evidence for maternal effects on seedling traits (135). Similarly, there were no maternal effects beyond germination in Anthoxanthum odoratum (145).

In general, relative to the number of maternal environmental studies done at the seed stage, few have considered the influence of specific environmental factors during the maternal generation on seedling traits, particularly in noncultivated species.

ADULTS

Genetic and environmental studies Several studies showing reciprocal differences for yield components in cultivated plants have been reviewed by Aksel (2). Singh & Murty (150) also found reciprocal differences in Brassica campestris for a number of yield characters including length of the fruit and yield per row. In their study, differences between reciprocal crosses were influenced by the environment, suggesting that some mothers were better able to exploit favorable conditions. Maternal effects have also been found for the probability of flowering and for the number of inflorescences in L. perenne

224 ROACH & WULFF

(74), and also for adult plant height in Nicotiana rustica (89). In some studies, yield components show no maternal effect (95).

One of the best-known examples of maternal cytoplasmic inheritance and its influence on adult characters is male sterility. Since this has been the object of numerous studies and reviews (33, 69), and probably represents a distinct phenomenon, we do not consider it here.

Maternal effects on adult traits may be indirect via seed size effects (39, 175). For example, Stanton (154) found a positive correlation between seed size and adult reproductive output in Raphanus raphanistrum. The influence of seed size on yield components may depend on environmental conditions. In a study with Austrian winter field pea, Murray et al (119) found that the yield of peas established from small-sized seed was significantly lower than the yield of peas from large- or medium-sized seed under cool, wet conditions. When the environmental conditions were not adverse but rather were favorable for pea growth, there were no differences in yield associated with seed size.

Maternal effects on adults may also be indirect via other earlier effects. For example, in Lolium multiflorum, maternal effects on adult tiller number were explained by the observation that earlier in the life cycle, tiller number is affected by maternal influences such as seed reserves and hormonal effects. And, by the nature of the tillering process, maternally caused early differences can carry over to the adult stage. Furthermore, since the number of inflorescences was related to the number of tillers, maternal effects on inflorescence number may also have been due to an earlier nutritional effect (45).

An indirect maternal effect may also occur due to variation in seed chemical composition, produced by fertilization treatments. For example, in Phaseolus vulgaris nitrogen fertilization increased protein content and seed size, but smaller seeds with higher protein content produced higher yielding plants than did the larger ones (133). In noncultivated species, seed composition seems to remain relatively stable; in Abutilon theophrasti, however, seeds that differed only in nitrogen content produced plants that differed in their competitive abilities (125).

Studies with Lolium perenne have shown inconsistent results even for the single trait-flowering time. Thomas (159) found that time of flowering was under genetic control of the individual and showed no maternal control between populations. However, Hayward (74) found both additive genetic control and a substantial maternal effect. Of the total variation in time, 20% of flowering in Hayward's study was under maternal control. Further studies by Hayward and colleagues (77, 78) using a within-population diallel analysis also showed a degree of maternal control for time of flowering. However, in Lolium multiflorum, the only adult trait for which there were no reciprocal


differences was flowering time (45). Flowering time has also demonstrated a maternal effect in other species, including Nicotiana (89) and Brassica (150), but it shows no maternal effect in Safflower (94) or in Melandrium album (99).

In maize, maternal cytoplasmic effects have been found for adult plant height and ear height (61). For some yield characters in this species, an interaction of cytoplasmic effects with the genotype and environment of the offspring have also been demonstrated (56). The percentage of oil and protein content of maize kernels showed a reciprocal effect which was not consistent over two generations (61). Garwood et al (61) suggested that this was due to a physiological influence (phenotypic maternal effect) rather than a cytoplasmic effect.

