Effects of inbreeding on male function and self-fertility in the partially self-incompatible herb Campanula rapunculoides (Campanulaceae)

We examined the effect of inbreeding on fitness (through both male and female functions) and changes in self-fertility in the partially self-incompatible species Campanula rapunculoides. Individuals in natural populations of C. rapunculoides varied extensively in their strength of self-incompatibility (SI). We crossed 11 individuals that differed in their strength of SI to generate families with four levels of inbreeding (f = 0.0, 0.25, 0.5, and 0.75). Progeny were scored for three traits related to male fitness and for outcrossed and selfed seed production. Analyses of variance revealed significant inbreeding depression for the three male traits and seed set. Families with strong or weak SI differed in their response to inbreeding. Families with weak SI had lower levels of inbreeding depression for most traits than families with strong SI, but strong SI families had a greater increase in selfed seed set, but not self-fertility, with inbreeding. Finally, we found evidence of a significant linear response to inbreeding for all three male reproductive traits and outcrossed seed, indicating that inbreeding depression was primarily caused by partially or fully recessive deleterious alleles. Variation in genetic load was associated with variation in self-fertility, a finding that suggests an evolutionary role for partial self-fertility in natural populations of C. rapunculoides.     

Parental genetic distance and patterns in nonrandom mating and seed yield in predominately selfing Arabidopsis thaliana

In this study, we ask two questions: (1) Is reproductive success independent of parental genetic distance in predominately selfing plants? (2) In the absence of early inbreeding depression, is there substantial maternal and/or paternal variation in reproductive success in natural populations? Seed yield in single pollinations and proportion of seeds sired in mixed pollinations were studied in genetically defined accessions of the predominately selfing plant Arabidopsis thaliana by conducting two diallel crosses. The first diallel was a standard, single pollination design that we used to examine variance in seed yield. The second diallel was a mixed pollination design that utilized a standard pollen competitor to examine variance in proportion of seeds sired. We found no correlation between reproductive success and parental genetic distance, and self-pollen does not systematically differ in reproductive success compared to outcross pollen, suggesting that Arabidopsis populations do not experience embryo lethality due to early-acting inbreeding or outbreeding depression. We used these data to partition the contributions to total phenotypic variation from six sources, including maternal contributions, paternal contributions and parental interactions. For seed yield in single pollinations, maternal effects accounted for the most significant source of variance (16.6 %). For proportion of seeds sired in mixed pollinations, the most significant source of variance was paternal effects (17.9 %). Thus, we show that population-level genetic similarities, including selfing, do not correlate with reproductive success, yet there is still significant paternal variance under competition. This suggests two things. First, since these differences are unlikely due to early-acting inbreeding depression or differential pollen viability, this implicates natural variation in pollen germination and tube growth dynamics. Second, this strongly supports a model of fixation of pollen performance genes in populations, offering a focus for future genetic studies in differential reproductive success.     

VARIATION IN SEED CHARACTERS IN NEMOPHILA MENZIESII: EVIDENCE OF A GENETIC BASIS FOR MATERNAL EFFECT

A growing body of evidence indicates that phenotypic selection on juvenile traits of both plants and animals may be considerable. Because juvenile traits are typically subject to maternal effects and often have low heritabilities, adaptive responses to natural selection on these traits may seem unlikely. To determine the potential for evolutionary response to selection on juvenile traits of Nemophila menziesii (Hydrophyllaceae), we conducted two quantitative genetic studies. A reciprocal factorial cross, involving 16 parents and 1960 progeny, demonstrated a significant maternal component of variance in seed mass and additive genetic component of variance in germination time. This experiment also suggested that interaction between parents, though small, provides highly significant contributions to the variance of both traits. Such a parental interaction could arise by diverse mechanisms, including dependence of nuclear gene expression on cytoplasmic genotype, but the design of this experiment could not distinguish this from other possible causes, such as effects on progeny phenotype of interaction between the environmental conditions of both parents. The second experiment, spanning three generations with over 11,000 observations, was designed for investigation of the additive genetic variance in maternal effect, assessment of paternal effects, as well as further partitioning of the parental interaction identified in the reciprocal factorial experiment. It yielded no consistent evidence of paternal effects on seed mass, nor of parental interactions. Our inference of such interaction effects from the first experiment was evidently an artifact of failing to account for the substantial variance among fruits within crosses. The maternal effect was found to have a large additive genetic component, accounting for at least 20% of the variation in individual seed mass. This result suggests that there is appreciable potential for response to selection on seed mass through evolution of the maternal effect. We discuss aspects that may nevertheless limit response to individual selection on seed mass, including trade-offs between the size of individual seeds and germination time and between the number of seeds a maternal plant can mature and their mean size.     

