Stephen G. Weller

The evolution of wind pollination in angiosperms.

Wind pollination (anemophily) of angiosperms probably evolved from insect pollination (entomophily) in response to pollinator limitation and changes in the abiotic environment. Recent evidence suggests that ambophily (a combination of both wind and insect pollination) might be more common than was previously presumed and could represent either a stable or transitional state. We review factors favoring the evolution of wind pollination and analyse the extent of specialization towards such pollination. Phylogenetic analyses suggest that anemophily is more likely to evolve in groups with small, simple flowers and dry pollen. Wind-pollinated plants appear to have a bimodal distribution in selfing rates, but further studies recognizing the possibility of a combination of wind and animal pollination within taxa are needed to clarify this relationship.

Gender and Sexual Dimorphism in Flowering Plants: A review of Terminology, Biogeographic Patterns, Ecological Correlates, and Phylogenetic Approaches

Since Darwin’s time and the publication of The Different Forms of Flowers on Plants of the Same Species (1877), there has been continuing interest in understanding the complex but fundamental biological processes of sexual reproduction in general, gender and sexual dimorphism in plants in particular, and why “hermaphrodite plants should ever have been rendered dioecious” (Darwin 1877). Patterns of association between dioecy (separate male and female plants) and ecological traits that might explain the evolution of dioecy have been examined in several floras and these studies have made biogeographic patterns of dioecy and other plant breeding systems better known. The importance of a phylogenetic approach in assessing the cause of gender and sexual dimorphism in plants also has been recognized, and in some circumstances phylogenetic approaches have clarified patterns of breeding system diversity. With the continued interest in the evolution of gender and sexual dimorphism in plants and with contributions from a number of disciplines, the terminology associated with this area has become increasingly difficult. In this chapter we discuss the terminology associated with gender and sexual dimorphism, review the biogeographic patterns and ecological correlates of sexual dimorphism, and discuss the importance of phylogenetic considerations in the evolution of gender and sexual dimorphism in plants.

EVOLUTION OF GYNODIOECY AND MAINTENANCE OF FEMALES: THE ROLE OF INBREEDING DEPRESSION, OUTCROSSING RATES, AND RESOURCE ALLOCATION IN SCHIEDEA ADAMANTIS (CARYOPHYLLACEAE)

Levels of inbreeding depression, outcrossing rates, and phenotypic patterns of resource allocation were studied to examine their relative importance in the maintenance of high numbers of females in gynodioecious Schiedea adamantis (Caryophyllaceae), an endemic Hawaiian shrub found in a single population on Diamond Head Crater, Oahu. In studies of inbreeding depression in two greenhouse environments, families of hermaphrodites exhibited significant inbreeding depression (δ = 0.60), based on a multiplicative fitness function using seeds per capsule, germination, survival, and the inflorescence biomass of progeny. Differences between inbred and outcrossed progeny were smallest at the early stage of seeds per capsule and more pronounced at the later stages of survival and inflorescence production. These results are consistent with inbreeding depression caused by many mutations of small effect. Using allozyme analyses, the inbreeding coefficient of adult plants in the field was not significantly different from zero, implying that δ in nature may be equal to one. The single locus estimate of the outcrossing rate for hermaphrodites was 0.50 based on progeny that survived to flowering; corrected for the disproportionate loss before flowering of progeny from selfing, the adjusted outcrossing rate at the zygote stage was 0.32, suggesting that considerable selfing occurs in hermaphrodites. Females were totally outcrossed. When females and hermaphrodites were compared for reproductive output in the field, females produced over twice as many seeds per plant as hermaphrodites, primarily because females had far more capsules per inflorescence than hermaphrodites. Females had greater mass per seed than hermaphrodites in the field, either because of greater provisioning or reduced inbreeding depression. There was no significant differential mortality with respect to sex over a seven year period. The higher number of seeds per plant of females, combined with substantial inbreeding depression and relatively high selfing rates for hermaphrodites, are probably responsible for the maintenance of females in this population. The predicted frequency of females based on data for seed production, the adjusted selfing rate, and inbreeding depression is 42%, remarkably close to the observed frequency of 39%. High levels of inbreeding depression suggest that considerable quantitative genetic variation is present for traits affecting fitness in this population, despite low allozyme variability and a presumed founder effect.

