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Origins of dioecy in the Hawaiian flora.

INTRODUCTION

The evolution of separate male and female plants in populations (dioecy) has occurred independently in many floras and in diverse taxa, and its repeated evolution has been of particular interest. The majority of flowering plant species are hermaphroditic, and worldwide only [approximately equal to] 4% of flowering plant species are dioecious (Yampolsky and Yampolsky 1922). The incidence of dioecy varies considerably in different regional floras (summarized in Steiner 1988), including values as low as 2.8% in California (Fox 1985) to 12-13% of species in New Zealand (Godley 1979; 18% of genera, Lloyd 1985; also see Webb and Kelley 1993). The Hawaiian flora is of particular interest for studies of dioecy. Gilmartin (1968, using Hillebrand's flora written in 1888) reported only 5% dioecy in the Hawaiian flora, but more recently Carlquist (1974), using data from a variety of sources including his own investigations, reported that 27.7% of the native Hawaiian angiosperm species and varieties were dioecious, a figure twice as high as that for the next highest flora of New Zealand.

Hypotheses on selective-forces promoting the evolution of dioecy include those that suggest that dioecy has evolved as a mechanism to avoid inbreeding depression as well as those that suggest that resource allocation, sexual selection, and ecological factors are important (reviewed in Bawa 1980, Thomson and Brunet 1990). Because of its high frequency of dioecy, the Hawaiian flora has been cited as critical evidence in support of some theories on factors promoting the evolution of dioecy (Baker 1967, Carlquist 1974, Bawa 1980, Thomson and Barrett 1981, Baker and Cox 1984). Carlquist (1966, 1974) suggested that the advantages of outcrossing with dioecy were sufficiently high in insular habitats that they outweighed the disadvantages of needing individuals of both sexes to establish populations after long distance dispersal. As a consequence, Carlquist suggested that the high-incidence of dioecy in Hawaii was in part a result of dioecious colonists. In contrast, Baker (1967) contended that self-compatible hermaphrodites were much more likely to colonize after long-distance dispersal because a single propagule was sufficient to start a population (Baker's law). He suggested that the high incidence of dioecy in the Hawaiian Islands was the result of autochthonous (in situ) evolution of dioecy (Baker 1967), although in later work (Baker and Cox 1984) he suggested several mechanisms that allow establishment by dioecious colonists. Thomson and Barrett (1981) suggested that the high levels of autochthonous evolution of dioecy in the Hawaiian Islands support the importance of outcrossing as a factor. Bawa (1980) used the Hawaiian flora to support his hypothesis of a correlation of dioecy with pollination by small generalist insects and with fruit dispersal by birds.

Analysis of the Hawaiian flora can offer special insights into the evolution of dioecy because the great isolation of the archipelago ([approximately equal to]4000 km from the nearest large mass of North America) has limited the number of angiosperm colonists. Previous estimates suggest that only [approximately equal to]272-282 long-distance colonists gave rise to the current native flowering plants (Fosberg 1948, Wagner et al. 1990, Wagner 1991). Phylogenetic considerations that have presented problems in analyses of other floras (Donoghue 1989) can be addressed by analysis of presumed colonists as well as extant species. With hypotheses about the colonists' breeding systems and lineages descended from these colonists, in lieu of more detailed phylogenies for most taxa, it is possible to distinguish current dioecious species that arose from dioecious colonists from those species where dioecy evolved autochthonously (in situ) within the Hawaiian Islands.

