EFFECTS OF SERIAL INBREEDING ON FITNESS COMPONENTS IN IMPATIENS CAPENSIS

Studies of inbreeding depression in wild plants customarily compare the fitness of outcrossed progeny to progeny derived from one generation of self-pollination. We compare levels of inbreeding depression in a greenhouse in two populations of jewelweed using progeny derived from random outcrosses, one generation of self-pollination, and three generations of selling. The progeny have expected inbreeding coefficients of, respectively, 0, 0.5, and 0.875. Seedling survivorship declined linearly with the level of inbreeding in both populations. Inbreeding also increased the variability of emergence date. Maternal family membership affected early seedling performance and often interacted significantly with the level of inbreeding. In contrast, path analyses reveal that inbreeding had both negative linear and positive quadratic direct effects on seed and final plant weight, causing the highly inbred progeny to outperform progeny derived from one generation of selfing. These results suggest either the rapid purging of deleterious alleles or diminishing epistasis among the loci affecting these characters. It is not clear why the loci affecting survival responded differently.     

EFFECTS OF DIFFERENT LEVELS OF INBREEDING ON FITNESS COMPONENTS IN MIMULUS GUTTATUS

Recent theoretical work has shown that there can be selection favoring the maintenance of sexual reproduction and the evolution of increased recombination when deleterious mutations at different loci interact synergistically, such that the logarithm of fitness declines at a greater than linear rate with the number of harmful mutations per genome. The purpose of this experimental study was to determine whether synergism exists for genes affecting fitness components in two partially selfing populations of the monkey flower Mimulus guttatus. For each wild population, a large randomly mated base population was constructed and many independent lines, inbred to differing degrees, were extracted from this base population. Lines with expected inbreeding coefficients of 0, 0.25, 0.5, and 0.75 were raised simultaneously in the greenhouse and were scored for germination, flowering, flower production, and pollen viability. All fitness traits except germination success declined with increased inbreeding, but in spite of the substantial inbreeding depression found in this study, relatively little evidence of synergistic epistasis was found. The only trait that showed evidence of synergism was pollen viability. These results indicate that synergism is not strong for the fitness components measured in this study. The evidence for synergism from other published studies is also reviewed.     

EFFECTS OF DIFFERENT LEVELS OF INBREEDING ON PROGENY FITNESS IN PLANTAGO CORONOPUS

Inbreeding depression (δ) is a major selective force favoring outcrossing in flowering plants. Many phenotypic and genetic models of the evolution of selfing conclude that complete outcrossing should evolve whenever inbreeding depression is greater than one-half, otherwise selfing should evolve. Recent theoretical work, however, has challenged this view and emphasized (1) the importance of variation in inbreeding depression among individuals within a population; and (2) the nature of gene action between deleterious mutations at different loci (epistasis) as important determinants for the evolution of plant mating systems. The focus of this study was to examine the maintenance of inbreeding depression and the relationship between inbreeding level and inbreeding depression at both the population and the individual level in one population of the partially self-fertilizing plant Plantago coronopus (L.). Maternal plants, randomly selected from an area of about 50 m² in a natural population, were used to establish lines with expected inbreeding coefficients (f) of 0, 0.25, 0.50, 0.75, and 0.875. Inbreeding depression was estimated both in the greenhouse and at the site of origin of the maternal plants by comparing growth, survival, flowering, and seed production of the progeny with different inbreeding coefficients. No significant inbreeding depression for these fitness traits was detected in the greenhouse after 16 weeks. This was in strong contrast to the field, where the traits all displayed significant inbreeding depression and declined with increased inbreeding. The results were consistent with the view that mutation to mildly deleterious alleles is the primary cause of inbreeding depression. At the family level, significantly different maternal line responses (maternal parent × inbreeding level interaction) provide a mechanism for the invasion of a selfing variant into the population through any maternal line exhibiting purging of its genetic load. At the population level, evidence for synergistic epistasis was detected for the probability of flowering, but not for total seed production. At the family level, however, a significant interaction between inbreeding level and maternal families for both traits was observed, indicating that epistasis could play a role in the expression of inbreeding depression among maternal lines.     