CRYPTIC SELF-INCOMPATIBILITY IN AMSINCKIA GRANDIFLORA

When seed production following selfand cross-pollination is similar, a species is usually regarded as self-compatible. On this basis, Ray and Chisaki (1957a) reported that the distylous species of Amsinckia (Boraginaceae) are either fully or partly self-fertile. The combination of floral heteromorphism and self-compatibility is unusual, since most heteromorphic species that have been studied are selfincompatible (Vuilleumier, 1967). Recent pollen flow studies of Amsinckia grandiflora Kleeb. indicate that pollinations of this species include a large proportion of intramorph pollination (Ornduff, 1976). However, in two out of three years, samples in a population revealed that the two morphs occurred in equal numbers, which in a selfcompatible distylous species would suggest a high rate of outcrossing. These observations led us to investigate the possibility that this species possesses a cryptic incompatibility system. This possibility was investigated by studies of progeny resulting from natural and artificial pollinations, pollen competition studies, and pollen tube growth studies.

Effects of light, alien grass, and native species additions on Hawaiian dry forest restoration.

Alien species invasions have already caused substantial ecological and eco- nomic damage and will likely have even greater negative consequences in the future. Thus, it is imperative to improve our basic ecological understanding of these invasions and enhance our ability to reverse or mitigate their often devastating effects. Invasions by fire- promoting alien grasses have played a particularly important role in the destruction of tropical dry forests and are a major reason why these ecosystems are now among the most endangered in the world. We investigated how light availability (full sun and 50% shade), alien grass control (bulldoze, herbicide, plastic mulch, and trim treatments), and native species additions (outplanting and direct-seeding) affected the establishment of native plants and the suppression of a dominant invasive bunchgrass (fountain grass, Pennisetum seta- ceum) within a highly degraded fenced dry forest remnant on the island of Hawaii. The percent cover of native species increased in all light, grass control, and species addition treatments throughout the 20 mo of the experiment, and was greatest in the shade, bulldoze, and outplant treatments. Although fountain grass cover also increased over time in all grass control treatments, the three more aggressive techniques all significantly reduced grass cover relative to the more moderate trim treatment. In addition, there was a significant overall negative correlation between the final cover of fountain grass and native species, suggesting that these native species may successfully compete with fountain grass for water and/or nutrients. Outplant survival and the number of individuals established from direct- seeding differed significantly among the grass control treatments, and in each case, the response was highly species specific. Photosynthetic rates of established outplanted indi- viduals and fountain grass did not differ significantly across most experimental environ- ments, indicating that the local dominance of fountain grass may not be due to superior physiological attributes. The results of this experiment highlight the importance of inves- tigating species- and treatment-specific responses before attempting larger-scale restoration projects, particularly when using rare and endangered species. This study also suggests that relatively simple techniques may be used to simultaneously establish populations of vig- orous understory native species and suppress alien grasses at relatively large spatial scales, and that remnant or newly created favorable microsites may be exploited to facilitate the establishment of rarer native overstory species.

Effects of microsite, water, weeding, and direct seeding on the regeneration of native and alien species within a Hawaiian dry forest preserve

Abstract Tropical dry forests are among the most endangered ecosystems in the world in general and in Hawaii in particular. To investigate the regeneration ecology of native and alien dry forest species on the island of Hawaii, we used a factorial experiment with microsite (sub-canopy vs. inter-canopy), water (supplemental vs. ambient), and weeding (alien species removed vs. not removed) treatments, and also seeded six native woody species into each plot at the start of the experiment. At the end of the 21-month study, the biomass of the volunteer native and alien species (i.e. unplanted species consisting mainly of relatively fast-growing shrubs) was nearly three and 13 times that of the seeded species, respectively. The biomass of the native volunteers was greater in the inter-canopy plots, greater for the seeded species in the sub-canopy plots, and did not differ significantly within this treatment for the alien species. Few species survived in the ambient water plots, resulting in greater biomass in the watered plots for all species. There were no significant differences in the biomass of the native species within the weeded vs. non-weeded plots; on the contrary, we found consistently positive correlations between the abundance of the seeded species and the volunteer native and alien species. Thus it may be possible to restore Hawaiis degraded dry forests by manipulating these naturally recruiting species to create microsites favorable for the eventual re-establishment of the endangered native canopy tree flora.