PARENTAL EFFECTS ON SEED DEVELOPMENT AND SEED YIELD IN RAPHANUS RAPHANISTRUM: IMPLICATIONS FOR NATURAL AND SEXUAL SELECTION

The possibility that sexual selection operates in angiosperms to effect evolutionary change in polygenic traits affecting male reproductive success requires that there is additive genetic variance for these traits. I applied a half-sib breeding design to individuals of the annual, hermaphroditic angiosperm, wild radish (Raphanus raphanistrum: Brassicaceae), to estimate paternal genetic effects on, or, when possible, the narrow-sense heritability of several quantitative traits influencing male reproductive success. In spite of significant differences among pollen donors with respect to in vitro pollen tube growth rates, I detected no significant additive genetic variance in male performance with respect to the proportion of ovules fertilized, early ovule growth, the number of seeds per fruit, or mean individual seed weight per fruit. In all cases, differences among maternal plants in these traits far exceeded differences among pollen donors. Abortion rates of pollinated flowers and fertilized ovules also differed more among individuals as maternal plants than as pollen donors, suggesting strong maternal control over these processes. Significant maternal phenotypic effects in the absence of paternal genetic or phenotypic effects on reproductive traits may be due to maternal environmental effects, to non-nuclear or non-additive maternal genetic effects, or to additive genetic variance in maternal control over offspring development, independent of offspring genotype. While I could not distinguish among these alternatives, it is clear that, in wild radish, the opportunity for natural or sexual selection to effect change in seed weight or seed number per fruit appears to be greater through differences in female performance than through differences in male performance.     

PATERNAL CARE: DIRECT AND INDIRECT GENETIC EFFECTS OF FATHERS ON OFFSPRING PERFORMANCE

Knowledge of how genetic effects arising from parental care influence the evolution of offspring traits comes almost exclusively from studies of maternal care. However, males provide care in some taxa, and often this care differs from females in quality or quantity. If variation in paternal care is genetically based then, like maternal care and maternal effects, paternal effects may have important consequences for the evolution of offspring traits via indirect genetic effects (IGEs). IGEs and direct–indirect genetic covariances associated with parental care can contribute substantially to total heritability and influence predictions about how traits respond to selection. It is unknown, however, if the magnitude and sign of parental effects arising from fathers are the same as those arising from mothers. We used a reciprocal cross‐fostering experiment to quantify environmental and genetic effects of paternal care on offspring performance in the burying beetle, Nicrophorus vespilloides. We found that IGEs were substantial and direct–indirect genetic covariances were negative. Combined, these patterns led to low total heritabilities for offspring performance traits. Thus, under paternal care, offspring performance traits are unlikely to evolve in response to selection, and variation in these traits will be maintained in the population despite potentially strong selection on these traits. These patterns are similar to those generated by maternal care, indicating that the genetic effects of care on offspring performance are independent of the caregiver's sex.     

Quantitative genetics of seed size variation inPhlox

Summary Because seed size is often associated with survival and reproduction in plant populations, genetic variation for seed size may be reduced or eliminated by natural selection. To test this hypothesis we assessed genetic sources of variation in seed size in a population ofPhlox drummondii to determine whether genetic differences among seeds influence the size they attain. A diallel cross among 12 plants from a population at Bastrop, Texas, USA allowed us to partition variance in the mass of seeds among several genetic and parental effects. We found no evidence of additive genetic variance or dominance genetic variance for seed mass in the contribution of plants to their offspring. Extranuclear maternal effects accounted for 56% of the variance in seed mass. A small interaction was observed between seed genotype and maternal plant. Results of this study support theory that predicts little genetic variation for traits associated with fitness.     