We analyzed current taxonomic information (Wagner et al. 1990; see also Sakai et al. 1995) on the breeding systems of known (extant and recently extinct) native species of the Hawaiian Islands as well as the breeding systems and lineages of colonists of the Hawaiian Islands with two objectives. The first objective was to report breeding system distributions of the Hawaiian flora, in light of recent systematic work, including better knowledge of breeding systems. The second objective was to distinguish whether the high incidence of dioecy in the Hawaiian flora results from (1) high rates of successful colonization by dioecious colonists (of endemic and indigenous species), (2) greater numbers of species in dioecious lineages than hermaphroditic lineages, or (3) evolution of dioecy in situ from hermaphroditic colonists. In the latter case, comparison of the ecological conditions associated with dioecious and hermaphroditic species may be especially relevant for ascertaining causal factors in the evolution of dioecy (see also Sakai et al. 1995).
TABLE 1. Comparisons of breeding system distributions from
Carlquist
(1974) and Wagner et al. (1990). Letters represent the sex of the
flowers (M = male, F = female, H = hermaphroditic) and parentheses
indicate the types of flowers found on the same plant. Ellipses
indicate categories that were not included in Carlquist's (1974)
analysis; N/A = not applicable.


                                       Species              Genera


Breeding system                     1974     1990      1974
1990


Dioecy (M) (F)                      27.7     14.7      15.3
11.4
Gynodioecy (F) (H)                   2.6      3.8       2.7
1.3
Subdioecy (M) (F) (rare H)           ...      0.6       ...
0
Polygamodioecy (M, rare H)
  (F, rare H)                        0.4      1.6       0.9
1.8
Hermaphroditism (H)                 56.9     62.4      64.4
62.0
Monoecy (M, F)                       5.0      7.6       7.2
10.9
Andromonoecy (M, H)                  2.5      4.5       4.1
5.2
Gynomonoecy (F, H)                   4.4      3.9       3.6
2.6
Polygamomonoecy (M, F, rare H)       0.5      0.1       1.8
0


Dimorphism                          30.7     20.7      18.9
14.4
Monomorphism                     69.3(*)     78.7      81.1
80.8
Unknown                              ...      0.5       ...
0.4
Mixed genera (dimorphic and
  monomorphic spp.)                  N/A      N/A       ...
4.4
N                                1490(*)      971       222
229


* Values were calculated using the sum of individual sexual
conditions (Carlquist, 1974: Table 13.1) rather than his dimorphic
total (based on N = 1449) or the data given (N = 1430). Note that
Carlquist's (1974) totals include species plus varieties; our 1990
data include species but do not count infraspecific taxa.


MATERIALS AND METHODS

Information was taken from the Manual of the Flowering Plants of Hawai'i (Wagner et al. 1990; referred to hereafter as the Manual) with some updating (see Appendix; see also Sakai et al. 1995). Terminology of breeding systems follows that given in the Manual. Following Lloyd (1980), we also use the term sexually dimorphic to collectively refer to taxa with dioecious, subdioecious, polygamodioecious, or gynodioecious systems; monomorphic refers to taxa with hermaphroditic, monoecious, andromonoecious, gynomonoecious, or polygamomonoecious systems (see Table 1 for definitions). Breeding systems were generally taken as those listed in the Manual. If data on breeding systems in the Manual were ambiguous, specimens (BISH, US) were re-examined or authorities for those taxa were consulted when possible (Schiedea, A. Sakai and S. Weller; Wikstroemia, S. Mayer; Bidens, F. Ganders). Five species were omitted from analyses because their breeding systems were unknown; Poa also was excluded from the generic-level analysis because the breeding systems of the native species are not known. Most genera were easily classified with respect to breeding system because species within them all had the same breeding system or at least were all monomorphic or all dimorphic. Genera comprised of species with both dimorphic and monomorphic breeding systems were classified as mixed.