A phylogenetic analysis of Schiedea and Alsinidendron (Caryophyllaceae: Alsinoideae): implications for the evolution of breeding systems

Phylogenetic analysis of Schiedea and Alsinidendron (Caryophyllaceae), a monophyletic lineage endemic to the Hawaiian Islands, produced six equally most parsimonious trees with 132 steps using morphological characters. Four major clades were found in all trees. Breeding system characters were excluded from the analysis because of the likelihood that dimorphism (gynodioecy, subdioecy, dioecy) has evolved in parallel in Schiedea, although subsequent inclusion of these characters had little effect on topology. Dimorphism is found in the two clades occurring primarily in dry habitats. Mapping of breeding systems on the phylogeny suggests that dimorphism has probably evolved on two or more occasions, depending on the number of character states and whether the character is treated as ordered or unordered. One to several reversals from dimorphism to hermaphroditism have also occurred. Dimorphic species occur only in dry habitats, but mapping of habitat on the phylogeny suggests that hermaphroditic species originally may have invaded dry habitats without evolving a dimorphic breeding system. Ecological shifts to very wet habitats appear to have favored the evolution of autogamy, which has occurred independently in the two clades largely restricted to mesic or wet habitats. The striking variation in breeding systems found in Schiedea and Alsinidendron appears to result in large part from the invasion of diverse habitats in the Hawaiian Islands following colonization by the ancestor of this lineage. Dioecy, the presence of separate pistillate (female) and staminate (male) plants in a population, occurs in about 4% of all flowering plants (Yampolsky and Yampolsky 1922). Numerous theoretical and empirical studies have addressed the question of why dioecy should evolve, given that female or male individuals suffer a 50% loss in reproductive potential relative to hermaphrodites. One set of arguments emphasizes the importance of inbreeding depression. In models developed by Lloyd (1975a) and Charlesworth and Charlesworth (1978), females may spread in populations if both inbreeding depression and selfing rates are high. Under these conditions, females spread because the.progeny of females, which are always outcrossed, will have higher fitness than the progeny of hermaphrodites, which self to varying degrees. If females produce more seeds than hermaphrodites, which seems likely on the basis of resource reallocation, they may spread even when inbreeding depression and selfing rates of hermaphrodites are lower. Other models (Charnov 1982) emphasize the importance of shifts in resource allocation. Empirical studies indicate the widespread occurrence of inbreeding depression (Schemske 1983; Schoen 1983; Sakai et al. 1989; Dudash 1990; Johnston 1992), and studies of selfing rates in several species with high inbreeding depression indicate that unisexual individuals should be favored by selection (Kohn 1988; Sakai and Weller, unpubl. data). Overall, little evidence has accumulated suggesting that either

Establishment of Lithospermum caroliniense on Sand Dunes: The Role of Nutlet Mass