The effect of maternal and paternal environments on seed characters in the herbaceous plant Campanula Americana (Campanulaceae)

Maternal environments typically influence the phenotype of their offspring. However, the effect of the paternal environment or the potential for joint effects of both parental environments on offspring characters is poorly understood. Two populations of Campanula americana, a woodland herb with a variable life history, were used to determine the influence of maternal and paternal light and nutrient environments on offspring seed characters. Families were grown in the greenhouse in three levels of light or three levels of nutrients. Crosses were conducted within each environmental gradient to produce seeds with all combinations of maternal and paternal environments. On average, increasing maternal nutrient and light levels increased seed mass and decreased percentage germination. The paternal environment affected seed mass, germination time, and percentage germination. However, the influence of the paternal environment varied across maternal environments, suggesting that paternal environmental effects should be evaluated in the context of maternal environments. Significant interactions between family and the parental environments for offspring characters suggest that parental environmental effects are genetically variable. In C. americana, the timing of germination determines life history. Therefore parental environmental effects on germination timing, and genetic variation in those parental effects, suggest that parental environments may influence life history evolution in this system.     

The role of maternal and paternal effects in the evolution of parental quality by sexual selection

Genetic models of maternal effects and models of mate choice have focused on the evolutionary effects of variation in parental quality. There have been, however, few attempts to combine these into a single model for the evolution of sexually selected traits. We present a quantitative genetic model that considers how male and female parental quality (together or separately) affect the expression of a sexually selected offspring trait. We allow female choice of males based on this parentally affected trait and examine the evolution of mate choice, parental quality and the indicator trait. Our model reveals a number of consequences of maternal and paternal effects. (1) The force of sexual selection owing to adaptive mate choice can displace parental quality from its natural selection optimum. (2) The force of sexual selection can displace female parental quality from its natural selection optimum even when nonadaptive mate choice occurs (e.g. runaway sexual selection), because females of higher parental quality produce more attractive sons and these sons counterbalance the loss in fitness owing to over-investment in each offspring. (3) Maternal and paternal effects can provide a source of genetic variation for offspring traits, allowing evolution by sexual selection even when those traits do not show direct genetic variation (i.e. are not heritable). (4) The correlation between paternal investment and the offspring trait influenced by the parental effects can result in adaptive mate choice and lead to the elaboration of both female preference and the male sexually selected trait. When parental effects exist, sexual selection can drive the evolution of parental quality when investment increases the attractiveness of offspring, leading to the elaboration of indicator traits and higher than expected levels of parental investment.     

PLANTING DENSITY INFLUENCES THE EXPRESSION OF GENETIC VARIATION IN SEED MASS IN WILD RADISH (RAPHANUS SATIVUS L.: BRASSICACEAE)

To determine the effects of density, genotype, and their interaction on individual seed mass in Raphanus sativus L., we replicated maternal and paternal families of seed across two planting densities in an experimental garden. Seeds were produced by a nested breeding design performed in the greenhouse. Among garden-raised plants, density had a strong negative effect on the mass of seeds produced. At low density, the identity of the greenhouse-grown maternal plants had a strong effect on F₂ seed mass, while in high-density plots, there were no significant parental effects on mean seed mass. Significant parental genotype density interactions contributed to variation in F₂ seed mass. Norms of reaction for each of the 15 paternal sibships illustrate paternal family density interactions. Three sibships exhibited significant declines in mean seed mass with increasing density; 12 sibships showed no change. Maternal family density interaction effects on seed mass were also detected; among maternal sibships, mean seed mass at low density was negatively correlated with mean seed mass at high density. These results demonstrate: a) planting density has a strong effect on mean individual seed mass produced by adults; b) density influences the magnitude of maternal effects on progeny phenotype; and c) genotype density interactions influence seed mass, potentially contributing to the maintenance of maternal genetic variation in seed mass in natural populations of wild radish.     

Models to estimate maternally controlled genetic variation in quantitative seed characters

Summary Estimating quantitative contributions to specific traits can be accomplished from a variety of genetic models (Mather 1949; Mather and Jinks 1971; Falconer 1981). Residual genetic effects, those beyond main and interaction effects of the embryo genotype, are often pooled under a single classification, termed maternal effects. Maternal contributions to seed-related traits can originate from various maternal sources (e.g., endosperm, testa and cytoplasm). Quantitative contributions of a maternal nature are not predictable from parental performance and effects are largely non-persistent over generations (Jinks et al. 1972). The methods used to determine maternal effects in quantitative traits often do not measure quantitative genetic parameters, while those that do are either complex or partially resolve potential contributions of individual sources of maternal effects. We present simple genetic models for estimating quantitative genetic parameters which take into account maternal effects expressed in the major seed tissues of higher plants.     

