Ann K. Sakai

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.

Origins of Dioecy in the Hawaiian Flora

Because of its presumed high levels of dioecy (separate male and female plants), study of the native Hawaiian angiosperm flora has been important in development of many hypotheses about conditions favoring the evolution of dioecy. The importance of ecological correlates with dioecy has proven difficult to assess, however, because of lack of data on the origins of dioecy in the Hawaiian Islands. Clearly, these correlations are of greater interest in taxa where dioecy evolved in the Hawaiian Islands (autochthonous evolution of dioecy) than in taxa that are the result of dioecious colonists with subsequent speciation in the Hawaiian Islands. Because the Hawaiian flora is small and extremely isolated, colonists can be identified and their breeding systems hypothesized, thus allowing inferences on the origins of dioecy. Using current taxonomic information, the incidence of dioecy in native Hawaiian angiosperm species is 14.7%, lower than previous estimates, but still the highest of any known flora worldwide. Ten percent of the colonists were sexually dimorphic (dioecious, gynodioecious, polygamodioecious, and subdioecious), and over half (55.2%) of current dimorphic species are in lineages arising from dimorphic colonists, showing that dimorphism is high in part because colonists were dimorphic. Autochthonous evolution of dimorphism occurred in at least 12 lineages (e.g., hermaphroditic colonists of Bidens (Asteraceae), the Hawaiian Alsinoideae (Caryophyllaceae), and Hedyotis (Rubiaceae) led to species-rich lineages that include many dimorphic species). One-third (31.8%) of current dimorphic species are in lineages arising from monomorphic colonists. Dioecy in the Hawaiian Islands is a result of both dimorphic colonists as well as evolution of dioecy in Hawaiian lineages from hermaphroditic colonists. The high incidence of dimorphism is not because dimorphic colonists evolved more species per colonist than monomorphic colonists. Detailed studies of individual lineages are critical to elucidate causal factors in the evolution of dioecy.

Growth in male and female aspen clones: a twenty-five-year longitudinal study

Field studies of Populus tremuloides at two sites in northern lower Michigan were conducted to compare the vegetative growth of ramets for male and female clones over a 25-yr period. Thirty-one clones were surveyed in 1981; 23 of these clones had been surveyed in 1956. There was no significant difference between the sexes in density (basal area divided by clonal area), mean diameter at breast height, oldest ramet age, or mean annual ring-width growth. Relative to male clones, female clones had larger numbers of ramets and greater basal area, showed a larger increase in areal spread over the 25-yr period, and had a different size class distribution. These data do not support the hypothesis that greater female investment in sexual reproduction associated with fruit production is at the expense of vegetative growth. The results suggest that further empirical longitudinal studies and measures of clonal growth as well as ramet growth are necessary to clarify the relationship of sexual reproduction and vegetative growth in long-lived clonal plants such as trembling aspen.

Biogeographical and Ecological Correlates of Dioecy in the Hawaiian Flora

The angiosperm flora of the Hawaiian Islands, with its high incidence of dioecy, has been central in development of hypotheses about the evolution of dioecy. Based on a recent taxonomic treatment of the Hawaiian angiosperm flora, we analyzed biogeo- graphic patterns of dioecy as well as the association of dioecy with ecological traits po- tentially important in the evolution of dioecy for native current species and genera. We also analyzed patterns for presumed colonists of the flora to control better for phylogenetic patterns in these traits. Dioecy is associated with woodiness, especially trees; however, this pattern does not hold for gynodioecy. Within woody species, dimorphism (dioecy, gyno- dioecy, subdioecy, polygamodioecy) is associated with mesic habitats and occurs more frequently in species with lowland and lowland-montane distributions. In contrast, in the endemic Hawaiian Alsinoideae (Schiedea and Alsinidendron) and in Bidens (two groups with autochthonous evolution of dimorphism), dimorphism is associated with more xeric habitats, and for the former group, with wind pollination. For the entire angiosperm flora, dimorphic species are associated with flowers that are small and green. Woody dioecious species and genera are disproportionately associated with wind pollination; hermaphroditic species are disproportionately bird pollinated primarily because of one species-rich lineage in the Campanulaceae. There was no association of dimorphism and pollinator type for colonists. Because of a few species-rich lineages, dimorphism is associated with dry fruits at the specific level, but at the generic level and for colonists, dimorphism is associated with fleshy fruits. Dioecious and gynodioecious species are found more often on older islands, a result of speciation of dimorphic colonists as well as autochthonous evolution of dimorphism. Single- island endemism is not associated with dioecy in the flora as a whole or with dimorphism within lineages evolving dimorphism autochthonously; thus Bakers law is not supported within the Hawaiian Islands. Because the Hawaiian angiosperm flora originated from a minimum of only 291 colonists, many of the associations of dimorphism with ecological traits occur because of the influence of only a few species-rich lineages. Better knowledge of phylogenetic patterns and further ecological studies, particularly within those groups evolving dioecy autochthonously, are needed to determine causality.

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

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.

Evolution of Dioecy in Schiedea (Caryophyllaceae: Alsinoideae) in the Hawaiian Islands: Biogeographical and Ecological Factors

Breeding systems in Schiedea and Alsinidendron (Caryophyllaceae: Alsinoideae) were characterized in order to determine whether the dioecy that occurs in Schiedea evolved in situ in the Hawaiian Islands. The occurrence of hermaphroditism in 14 of the 22 species of Schiedea, as well as outgroup comparison, indicate that dioecy is a derived breeding system. Species diversity and endemism are greatest on the older Hawaiian Islands, suggesting that these islands were colonized first. Diclinous breeding systems are more common on the older islands, probably because of the greater length of time available for the evolutionary transition from hermaphroditism to dicliny. Dicliny appears to reduce the probability of inter-island colonizations; among extant species those with hermaphroditic breeding systems are more likely to occur on more than a single island. Based on distributional patterns, it appears likely that dicliny has evolved at least three and possibly six times in Schiedea. Species occurring in dry areas are likely to have evolved from wet or diverse mesic forest ancestors. As species of Schiedea shifted to dry habitats, the evolution of dicliny appears to have been favored, perhaps by loss of pollinators and subsequent increased selfing rates. Under such conditions, the expression of inbreeding depression may have favored unisexual individuals and the evolution of dioecy.