Fitness Traits and Dispersal Ability in the Herb Tragopogon pratensis (Asteraceae): Decoupling the Role of Inbreeding Depression and Maternal Effects

Abstract: Inbreeding depression can decrease several fitness traits and maternal effects can strongly influence the amount of inbreeding depression. Understanding the effects of inbreeding depression on plant fitness is especially important in the context of habitat fragmentation, where plant populations become smaller and more isolated, exhibiting increasing levels of inbreeding depression. We examined the joint influence of inbreeding depression and maternal effects on life cycle traits and dispersal ability in the herb Tragopogon pratensis that grows in fragmented populations in Europe. We conducted experimental crosses to obtain selfed and outcrossed progeny in two contrasted environments. In particular, we produced a first generation of seeds and plants that were self-pollinated again to produce a second generation of seeds. Individual seeds were weighed and their pappuses measured to estimate the dispersal potential. Pollination treatment only had a significant effect on seed mass and dispersal ability. Coefficients of inbreeding depression did not differ between selfed and outcrossed plants. Seed mass had a significant effect on germination date. Environment had a significant effect on mass of the second generation of seeds and the interaction between pollination treatment and family was significant for six traits, indicating the existence of strong maternal effects in T. pratensis. Results suggest population differentiation. Overall, T. pratensis populations exhibited a good performance under selfing, in terms of life cycle traits and dispersal ability, which would allow the species to cope with problems associated with fragmentation.     

Joint evolution of differential seed dispersal and self‐fertilization

Differential seed dispersal, in which selfed and outcrossed seeds possess different dispersal propensities, represents a potentially important individual‐level association. A variety of traits can mediate differential seed dispersal, including inflorescence and seed size variation. However, how natural selection shapes such associations is poorly known. Here, we developed theoretical models for the evolution of mating system and differential seed dispersal in metapopulations, incorporating heterogeneous pollination, dispersal cost, cost of outcrossing and environment‐dependent inbreeding depression. We considered three models. In the ‘fixed dispersal model’, only selfing rate is allowed to evolve. In the ‘fixed selfing model’, in which selfing is fixed but differential seed dispersal can evolve, we showed that natural selection favours a higher, equal or lower dispersal rate for selfed seeds to that for outcrossed seeds. However, in the ‘joint evolution model’, in which selfing and dispersal can evolve together, evolution necessarily leads to higher or equal dispersal rate for selfed seeds compared to that for outcrossed. Further comparison revealed that outcrossed seed dispersal is selected against by the evolution of mixed mating or selfing, whereas the evolution of selfed seed dispersal undergoes independent processes. We discuss the adaptive significance and constraints for mating system/dispersal association.     

INBREEDING DEPRESSION IN HYDROPHYLLUM APPENDICULATUM: ROLE OF MATERNAL EFFECTS,CROWDING, AND PARENTAL MATING HISTORY

This paper examines several aspects of the expression of inbreeding depression in an outcrossing, obligately biennial plant, Hydrophyllum appendiculatum (Hydrophyllaceae). The amount of inbreeding depression detected was small during the first year of life but increased with age and had significant effects on adult size and reproductive traits. The lack of significant inbreeding depression during early growth is likely due to the overriding influence of maternal environmental effects on seed size and seedling growth. However, as maternal effects decreased with age, the seedling's own genotype became a more important determinant of its fate. To examine whether the expression of inbreeding depression was sensitive to ecological conditions, selfed and outcrossed seedlings were grown alone or with other H. appendiculatum seedlings. No inbreeding depression was detected in the plants grown alone. In contrast, under competitive conditions, outcrossed seedlings were significantly larger than selfed seedlings by the end of the first growing season. To address whether parental mating history influences the amount of inbreeding depression expressed, I examined the consequences of two successive generations of selfing on seed set and seed weight. The amount of inbreeding depression increased following the second generation of selfing. In the first generation, seed set and seed weight differed by less than 5% between selfed and outcrossed progeny. However, both traits were 15% greater for outcrossed plants after two generations. These results indicate that the alleles responsible for the reductions in these traits were not purged and suggest the action of multiple loci with deleterious effects.     