The relative importance of genetic and nongenetic inheritance in relation to trait plasticity in Callosobruchus maculatus

A trait's response to natural selection will reflect the nature of the inheritance mechanisms that mediate the transmission of variation across generations. The relative importance of genetic and nongenetic mechanisms of inheritance is predicted to be related to the degree of trait plasticity, with nongenetic inheritance playing a greater role in the cross‐generational transmission of more plastic traits. However, this prediction has never been tested. We investigated the influence of genetic effects and nongenetic parental effects in two morphological traits differing in degree of plasticity by manipulating larval diet quality within a cross‐generational split‐brood experiment using the seed beetle Callososbuchus maculatus. In line with predictions, we found that the more plastic trait (elytron length) is strongly influenced by both maternal and paternal effects whereas genetic variance is undetectable. In contrast, the less plastic trait (first abdominal sternite length) is not influenced by parental effects but exhibits abundant genetic variance. Our findings support the hypothesis that environment‐dependent parental effects may play a particularly important role in highly plastic traits and thereby affect the evolutionary response of such traits.     

Paternal but not maternal age influences early-life performance of offspring in a long-lived seabird

Variability in demographic traits between individuals within populations has profound implications for both evolutionary processes and population dynamics. Parental effects as a source of non-genetic inheritance are important processes to consider to understand the causes of individual variation. In iteroparous species, parental age is known to influence strongly reproductive success and offspring quality, but consequences on an offspring fitness component after independence are much less studied. Based on 37 years longitudinal monitoring of a long-lived seabird, the wandering albatross, we investigate delayed effects of parental age on offspring fitness components. We provide evidence that parental age influences offspring performance beyond the age of independence. By distinguishing maternal and paternal age effects, we demonstrate that paternal age, but not maternal age, impacts negatively post-fledging offspring performance.     

Paternal effects in Arabidopsis indicate that offspring can influence their own size

The existence of genetic variation in offspring size in plants and animals is puzzling because offspring size is often strongly associated with fitness and expected to be under stabilizing selection. An explanation for variation in seed size is conflict between parents and between parents and offspring. However, for this hypothesis to be true, it must be shown that the offspring genotype can affect its own size. The existence of paternal effects would support this hypothesis, but these have rarely been shown. Using a diallel cross among four natural accessions of Arabidopsis thaliana we show that maternal, paternal and positional effects jointly influence seed size, number and the frequency of seed abortion. We found that seed abortion (%) depends on the combination of maternal and paternal genotypes, suggesting the existence of mate choice or epistatic incompatibility among accessions of A. thaliana. In addition, since paternal genotype explains approximately 10 per cent of the variation in seed size, we propose that A. thaliana''s offspring must influence the amount of resources allocated to themselves. Identification of paternal effects in Arabidopsis should facilitate dissection of the genetic mechanisms involved in paternal effects.     

A model of triploid endosperm evolution driven by parent-offspring conflict

The parental investment in angiosperms comprises the endosperm, a nutrient reserve that is used during seed development. The endosperm contains genes from both parents. The most common endosperm form is the 3n Polygonum -type with more maternal genetic influence than paternal, i.e. with two maternal nuclei and one paternal nucleus. The evolutionary original state is thought to be a diploid endosperm with equal influence of the parents. We focus on the evolution of the triploid endosperm and show that a gene for triploid endosperm would have an initial advantage in a population of diploid endosperm type plants, and increase to fixation. We assume that endosperm amount is controlled by endosperm genes. Then a gene causing triploid endosperm will increase the influence of the mother plant on parental investment. The production of endosperm with two copies of the maternal genes will modify the inheritance of endosperm amount and cause an increased production of seeds.     