The adaptive significance of variation in nutlet mass in relation to emergence and survival was investigated experimentally in Lithospermum caroliniense (Boraginaceae), a herbaceous sand dune species. In a wetter than average year, moisture availability in the field was varied by supplemental watering. Nutlet mass was positively correlated with emergence and seedling size, but not survival. Supplemental watering had little effect on emergence or survival because of the heavy and evenly spaced rains during the experiment. Size hierarchies established during the 1st yr of growth persisted for the next 2 yr. Survival to the 2nd yr was greatest for seedlings derived from the larger nutlets. In a drier than average, depth of nutlet burial was varied in addition to supplemental watering and nutless mass. Deeply buried nutlets emerged later than shallowly buried nutlets, and emergence was significantly greater in the plots receiving supplemental water. There was no obvious relationship between nutlet mass and emergence when nutlets were buried at shallow depths, but for deeply buried nutlets, larger nutlets were more likely to emerge. Nutlet mass had no effect on survival of seedlings, although survival rates averaged 92.2% in the watered subplots, compared to 43.4% in the unwatered subplots. No interaction occurred between the watering treatment and nutlet mass. In the second experiment, propagule mass had a significant effect on seedling size during the 1st yr, and larger seedlings had higher overwinter survival. By the 2nd yr, size differences related to initial nutlet mass had disappeared. In both experiments, height and leaf number were strongly correlated from year to year. Block effects were pronounced in both experiments due to differences in soil moisture content among the plots. Regardless of nutlet mass, growth was greatest in the driest plots. In each experiment, some flowering occurred in the drier plots by the 3rd yr of growth. Results demonstrated the proximal adaptive significance of nutlet mass in L. caroliniense. Identifying the factors influencing evolution of nutlet mass is more difficult, but there probably has been strong selection for seedlings derived from large nutlets. In addition, the greater ability of large nutlets to emerge when deeply buried has probably been important, since L. caroliniense is most prominent on rapidly accreting sand dunes.

Dioecy and the evolution of pollination systems in Schiedea and Alsinidendron (Caryophyllaceae: Alsinoideae) in the Hawaiian Islands

The transition from biotic to wind pollination and the consequencesof this transition for the evolution of dioecious breeding systems wereinvestigated in Schiedea and Alsinidendron(Caryophyllaceae: Alsinoideae), genera endemic to the Hawaiian Islands. The potential for wind pollination was studied for five species ofSchiedea using a wind tunnel. Morphological correlates of windpollination for these species were then used to infer the presence orabsence of wind pollination in the remaining Schiedea species. Hermaphroditic Alsinidendron and Schiedea species,which occur in mesic to wet forests, or less commonly in dry habitats,show little or no indication of wind pollination. These species had lowpollen:ovule ratios, large relative pollen size, diffuse inflorescences,substantial nectar production in several cases, and appear to bebiotically pollinated or autogamous. Sexually dimorphic species, whichall occur in dry habitats, are wind pollinated, based on wind tunnelresults or morphological adaptations indicating the potential for windpollination. These adaptations include high pollen:ovule ratios, smallpollen size, moderately to highly condensed inflorescences, and reducednectaries and nectar production. Shifts to wind pollination anddimorphism are strongly correlated in Schiedea, suggesting theclose functional relationship of the twophenomena.

INBREEDING DEPRESSION IN MORPHOLOGICAL AND PHYSIOLOGICAL TRAITS OF SCHIEDEA LYDGATEI (CARYOPHYLLACEAE) IN TWO ENVIRONMENTS

We compared inbreeding depression in hermaphroditic Schiedea lydgatei and its gynodioecious sister species, S. salicaria, to infer the level of inbreeding depression in their common ancestor. With measurements of selfing rates, this information can be used to assess the importance of inbreeding depression in the evolution of breeding systems in S. lydgatei and S. salicaria. Morphological and physiological characters related to fitness were compared for inbred and outcrossed S. lydgatei in high‐ and low‐fertilizer environments in the greenhouse. Seed mass, number of seeds per capsule, germination, survival, biomass, number of flowers, and age at first flowering were compared for inbred versus outcrossed progeny. We also measured inbreeding depression in maximal rates of photosynthetic carbon assimilation and stomatal conductance to water vapor, traits that affect fitness through their influence on plant carbon balance and water‐use efficiency (ratio of carbon gain to water loss). All traits except number of seeds per capsule in parents and survival showed inbreeding depression, with the magnitude depending on family and environment. High inbreeding depression is likely in the ancestor of S. lydgatei and S. salicaria, indicating that, with sufficiently high selfing rates, females could spread in populations. Hermaphroditism in S. lydgatei is probably favored by low selfing rates. In contrast, the evolution of gynodioecy in S. salicaria apparently has been favored by relatively high selfing rates in combination with high inbreeding depression.