The effectiveness of some mechanisms of reproductive isolation in Arum maculatum and A. italicum (Araceae)

Mechanisms of reproductive isolation were studied in two species of Arum , A. italicum and A. maculatum , growing in England and the south of France. The study focused on three potential mechanisms for reproductive isolation: the effectiveness of dichogamy as a barrier to autogamy; the ability of self and outcrossed pollen to germinate on stigmas at different stages of anthesis and to effect pollination; and postzygotic barriers to selfing. Dichogamy was found to provide a very effective barrier to within-inflorescence selfing in these species, as no seeds were produced by spontaneous self-pollination (i.e. autogamy) in any population of either species. However, the study found that geitonogamy (cross-pollination between inflorescences of a same individual or clone) was possible, as genotypes frequently produced several inflorescences and stigmas were found to be receptive to pollen from before anthesis until their contraction at the end of the female phase of flowering. Hand pollination with self pollen from clone inflorescences produced as numerous and heavy seeds as outcross pollination. In addition, the germination and growth of geitonogamously produced seed was similar to that of outcrossed seed, suggesting that this potential postzygotic barrier is absent or weak. These findings suggest that geitonogamous seed production may be unrestricted by significant pre- or postzygotic barriers. The possible advantages of geitonogamy in Arum are discussed.  © 2006 The Linnean Society of London, Botanical Journal of the Linnean Society , 2006, 150 , 323–328.     

Evolution of the Selfing Rate and Resource Allocation Models

Abstract First, evolutionary theories of selfing of terrestrial plants are reviewed briefly. The evolution of the selfing rate is controlled mainly by (1) the benefit of enhanced genetic relatedness to seeds and (2) the cost of lowered fitness of selfed offspring (inbreeding depression), being modified by (3) fertility assurance under pollen limitation, (4) reduced performance as pollen donor, (5) reduced expenditure to male function, and (6) lowered genetic recombination. Models of the joint evolution of selfing and inbreeding depression predict either strong outcrossing or predominant selfing. Although wind-pollinated plants fit the prediction, some animal-pollinated species have intermediate selfing rates, refuting the theory.
Second, three resource allocation models are analyzed, in which an individual plant optimally allocates limited resources to outcrossed seeds, selfed seeds, and to energy reserves for the next year. The first model explains how the number of outcrossed and selfed offspring change with plant size when they differ in dispersal distance. The second model predicts that, in a disturbed habitat, the plant is likely to be annual and to produce both selfed and outcrossed seeds; in contrast, in a stable habitat, the plant tends to be perennial and to abort selfed seeds selectively. Hand pollination may increase seed production for perennials but not for annuals. The third model explains the observed difference between animal and wind pollinated plants in the out-crossing rate pattern by the difference in the way pollen acquisition increases with investment.     

The effect of timing of pollination on the mating system and fitness ofKalmia latifolia (Ericaceae)

Plant mating systems are known to vary within species and some immediate ecological factors have been found to be associated with the geographic distribution of selfing. The environmental condition of the maternal plant may influence the production of selfed seed relative to outcrossed seed. This study investigated the effect of late pollination on the mating system of Kalmia latifolia, a long-lived perennial shrub. A 2 × 2 experimental design was used to determine whether reproductive success declines over the course of the flowering season and whether there was an interaction between pollination time (early vs. late in the season) and pollen type (self-fertilized vs. outcrossed). An interaction of this sort would indicate context-dependent fitness of selfed seeds compared to outcrossed seeds and, thus, show an ecological influence over a plant's mating system. Relative fitness was assessed in terms of female reproductive success. Timing of pollination did not affect abortion of outcrossed seeds; however, delay in pollination increased abortion of selfed seeds by 34.7%. Thus, it appears that plants selectively aborted selfed seeds rather than outcrossed seeds and this selection was more intense at the end of the season. An ecological factor such as time of pollination may affect the mating system of K. latifolia.     