CHROMATOGRAPHIC EVIDENCE OF HYBRIDIZATION AND EVOLUTION IN PHLOX MACULATA

Representatives of P. maculata ssp. maculata and P. glaberrima ssp. interior and 36 putative hybrids were collected from a population in central Indiana. Chromatographic analysis revealed the presence of nine diagnostic components in P. maculata ssp. maculata and eight such components in P. glaberrima ssp. interior. Putative F₁ hybrids contained all or most of the parental marker components; markers of the non-recurrent parent were absent in the two classes of putative backcross progeny. The characters of P. maculata ssp. pyramidalis are a composite of those present in P. maculata ssp. maculata and P. glaberrima ssp. interior, and the former is virtually identical to certain hybrids from the population in question. The contention that P. maculata ssp. pyramidalis is a stabilized derivative of natural hybridization between these taxa is substantiated by the presence of all of the diagnostic constituents of the putative parents on its chromatograms. It is the author's opinion that the definitive data which chromatography affords will be invaluable in elucidating the complex pathways of evolution in Phlox.     

CROSSING-DISTANCE EFFECTS IN DELPHINIUM NELSONII: OUTBREEDING AND INBREEDING DEPRESSION IN PROGENY FITNESS

Depending on its genetic causes, outbreeding depression in quantitative characters may occur first in the free-living F₁ generation produced by a wide cross. In 1981–1985, we generated F₁ progenies by hand-pollinating larkspurs (Delphinium nelsonii) with pollen from 1-m, 3-m, 10-m, or 30-m distances. From the spatial genetic structure indicated by previous electrophoretic and reciprocal transplantation studies, we estimate that these crosses range from being inbred (f ≈ 0.06) to outbred. We planted 594 seeds from 66 maternal sibships under natural conditions. As of 1992, there was strong evidence for both inbreeding depression and outbreeding depression. Progeny from intermediate crossing distances grew approximately twice as large as more inbred or outbred progeny in the first 5 yr after planting (P = 0.013, repeated measures ANOVA), and survived almost 1 yr longer on average (contrast of 3-m and 10-m treatments versus 1 m and 30 m; P = 0.028, ANOVA). Twenty maternal sibships produced flowering individuals; only four and two of these represented 1-m and 30-m crossing distances, respectively (P = 0.021, G-test). The cumulative fitness of intermediate distance sibships averaged about twice that of 1-m sibships, and five to eight times that of 30-m sibships (P = 0.017, ANOVA). Thus, even though progeny of 1-m crosses were inbred to a degree only about one-eighth that of selling, inbreeding depression approximated 50%, and outbreeding depression equaled or exceeded 50% for all fitness components.     

PHYSIOLOGICAL EVIDENCE OF HYBRIDIZATION AND RETICULATE EVOLUTION IN PHLOX MACULATA

A comparative physiological analysis was conducted on a hybrid swarm involving P. maculata subsp. maculata and P. glaberrima subsp. interior. The population contained an array of segregates and introgressants. Hybrids displayed a high degree of heterogeneity in their physiological attributes, some characters being intermediate to, similar to, or transgressing those of the parental taxa. For example, both net photosynthetic rates and net photosynthetic/dark respiratory ratios were enhanced in the hybrids, and the level of enhancement was associated with the level of morphological intermediacy. Conversely, no enhancement was noted in either respiration rates or foliar fresh weight/ovendry weight ratios of the hybrids. Because of physiological imbalance, about one-third of the hybrids were eliminated early in their development. Representatives of P. maculata subsp. pyramidalis, a putative stabilized derivative of hybridization between the above two parental species, were intermediate in most physiological features and closely resembled some natural hybrids. The data verify that the physiological features of subspecies pyramidalis can be assembled through recombination of the P. maculata and P. glaberrima genomes.     

INBREEDING AND ITS FITNESS EFFECTS IN AN INSULAR POPULATION OF SONG SPARROWS (MELOSPIZA MELODIA)

Inbreeding depression is thought to be a major factor affecting the evolution of mating systems and dispersal. While there is ample evidence for inbreeding depression in captivity, it has rarely been documented in natural populations. In this study, I examine data from a long-term demographic study of an insular population of song sparrows (Melospiza melodia) and present evidence for inbreeding depression. Forty-four percent of all matings on Mandarte Island, British Columbia, were among known relatives. Offspring of a full-sib mating (f = 0.25) experienced a reduction in annual survival rate of 17.5% on average. Over their lifetime, females with f = 0.25 produced 48% fewer young that reached independence from parental care. In contrast, male lifetime reproductive success was not affected by inbreeding. Reduced female lifetime reproductive success was mostly due to reduced hatching rates of the eggs of inbred females. Relatedness among the parents did not affect their reproductive success. Using data on survival from egg stage to breeding age, I estimated the average song sparrow egg on Mandarte Island to carry a minimum of 5.38 lethal equivalents (the number of deleterious genes whose cumulative effect is equivalent to one lethal); 2.88 of these lethal equivalents were expressed from egg stage to independence of parental care. This estimate is higher than most estimates reported for laboratory populations and lower than those reported for zoo populations. Hence, the costs of inbreeding in this population were substantial and slightly above those expected from laboratory studies. Variability in estimates of lethal equivalents among years showed that costs of inbreeding were not constant across years.     