FERTILIZATION DYNAMICS AND PARENTAL EFFECTS UPON FRUIT DEVELOPMENT IN RAPHANUS RAPHANISTRUM: CONSEQUENCES FOR SEED SIZE VARIATION

Seed weight varies significantly within and among fruits of wild radish (Raphanus raphanistrum). To determine sources of this variation, we studied fertilization and seed development following controlled pollinations. Within fruits, central ovules were fertilized prior to distal ovules and attained greater seed size. Ninety-seven percent of the variation in mean seed wt per fruit was explained by an analysis of variance incorporating parental effects, pollination date, and the number of seeds per fruit. We document strong maternal effects on the number of ovules per ovary, the number of fertilized ovules per ovary, the number of seeds per fruit, and mean individual seed wt per fruit. Across females, pollen donor had a slight but significant effect on seed wt; no paternal effects on fertilization rate, zygote number, or seed number per fruit were detected. Within females, with one exception, pollen donor had no significant effect on these components of seed development. Stronger maternal main effects may be due to donor x recipient interactions, cytoplasmic factors, the genetic inequity within triploid endosperm, and/or strict maternal control over resource allocation. The large maternal effects relative to paternal effects may limit the rate at which natural selection acts on paternal traits expressed prior to seed maturation.     

Genetic variation, disequilibrium and natural selection on reproductive traits in Allium vineale

Bulbils and seeds collected from Allium vineale plants from natural populations were grown under uniform conditions. The bulbil-derived offspring represented the parental generation, whereas the seed-derived offspring represented the sexually produced offspring generation. Molecular markers were used to identify maternal genets. Variation in traits determining the allocation to sexual and asexual reproduction was partitioned among genets and ramet families in the parental and offspring generations. From observations of a release of genetic variation and slippage in the mean phenotype in the offspring generation, we inferred that there exists extensive genetic disequilibrium for reproductive traits in A. vineale populations, that most of the genetic variance is because of dominance effects, and that natural selection favours a reduced allocation to sexual reproduction. No genetic correlation between sexual and asexual allocation traits was found. We discuss the implications of these results with respect to the evolution of a mixed reproductive system in A. vineale.     

EFFECTS OF MATERNAL AND PATERNAL ENVIRONMENT AND GENOTYPE ON OFFSPRING PHENOTYPE IN SOLIDAGO ALTISSIMA L.

To predict the possible evolutionary response of a plant species to a new environment, it is necessary to separate genetic from environmental sources of phenotypic variation. In a case study of the invader Solidago altissima, the influences of several kinds of parental effects and of direct inheritance and environment on offspring phenotype were separated. Fifteen genotypes were crossed in three 5 × 5 diallels excluding selfs. Clonal replicates of the parental genotypes were grown in two environments such that each diallel could be made with maternal/paternal plants from sand/sand, sand/soil, soil/sand, and soil/soil. In a first experiment (1989) offspring were raised in the experimental garden and in a second experiment (1990) in the glasshouse. Parent plants growing in sand invested less biomass in inflorescences but produced larger seeds than parent plants growing in soil. In the garden experiment, phenotypic variation among offspring was greatly influenced by environmental heterogeneity. Direct genetic variation (within diallels) was found only for leaf characters and total leaf mass. Germination probability and early seedling mass were significantly affected by phenotypic differences among maternal plants because of genotype ( genetic maternal effects ) and soil environment ( general environmental maternal effects ). Seeds from maternal plants in sand germinated better and produced bigger seedlings than seeds from maternal plants in soil. They also grew taller with time, probably because competition accentuated the initial differences. Height growth and stem mass at harvest (an integrated account of individual growth history) of offspring varied significantly among crosses within parental combinations ( specific environmental maternal effects ). In the glasshouse experiment, the influence of environmental heterogeneity and competition could be kept low. Except for early characters, the influence of direct genetic variation was large but again leaf characters (= basic module morphology) seemed to be under stricter genetic control than did size characters. Genetic maternal effects, general environmental maternal effects, and specific environmental maternal effects dominated in early characters. The maternal effects were exerted both via seed mass and directly on characters of young offspring. Persistent effects of the general paternal environment ( general environmental paternal effects ) were found for leaf length and stem and leaf mass at harvest. They were opposite in direction to the general environmental maternal effects, that is the same genotypes produced “better mothers” in sand but “better fathers” in soil. The general environmental paternal effects must have been due to differences in pollen quality, resulting from pollen selection within the male parent or leading to pre- or postzygotic selection within the female parent. The ranking of crosses according to mean offspring phenotypes was different in the two experiments, suggesting strong interaction of the observed effects with the environment. The correlation structure among characters changed less between experiments than did the pattern of variation of single characters, but under the competitive conditions in the garden plant height seemed to be more directly related to fitness than in the glasshouse. Reduced competition could also explain why maternal effects were less persistent in the glasshouse than in the garden experiment. Evolution via selection of maternal effects would be possible in the study population because these effects are in part due to genetic differences among parents.     