PATERNAL EFFECTS

Passing reference has been made a number of times to paternal effects (i.e. an additional contribution of the paternal parent to the phenotype of the offspring beyond the nuclear zygotic contribution). These effects have been found, for example, for seed size in corn (102), soybean (90), wheat (13), and pearl millet (15, 16). In a series of crosses with maize, Fleming (55) demonstrated that male cytoplasm can influence the hereditary expression of yield characters in progeny, but these effects may be influenced by the maternal cytoplasm and by yearly interactions between cytoplasmic and environmental effects. A few plant groups, such as Oenothera and Geranium, show persistent paternal cytoplasmic inheritance (reviewed by 164). Paternal effects in Geranium have recently been confirmed in a study in a natural population (135). The existence of these effects is important for the interpretation of cytoplasmic studies, and it cautions against the assumption that any and all reciprocal differences are due to maternal effects. It is important, therefore, to test the relative importance of maternal or paternal influences (165).

DISCUSSION

The general pattern which has emerged to date is that at the seed stage, a large proportion of the variation is under maternal control, and this maternal control appears to have a large environmental component. These effects carry through to the early seedling stages, but at the late seedling stage, the genotype of the offspring itself begins to contribute significantly to the variation. Endosperm maternal effects and most phenotypic maternal effects have their major influence via the seed or seed structure. Cytoplasmic inheritance is the only mechanism for direct maternal effects on adult traits, although there may be indirect carryover effects from the seed or seedling stage. It is not surprising

226 ROACH & WULFF

therefore that the influence of maternal effects diminishes later in the life cycle. Because maternal effects at the adult stage may be important, they cannot be ignored in breeding programs, and they may have important consequences for fitness in natural populations.

This review of the evidence has revealed two large gaps in the types of studies done on maternal effects. First, a detailed separation of the causes of maternal effects still needs to be done. As outlined in Figure 1, there are, beyond the maternal zygotic contribution, several ways in which the maternal parent can influence the juvenile phenotype. With few exceptions, these effects have not been separated, and thus, the exact cause of the differential contribution from the maternal parent is not known.

The second discontinuity in our review is the lack of studies on noncultivated species in natural populations. Studies in natural populations have demonstrated that environmental variables can have an important influence on seed size and germination, there have been few genetic studies, however, and no conclusive identification has been made of the specific causes of the maternal effects.

In 1963, Cockerham (26) suggested that maternal effects in plants were minimal and did not generally require consideration. From the evidence presented here it is clear that maternal effects can have a significant effect on the phenotype of an individual. Therefore, for many types of evolutionary and ecological studies it will be important to consider this type of variation. Failure to consider the contribution of maternal effects to the phenotype of individuals can lead to erroneous interpretations of experimental results. This was clearly demonstrated in a series of studies with Lolium perenne. In the first study, without reciprocals, Hayward & Breese (75) found that for certain traits there were high levels of dominance and interaction. However, a later study using a full diallel analysis showed reciprocal differences for these same traits and demonstrated that the earlier results were a reflection of a high maternal component (58). Quantitative studies designed to identify maternal effects clearly can increase our ability to understand processes within plant populations.

Unfortunately, it may be difficult to predict the importance of maternal effects for a particular species. Studies have shown that for closely related species, and even within one species, there are no consistent patterns of maternal effects for the same trait (44, 45). Two studies with Lolium perenne showed the mean values of seed weight to be exclusively under maternal control (10, 157); but in a later study with the same species, seed weight showed no maternal effect, only additive genetic control (160). There is no reason to expect that the same controls should operate in different populations of a species, or in similar populations in dissimilar environments (161). Different species, and different individuals within a population, may react differently to the same maternal environmental treatments, for example, via


interactions between maternal effects and progeny genotype (3, 4, 105). Thus, generalizations about maternal effects across populations or even across genotypes are not easy.

One of the difficult questions in ecological or quantitative genetic studies in natural populations is how to study maternal effects. Very often one does not have the time or facilities to do the crosses required for complete genetic analysis of these effects. As an alternative, seed weight is often used as an estimate of maternal effects in ecological (143) and agricultural studies (1, )66). A number of experimental studies (cited earlier in this paper) have demonstrated that changing the environment of the mother has a significant effect on the size of the seed produced. It is assumed that if there is a correlation between seed weight and traits expressed later in the life cycle, then there is evidence for maternal effects (143). Sometimes mean seed size is highly correlated with maternal ability (97, 112). However, this may not always be the case. In studies using seed weight as an estimate of maternal effects, it must be recognized that maternal influences will be underestimated because this technique ignores other causes of maternal effects, including nutritional differences and cytoplasmic inheritance (Figure 1). Some studies have shown significant maternal effects on traits despite the absence of any correlation with seed size (29, 43, 159). Moreover, the effect of seed size is often confined to the early growth stages (103, 158); therefore, seed weight cannot be used to estimate maternal effects for late-life traits.