Consequences of differences in flowering date on seed production in Heloniopsis orientalis (Liliaceae)

We examined the consequences of differences in flowering date on seed production in the self-compatible herb Heloniopsis orientalis. The number of selfed seeds per fruit, as determined by microsatellite markers, did not depend on when the plant flowered, whereas the number of outcrossed seeds per fruit increased with later flowering dates. Consequently, the selfing rate decreased with later flowering dates. The number of seeds (including both selfed and outcrossed ones) per fruit and the seed?:?ovule ratio increased with later flowering dates. We also examined the effects of pollinators and plant size on seed production. The visitation rate of Diptera did not depend on the flowering season, whereas that of Hymenoptera markedly increased as the flowering season progressed. Diptera stayed longer than Hymenoptera on each plant and flower. Seed production per fruit did not depend on plant size. Thus, the change in selfing rate associated with later flowering dates resulted from the seasonal change in pollinators rather than plant size.     

Assessing frequency-dependent seed size selection: a field experiment

Seed size is a life history attribute that affects the probability of seed predation, and therefore affects plant fitness. Compared with smaller seeds, those with large size should be more attractive to predators, as they constitute a more profitable food item because of higher energetic and/or nutrient content. However, predator preferences may be frequency-dependent in the sense that they may be modulated by the relative abundance of alternative seeds of different sizes. We set up a field experiment to evaluate frequency-dependent seed predation using seeds of Cryptocarya alba (Lauraceae), at La Campana National Park in central Chile. Predators (rodents and birds) preferentially consumed large seeds in an antiapostatic manner. These selective responses were maintained throughout the experiment and seed selection by predators was not affected by previous seed consumption. Our results suggest that (a) large seeds are very profitable food items actively sought by seed predators even at low relative abundance, (b) seed selection is expressed in a short time scale and (c) seed predators, by consuming large seeds consistently, have the potential to modify significantly the quality of plant progeny.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 81 , 307–312.     

Variation of selfing rate and inbreeding depression among individuals and across generations within an admixed Cedrus population

We investigated the variation and short-term evolution of the selfing rate and inbreeding depression (ID) across three generations within a cedar forest that was established from admixture ca 1860. The mean selfing rate was 9.5%, ranging from 0 to 48% among 20 seed trees (estimated from paternally inherited chloroplast DNA). We computed the probability of selfing for each seed and we investigated ID by comparing selfed and outcrossed seeds within progenies, thus avoiding maternal effects. In all progenies, the germination rate was high (88–100%) and seedling mortality was low (0–12%). The germination dynamics differed significantly between selfed and outcrossed seeds within progenies in the founder gene pool but not in the following generations. This transient effect of selfing could be attributed to epistatic interactions in the original admixture. Regarding the seedling growth traits, the ID was low but significant: 8 and 6% for height and diameter growth, respectively. These rates did not vary among generations, suggesting minor gene effects. At this early stage, outcrossed seedlings outcompeted their selfed relatives, but not necessarily other selfed seedlings from other progenies. Thus, purging these slightly deleterious genes may only occur through within-family selection. Processes that maintain a high level of genetic diversity for fitness-related traits among progenies also reduce the efficiency of purging this part of the genetic load.     

Outcrossing rate and inbreeding depression in the perennial yellow bush lupine, Lupinus arboreus (Fabaceae)

Little is known about the breeding systems of perennial Lupinus species. We provide information about the breeding system of the perennial yellow bush lupine, Lupinus arboreus, specifically determining self-compatibility, outcrossing rate, and level of inbreeding depression. Flowers are self-compatible, but autonomous self-fertilization rarely occurs; thus selfed seed are a product of facilitated selfing. Based on four isozyme loci from 34 maternal progeny arrays of seeds we estimated an outcrossing rate of 0.78. However, when we accounted for differential maturation of selfed seeds, the outcrossing rate at fertilization was lower, ～0.64. Fitness and inbreeding depression of 11 selfed and outcrossed families were measured at four stages: seed maturation, seedling emergence, seedling survivorship, and growth at 12 wk. Cumulative inbreeding depression across all four life stages averaged 0.59, although variation existed between families for the magnitude of inbreeding depression. Inbreeding depression was not manifest uniformly across all four life stages. Outcrossed flowers produced twice as many seeds as selfed flowers, but the mean performance of selfed and outcrossed progeny was not different for emergence, seedling survivorship, and size at 12 wk. Counter to assumptions about this species, L. arboreus is both self-compatible and outcrosses ～78% of the time.     