CONSEQUENCES OF FLORAL VARIATION FOR MALE AND FEMALE REPRODUCTION IN EXPERIMENTAL POPULATIONS OF WILD RADISH,RAPHANUS SATIVUS L

We documented effects of floral variation on seed paternity and maternal fecundity in a series of small experimental populations of wild radish, R. sativus. Each population was composed of two competing pollen donor groups with contrasting floral morphologies and several designated maternal plants. Progeny testing with electrophoretic markers allowed us to measure paternal success. Realized fecundity by each maternal plant and the fraction of those seeds attributable to each pollen donor group were used as outcome variables in path analysis to explore relationships between floral characters (petal size, pollen grain number per flower, and modal pollen grain size), pollinator visitation patterns, and reproductive success. A wide range of pollinator taxa visited the experimental populations, and patterns of discrimination appeared to vary among them. The impact of visitation on male and female reproduction also varied among taxa; visits of small native bees significantly increased paternal success, while those of honey bees reduced male fitness. Only visits by large native bees had discernible effects on recipient fecundity, and, overall, fecundity was not limited by visitation. Maternal plants bearing large-petalled flowers produced fewer flowers during the experiment, reducing their total seed production. In these small populations, postpollination processes (at least in part, compatibility) significantly influenced male and female reproductive success. Variation in pollinator pools occurring on both spatial and temporal scales may act to preserve genetic variation for floral traits in this species.     

Effects of habitat fragmentation on parental correlations in the seed rain of a bird-dispersed species

Seed dispersal plays a crucial role in natural forest regeneration. Changes in the seed rain due to anthropogenic habitat alteration can influence seedling recruitment patterns and affect the evolutionary dynamics of populations. Using a combined endocarp-embryo microsatellite assay of naturally dispersed seeds, we concomitantly quantify the contribution of contemporary pollen and seed dispersal to the genetic structure of the seed rain of the shrub species Pistacia lentiscus L. The study was conducted in two consecutive seasons at four forest fragments embedded in contrasting (connected vs. isolated) landscapes. Interseasonal variation in the parental genetic structure of the seed rain was assessed through analysis of molecular variance, and paternal and maternal correlations and effective parental numbers were computed for different fragments and microhabitats (within fragments) using genetic kinship analysis. Temporal variation in the genetic structure of the dispersed seeds was higher for maternal gametes, reflecting a more temporally variable contribution of individual mother plants to the seed rain, as a potential consequence of masting and/or natural heterogeneity. Higher effective numbers of fathers than mothers were consistently observed in all studied forest fragments and microhabitats, the difference being more pronounced for connected than for isolated fragments. The effective number of mothers, directly influenced by disperser birds’ behavior, was apparently insensitive to fragmentation. Despite potentially high mobility of pollen by wind and seeds by birds, habitat fragmentation could influence the parental structure of dispersed seeds, with potential consequences for the genetic structure of the adult generation.     

The influence of light on paternal plants in Campanula americana (Campanulaceae): pollen characteristics and offspring traits

Offspring trait expression is determined by the combination of parental genes and parental environments. Although maternal environmental effects have been widely characterized, few studies have focused on paternal environmental effects. To determine whether light availability influences pollen and offspring traits in the woodland herb Campanula americana, we reared clones of 12 genotypes in two light levels. In the parental generation we measured pollen number and size. Plants grown under high light produced more pollen grains per flower than those grown under low light. However, the response was genotype specific; some individuals responded little to changes in light availability while others substantially reduced pollen production. As a consequence, paternity ratios may vary between light environments if more pollen is associated with greater siring success. We crossed a subset of these plants to produce the offspring generation. The paternal and maternal light environments influenced offspring seed mass, percentage germination, and days to germination, while only maternal light levels influenced later life traits, such as leaf number and size. Maternal and paternal environmental effects had opposite influences on seed mass, percentage germination and days to germination. Finally, there was no direct relationship between light effects on pollen production and offspring trait expression.