Environmental studies, done under controlled experimental conditions, have clearly demonstrated that phenotypic maternal effects can be caused by a number of different environmental factors. Seed size, for example, has shown a sensitivity to maternal temperature, water availability, resource availability, and hormone level. These environmental conditions will fluctuate during a growing season, and the importance of these factors may be reflected in the variation in seed weight observed within a growing season (20, 58, 59, 136). The importance of this variation may be similarly reflected in within-plant positional effects on seed size, when seeds in different positions are exposed to different levels of resources (1 10). Whereas studies in a controlled environment can identify one particular maternal environmental factor which may have an influence on the juvenile phenotype, it is hard to make the link between controlled and field experiments because it is difficult to identify the small-scale heterogeneity perceived by an individual plant in the field. It has been shown that small-scale heterogeneity can be important in field studies (70, 71, 135). Not only is this scale of environmental heterogeneity hard to measure, but the relevant scale of heterogeneity may change for different stages of the life cycle (135). Experiments need to be done to identify precisely the environmental causes and consequences of maternal effects under natural conditions.

It is clear from this review that maternal effects can confuse the interpreta-

228 ROACH & WULFF

tion of genetic studies (1 16). When maternal half-sibships are used in quantitative genetic studies, maternal effects will yield biased estimates of heritability (51) and may lead one to conclude falsely that there is heritable variation in a population. A false prediction concerning the response to selection may also occur for the opposite reason. In an experimental study with mice, Falconer (52) found a strong response to selection for litter size despite zero heritability for this trait. Further examination of this trait revealed a strong maternal effect, which explained his observed results. Simple maternal effects will always inflate variation between families while having no effect on variances within families. However, the variance within families will be inflated if there is an interaction between progeny genotype and maternal effect (106). The type of maternal effect (Figure 1), the covariance between maternal and offspring effects (38, 170, 178), and the persistence of these effects through successive generations (3, 134, 179) will all influence the interpretation of selection studies. In addition to the need for more experimental work to identify these effects, more theoretical analysis of the evolutionary significance of maternal effects and maternal interaction effects is needed.

As a consequence of maternal effects, not only does the maternal parent have a greater influence than the paternal parent on the offspring phenotype, but the maternal phenotype may for some traits also have a greater influence than the offspring on the offspring's own phenotype. For example, seed germination appears to be almost exclusively under maternal control, via the seed coat or other structures (references cited earlier). A conflict between the parent and offspring may develop: while for an individual offspring it is always advantageous to germinate early, the parental genotype may favor a delay in germination in order to reduce offspring competition (50) or to ensure success of offspring in a temporally heterogeneous environment (177). The evolution of the integuments and endosperm has also been discussed as a mechanism that allows mothers increased control over the distribution of maternal investment to embryos, because the mother can respond to differences in vigor of early growth among offspring genotypes (178). It is clear, that maternal effects mny have had important cansequences during the evofu- tion of many traits and may be critical to our understanding of ecological and genetic mechanisms in present-day populations.

ACKNOWLEDGMENTS

We would like to thank H. M. Alexander, J. Antonovics, M. Hayward, A. Lubbers, M. Price, and J. Schmitt, for their constructive comments on earlier drafts of this paper. We would also like to thank A. Winn for many helpful discussions with us on this subject. This paper was written while R. D. Wulff was on leave of absence from the Universidad Central de Venezuela; she was


supported in part by a grant from Consejo de Desarrollo Cientifico y Human- istico of the Universidad Central de Venezuela, Caracas. Special thanks to A. Herrera whose generous cooperation, in part, made this leave possible. D. A. Roach was supported by NIH National Research Service Award F32- AG05376 from NIA during this time.

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