THE INFLUENCE OF THE MATING SYSTEM ON SEED SIZE VARIATION IN CRINUM ERUBESCENS (AMARYLLIDACEAE)

We present evidence that extreme seed size variation in fruits of Crinum erubescens (range: 0.1 to 66.5 g per seed) occurs when mating pairs are inbred, either from selfing or biparental inbreeding. Several relatively uniform seeds of intermediate size are produced when pollen from several pollen donors is applied simultaneously to a flower. Selfed fruits and some fruits pollinated with a single pollen donor produce both large and small seeds, although selfed fruits produce fewer seeds than outcrossed fruit. These results are contrary to the hypothesis that variation in seed size is attributable to either pollen competition or differential allocation of maternal resource to seeds of different genotypes.     

FITNESS CONSEQUENCES OF MATING SYSTEM,SEED WEIGHT,AND EMERGENCE DATE IN A WINTER ANNUAL,COLLINSIA VERNA

Selfed and outcrossed progeny of 60 maternal parents were produced to investigate the joint and individual effects of mating system, seed weight, and emergence date on the expression of characters related to fitness and adult fecundity. A series of analyses of variance investigated these effects through time and indicated that 1) mating system explained 56% of the variance in seed weight, 2) seed weight explained 51% and mating system explained 38% of the variance in emergence date, and 3) mating system explained 71% and seed weight explained 15% of the variance in fecundity. Outcrossed-seed means differed significantly from selfed-seed means for all traits measured. On average, outcrossed seeds were larger, germinated earlier, had higher percentage emergence, and produced plants that were more fecund than selfed seeds. The coefficient of inbreeding depression increased through time in this study, from 0.05 for seed weight to 0.23 for fecundity. Seed weight and emergence date were positively correlated, both phenotypically and genetically, for both mating systems. Genetically, this indicates that genes that increase the value of seed weight also increase the value of emergence date and vice versa. Phenotypically, the positive correlation indicates that larger seeds germinate later. Outcrossed seeds were significantly larger but germinated earlier than selfed seeds, suggesting that mating system has an overriding effect in influencing fitness. In light of the selection on emergence date quantified in a previous study, seed weight, emergence date, and mating system may be functioning as a cluster of characters on which selection acts jointly in this species.     

LIMITS TO REPRODUCTIVE SUCCESS IN A PARTIALLY SELF-INCOMPATIBLE HERB: FECUNDITY DEPRESSION AT SERIAL LIFE-CYCLE STAGES

Like many angiosperms, Crinum erubescens is partially self-compatible, producing fewer seeds upon selfing than after outcrossing. In this paper we test the relative magnitude of the prefertilization and postfertilization effects of self-incompatibility, inbreeding depression, or both in a natural population of this hermaphroditic tropical herb. We characterize prefertilization effects by examining pollen tube growth, while postfertilization effects are characterized by examination of embryo abortion and seed maturation. Statistical methods are developed to test the magnitude of these effects from one life-cycle stage to the next. We find that although pollen performance in selfed flowers is lower than that in outcrossed flowers, pollen performance is low overall. Postfertilization effects attributable to inbreeding depression account for a larger proportion of the reduction in fecundity in selfed compared to outcrossed flowers. Among naturally pollinated plants, despite ample pollen deposition, the numbers of fruits and seeds set are intermediate to selfed and outcrossed treatments.     

Effects of inbreeding on traits that influence dispersal and progeny density in Cakile edentula var. lacustris (Brassicaceae)

Inbreeding may influence the intensity of sibling competition by altering the number of offspring produced or by changing plant morphology in ways that influence seed dispersion patterns. To test this possibility, effects of inbreeding on seed production and on traits that influence progeny density were measured using experimental pollinations of flowers of Cakile edentula var. lacustris. Different flowers on a plant were either hand pollinated with self pollen (with and without emasculation) or foreign pollen, or they were allowed to be pollinated naturally. Selfed flowers matured significantly fewer viable seeds than outcrossed flowers (10.3% less seed maturation with inbreeding depression of 19.2%), due in large part to a greater percentage of proximal seed abortions and lower germination success. Plants grown from selfed seeds tended to have lower seed production (37 fewer seeds on average, with inbreeding depression of 16.2%), caused in part by an increase in the percentage of fruits with proximal seed abortions, although this effect was not significant. Inbreeding depression in total fitness was 29.0%, which corresponds to a difference of 46 seeds per pollinated ovule. Selfing rate estimates were usually intermediate to high, indicating that inbreeding effects observed in this study would be present in naturally pollinated progeny. Although the influence of inbreeding directly on dispersal was negligible, the predicted reduction in sibling competition caused by reduced seed production resulted in an estimate of inbreeding depression of 17.5%, which is 11.5% lower than that measured under uniform conditions. Consequently, inbreeding depression estimated under natural dispersion patterns may be lower than that estimated under uniform conditions since seeds from self- and cross-pollination may not experience the same competitive environment in the field. Inbreeding in the maternal generation, therefore, could influence progeny fitness not only by determining the genetic composition of progeny, but also by influencing the competitive environment in which progeny grow.     