INBREEDING DEPRESSION IN PARTIALLY SELF-FERTILIZING PHLOX

Inbreeding depression was measured in terms of the relative survivorship of self versus cross seed in 14 Phlox drummondii cultivars and 10 populations of P. cuspidata. The cultivars are predominantly outcrossing; P. cuspidata is predominantly self-fertilizing. The relative survivorship of self versus cross seed averages 0.84 in the cultivars and 0.99 in P. cuspidata. In wild P. drummondii, the average is 0.83. The mean number of lethal equivalents per zygote averages 0.69 in the cultivars and 0.05 in P. cuspidata, versus 0.79 in the wild P. drummondii. There is a significant negative correlation between the amount of automatic self-seed produced by a cultivar and the number of lethal equivalents it carries (r = ?0.60). Phlox cuspidata has a lower level of cross-seed abortion than P. drummondii, which probably is not due to a difference in the incidence of lethal genes in their populations.     

EFFECTS OF PARENTAL IDENTITIES AND ENVIRONMENT ON COMPONENTS OF CROSSING SUCCESS IN PHLOX DRUMMONDII

A controlled pollination study, involving a diallel crossing scheme among 15 Phlox drummondii individuals grown under either control, low water or low nutrient conditions, was performed. The results of this research demonstrate that, although plant size and flower number are responsive to the treatments, pollen germination percentage, the survival probability of developing seeds and the weight of mature seeds are buffered against water and nutrient deprivation. However, the identities of male and female parents did have significant effects on pollen germination and seed survival, and female identity had a significant effect on seed weight.     

FITNESS CONSEQUENCES OF MATERNAL AND NONMATERNAL COMPONENTS OF INBREEDING IN THE GYNODIOECIOUS PHACELIA DUBIA

I assessed the relationship between the level of inbreeding, F, and fitness, and the effects of nonmaternal and maternal components of inbreeding on fitness in Phacelia dubia. I conducted two generations of controlled crosses and tested the performance of the F₂ progeny in field and artificial conditions covering the whole life cycle. Inbreeding significantly decreased the individual contribution of seeds to the next generation in the field, but this decrease apparently is not enough to explain the maintenance of gynodioecy. The inbred progeny contributes significantly to the population genetic structure of P. dubia. Fitness estimates and fitness components tended to decrease, usually monotonically, with F. However, nonmonotonic relationships were found in male fitness components and, in some families, in fitness estimates, seed production per fruit, and establishment. Most of the inbreeding depression takes place at the level of seed establishment in the field, but, in artificial conditions the effects of inbreeding were similar at fecundity and establishment. I studied maternal and nonmaternal components of inbreeding by testing the effects of the relatedness of maternal grandparents and parents on the performance of the progeny. Both components affected fitness. Inbreeding depression was conditioned by the level of inbreeding of the maternal plant, but this interaction varied at different fitness components. Also, the magnitude and even the direction of the relationship between fitness and F changed as a result of the combined effects of maternal and nonmaternal components of inbreeding. Such interactions can render convex or concave fitness functions, giving in the latter case the appearance of a false purging. Maternal effects of inbreeding can result from several processes: maternal investment perhaps with serial adjustments during seed development, purging of recessive deleterious genes, and nucleocytoplasmic interactions. These results illustrate the importance of maternal effects of inbreeding, and the complex effects of inbreeding on fitness. A full understanding of the fitness consequences of inbreeding and, therefore, their potential implications in the evolution of breeding systems, should take into account male and female components as well as transgenerational effects in the context of the particular environment in which fitness is evaluated.     

QUANTITATIVE GENETICS OF FITNESS TRAITS IN A WILD POPULATION OF PHLOX

To determine if the evolution of fitness traits in the annual plant, Phlox drummondii, is constrained by lack of genetic variation, we calculated the heritability and genetic correlation of 16 traits in a field population. Full- and half-sib families of seeds were generated in the greenhouse and planted back into the study population. Of 855 seeds that germinated, 609 survived to produce fruit. For each plant we measured several aspects of plant size and three components of female fecundity: total number of fruits produced, number of seeds per fruit, and mass of individual seeds. Heritability of traits ranged from 0.00 to 0.15. Several traits showed significant levels of additive genetic variance, but we found no evidence of additive genetic variance in components of female fecundity and no evidence of negative genetic correlation between fitness traits. These results suggest that evolution in this population would be constrained by lack of heritable variation in fitness traits.     