Seed dormancy in relation to seed storage behaviour in Acer

Dormancy in seeds of Acer opalus is shown to be mainly caused by the seed coats, although a slight embryo dormancy exists in fresh seeds. The ability to germinate after drying indicates that seed storage behaviour is orthodox. Recalcitrant seeds were heavier than orthodox seeds not only within section Acer but also within the whole genus after statistical control of phylogeny, through a phylogenetic ANOVA with data from two different Acer phylogenies. An evolutionary change from orthodox to recalcitrant behaviour is postulated for genus Acer , but this change appears not to have been accompanied by a change in seed dormancy, at least in the taxonomic section in which Acer opalus belongs.  © 2004 The Linnean Society of London, Botanical Journal of the Linnean Society , 2004, 145 , 203–208.     

Why are small seeds dispersed through animal guts: large numbers or seed size per se?

Long-distance dispersal of seeds is an important process in metapopulation dynamics and in plant migrations, but at the same time extremely difficult to observe or quantify directly. If seed dispersal ability were related to attributes of seeds or motherplants, long-distance seed dispersal would be predictable by indirect approximation using easy-to-measure traits. Seed size has been suggested to be such a key trait in seed dispersal ability. However, having smaller seeds also implies having more numerous seeds per plant individual (given equal reproductive effort), and consequently increases the probability of seeds being ingested accidentally. The question is whether small-seeded species are more abundant in herbivore dung because smaller seed size increases survival rate during gut passage or because they are produced (and ingested) in greater numbers than larger seeds. We investigated endozoochorous seed dispersal via cattle grazing a meadow, and related seed abundance in dung samples to seed attributes. We found that seeds were ingested and passed through the bovine intestinal tract in proportion to the numbers produced per unit area in the grazed vegetation. In contrast, no relationship could be found between endozoochorous dispersal potential (measured as abundance of seeds in dung samples corrected for seed output in the grazed vegetation) and seed attributes such as seed mass, seed shape (roundness), and thickness of the seed coat. This finding underlines the importance of seed number in plant dispersal ability. In addition, it shows that grazing mammals may constitute an important dispersal vector for many plant species conventionally classified as 'unspecialised'.     

Reproductive biology of the invasive exotic shrub, Rhododendron ponticum L. (Ericaceae)

The reproductive biology of an exotic species will affect its ability to become naturalized and invasive in non-native habitats. Rhododendron ponticum is an ecologically damaging exotic weed in the British Isles, which spreads predominantly by seed. I investigated how inbreeding and outcrossing affect seed production and germination in a wild population of this species in Ireland. Experimental manipulations revealed low fruit and seed set when insects were excluded from flowers, suggesting that this species has limited capability for spontaneous autogamy. Hand-pollination treatments showed that, although flowers are self-compatible (with self and same plant pollen), higher levels of seed set occur following outcrossing (xenogamy). There was no significant difference in rate of germination of seeds from inbred or outcrossed treatments. The addition of xenogamous pollen to open flowers did not increase fruit or seed set, suggesting that flowers in this population are not pollen limited: native generalist pollinators, mainly bumblebees ( Bombus spp.), are providing an adequate pollinator service. This work demonstrates that outcrossing increases seed set and pollinators are required to facilitate this. Hence, generalist native pollinators can promote invasion by exotic plants. Native pollinators can clearly play an important part in alien species invasion.  © 2007 The Linnean Society of London, Botanical Journal of the Linnean Society , 2007, 155 , 373–381.     

Inbreeding effects on fitness traits in the heterocarpic herb Leontodon autumnalis L. (Asteraceae)

Heterocarpic plants are characterized by the production of distinct types of fruits that usually differ in their ecological behavior. In the Asteraceae, differences are mainly found between peripheral non-dispersal and central dispersal achenes (single-seeded fruits). Inbreeding depression is considered as an evolutionary force as it may reduce several fitness traits, and in the case of heterocarpic plants, it could influence fitness traits (e.g., seed set, germination rate, growth rate) of each fruit morph, which may have important ecological and evolutionary consequences. In particular, differential effects on fitness traits and dispersal of selfed and outcrossed progeny can strongly determine the viability of extant populations and the potential to colonize new habitats. We conducted a hand-pollination experiment in greenhouse conditions to test whether inbreeding affects the fitness of achene morphs in the heterocarpic herb Leontodon autumnalis (Asteraceae). Results show that achene morphs significantly differ in their ecological behavior, peripheral achenes germinating more and faster than central achenes. The significant interaction between pollination treatment and achene morph for germination probability might indicate a link between dormancy and mating system in L. autumnalis: germination was higher for outcrossed achenes in central achenes whereas the opposite pattern was exhibited by peripheral achenes. Selfing dramatically reduced seed set, probably as a consequence of strong self-incompatibility mechanisms rather than inbreeding effects. Inbreeding depression significantly affected late life-cycle traits, such as growth rate and biomass at flowering. Overall, results suggest that inbreeding depression seems to be an important selective force maintaining outcrossing in L. autumnalis.     

POLLEN AND OVULE SOURCES AFFECT SEED PRODUCTION OF LOBELIA CARDINALIS (LOBELIACE AE)

To examine the breeding system and components of male and female reproductive success in the hermaphroditic plant Lobelia cardinalis, we performed three crossing experiments with plants taken from natural populations. The experiments were designed to determine if the crossing success of plants as pollen and ovule parents was affected by the distance among mates, including self-pollinations and pollinations between populations; to determine if plants differed in their abilities to sire or mature seed; and to determine if there was a correlation between a plant's success at siring and maturing seed. Selfpollinations resulted in significantly fewer seeds per fruit and significantly smaller seeds. There were no significant differences in germinability between selfed and outcrossed seeds. Distance among parents within a population did not affect any of the traits. Outcrosses within and between population produced similar numbers of seeds per fruit, similar seed weights, and similar germination success. There were highly significant differences among maternal plants in all three experiments in the number of seeds they matured, mean seed weight, and seed germinability. The maternal parent was the most important factor determining seed production, but there were also significant differences among paternal plants in the number of seeds they sired (all three experiments), in the germinability of the seeds they sired (two experiments), and in the sizes of seeds they sired (one experiment). Our results indicate that differences in success of Lobelia plants as male parents cannot be due solely to their relatedness to the female parent.     

Fruit and seed ontogeny related to the seed behaviour of two tropical species of Caesalpinia (Leguminosae)

Caesalpinia echinata and C. ferrea var. ferrea have different seed behaviours and seed and fruit types. Comparison of the seed ontogeny and anatomy partly explained the differences in seed behaviour between these two species of Brazilian legumes; some differences were also related to fruit development. The seed coat in C. ferrea consisted of two layers of osteosclereids, as well as macrosclereids and fibres, to form a typical legume seed coat, whereas C. echinata had only macrosclereids and fibres. In C. echinata , the developing seed coat had paracytic stomata, a feature rarely found in legume seeds. These seed coat features may account for the low longevity of C. echinata seeds. The embryogeny was similar in both species, with no differences in the relationship between embryo growth and seed growth. The seeds of both species behaved as typical endospermic seeds, despite their different morphological classification (exendospermic orthodox seeds were described for C. echinata and endospermic orthodox seeds for C. ferrea ). Embryo growth in C. ferrea accelerated when the sclerenchyma of the pericarp was developing, whereas embryonic growth in C. echinata was associated with the conclusion of spine and secretory reservoir development in the pericarp. Other features observed included an endothelial layer that secreted mucilage in both species, a nucellar summit, which grew up into the micropyle, and a placental obturator that connected the ovarian tissue to the ovule in C. ferrea . © 2004 The Linnean Society of London, Botanical Journal of the Linnean Society , 2004, 146 , 57–70.