NATURAL HYBRIDIZATION BETWEEN PHLOX MACULATA AND PHLOX GLABERRIMA AND ITS EVOLUTIONARY SIGNIFICANCE

Levin, 1). A. (U. Illinois, Urbana.) Natural hybridization between Phlox maculata and Phlox glaberrima and its evolutionary significance. Amer. Jour. Bot. 50(7): 714–720. Illus. 1963.—Field and herbarium studies indicate that Phlox maculata ssp. pyramidalis is similar to P. glaberrima ssp. interior in a number of characteristics. A hybrid swarm involving P. maculata ssp. maculata and P. glaberrima ssp. interior was discovered which contained some plants that were almost identical to P. maculata ssp. pyramidalis. Crosses between P. maculata and P. glaberrima indicate that the 2 species cross readily. The chromosome complements of the 2 species are morphologically similar. These data suggest that P. maculata ssp. pyramidalis is a stabilized introgressant type.     

EFFECTS OF CROSS AND SELF-FERTILIZATION ON PROGENY FITNESS IN LOBELIA CARDINALIS AND L. SIPHILITICA

Inbreeding depression, or the decreased fitness of progeny derived from self-fertilization as compared to outcrossing, is thought to be the most general factor affecting the evolution of self-fertilization in plants. Nevertheless, data on inbreeding depression in fitness characters are almost nonexistent for perennials observed in their natural environments. In this study I measured inbreeding depression in both survival and fertility in two sympatric, short-lived, perennial herbs: hummingbird-pollinated Lobelia cardinalis (two populations) and bumblebee-pollinated L. siphilitica (one population). Crosses were performed by hand in the field, and seedlings germinated in the greenhouse. Levels of inbreeding depression were determined for one year in the greenhouse and for two to three years for seedlings transplanted back to the natural environment. Fertility was measured as flower number, which is highly correlated with seed production under natural conditions in these populations. Inbreeding depression was assessed in three ways: 1) survival and fertility within the different age intervals; 2) cumulative survival from the seed stage through each age interval; and 3) net fertility, or the expected fertility of a seed at different ages. Net fertility is a comprehensive measure of fitness combining survival and flower number. In all three populations, selfing had nonsignificant effects on the number and size of seeds. Lobelia siphilitica and one population of L. cardinalis exhibited significant levels of inbreeding depression between seed maturation and germination, excluding the consideration of possible differences in dormancy or longterm viability in the soil. There was no inbreeding depression in subsequent survival in the greenhouse in any population. In the field, significant survival differences between selfed and outcrossed progeny occurred only in two years and in only one population of L. cardinalis. For both survival and fertility there was little evidence for the expected differences among families in inbreeding depression. Compared to survival, inbreeding depression in fertility (flower number) tended to be much higher. By first-year flower production, the combined effects on survival and flower number caused inbreeding depression in net fertility to reach 54%, 34% and 71% for L. siphilitica and the two populations of L. cardinalis. By the end of the second year of flowering in the field, inbreeding depression in net fertility was 53% for L. siphilitica and 54% for one population of L. cardinalis. For the other population of L. cardinalis, these values were 76% through the second year of flowering and 83% through the third year. Such high levels of inbreeding depression should strongly influence selection on those characters affecting self-fertilization rates in these two species.     

PHENOTYPIC AND GENETIC EFFECTS OF HYBRIDIZATION IN DARWIN'S FINCHES

Morphological consequences of hybridization were studied in a group of three interbreeding species of Darwin's finches on the small Galápagos island of Daphne Major in the inclusive years 1976 to 1992. Geospiza fortis bred with G. scandens and G. fuliginosa. Although interbreeding was always rare (< 5%), sufficient samples of measurements of hybrids and backcrosses were accumulated for analysis. Five beak and body dimensions and mass were measured, and from these two synthetic (principal-component) traits were constructed. All traits were heritable in two of the interbreeding species (G. fuliginosa were too rare to be analyzed) and in the combined samples of F, hybrids and backcrosses to G. fortis. In agreement with expectations from a model of polygenic inheritance, hybrid and backcross classes were generally phenotypically intermediate between the breeding groups that had produced them. Hybridization increased additive genetic and environmental variances, increased heritabilities to a moderate extent, and generally strengthened phenotypic and genetic correlations. New additive genetic variance introduced by hybridization is estimated to be two to three orders of magnitude greater than that introduced by mutation. Enhanced variation facilitates directional evolutionary change, subject to constraints arising from genetic correlations between characters. The Darwin's finch data suggest that these constraints become stronger when species with similar proportions hybridize, but some become weaker when the interbreeding species have different allometries. This latter effect of hybridization, together with an enhancement of genetic variation, facilitates evolutionary change in a new direction.