Native species included endemic species (found naturally only in the Hawaiian Islands), indigenous species (found naturally in the Hawaiian Islands as well as elsewhere), and also those species that were noted in the Manual as questionably naturalized (i.e., possibly native or questionably introduced by colonizing Polynesians). Each indigenous species was counted as one colonization, even for species such as Scaevola sericea that have colonized the islands on multiple occasions. Presumed original colonists were derived from consideration of two previous estimates of colonization events in the Hawaiian archipelago (Fosberg 1948, Carlquist 1974), and from phylogenetic relationships reported in the Manual by over 50 contributors, including more recent information communicated to us by them. Colonists for taxa without a specialist were inferred from morphological studies conducted (by W. L. Wagner and D. R. Herbst) in preparation of the Manual and from consultation of taxonomic works with more general discussions of relationships. Explicit phylogenetic discussion of Hawaiian angiosperm lineages has begun to emerge only recently (Baldwin et al. 1990; Wagner and Funk 1995; Weller et al. 1995; F. Ganders, unpublished manuscript).

In the absence of more specific information, we assigned the breeding system of the colonist based on genera or species related to the endemic Hawaiian taxa; in most cases, however, the closest sister taxon of the Hawaiian species is unknown. For nonendemic genera, we used the general conditions present in extra-Hawaiian species, unless more specific relationships within the genus could be determined. In more difficult cases, the breeding system of the colonist was assigned only a more general designation (e.g., monomorphic or dimorphic). Ten colonists had unknown breeding systems and were omitted from analyses of breeding systems, thus making our estimate of dimorphism in the colonists a conservative one.

Because the data set used in this paper is not available in any source in its entirety, a comprehensive list of the presumed colonists and their resulting Hawaiian lineages is listed in the Appendix. The Appendix also includes additional attributes for each presumed colonist that relate to ecological correlates of breeding systems in the Hawaiian flora (Sakai et al. 1995). Presumed colonists with breeding systems that were difficult to determine or where our determination differed from earlier works (e.g., Carlquist 1974, Bawa 1982; others in Appendix) are discussed in more detail in the notes to the Appendix.

RESULTS

Of the 971 native species, 14.7% are dioecious and 20.7% are dimorphic, proportions that are the highest of any flora studied, but far lower than Carlquist's earlier estimates that included infraspecific taxa (1974: Chapter 13; Table 1). Our results differ because we did not use infraspecific taxa (there was no variation in breeding system at that level), and because recent taxonomic changes (Wagner et al. 1990) reduced the total number of both hermaphroditic and dioecious taxa, but disproportionately affected dimorphic taxa, especially infraspecific taxa in Loganiaceae, Pittosporaceae, Rubiaceae, and Rutaceae. Changes also result in small part to more detailed studies of breeding systems. At the generic level, 11.4% are dioecious; 14.4% are dimorphic. Strictly dioecious genera have a mean of 3.04 species/genus (N = 24, SD = 4.03); strictly hermaphroditic genera have a mean of 3.65 species/genus (N = 142, SD = 6.27).

The 971 native Hawaiian species are the result of speciation from 291 presumed colonists, a number slightly higher than that of previous estimates (Fosberg 1948, Carlquist 1974, Wagner et al. 1990, Wagner 1991). Six colonists gave rise to more than one genus, and in 45 genera, the species are the result of more than one colonization. Two-thirds of the colonists (194/ 291) are represented by only a single species. Of the 119 indigenous colonists, all but 10 are represented by only one species. From those 10 colonists [Lepidium (Brassicaceae), Gahnia and Mariscus (Cyperaceae), Eugenia (Myrtaceae), Boerhavia and Pisonia (Nyctaginaceae), Peperomia (Piperaceae), Portulaca (Portulacaceae), and 2 colonists of Korthalsella (Viscaceae)], indigenous species are presumed to have given rise directly to endemic species and both indigenous and endemic species are extant.

At the other extreme, one colonist in the Campanulaceae has given rise to four genera (Clermontia, Cyanea, Delissea, and Rollandia) with a total of 91 species ([greater than]9% of the total flora) and the one colonist of Stenogyne, Phyllostegia and Haplostachys (Lamiaceae) has resulted in 53 species. Other species-rich lineages include those for Melicope (47 species, Rutaceae), the silversword complex (28 species of Dubautia, Argyroxyphium, and Wilkesia, Asteraceae), the Hawaiian Alsinoideae (Schiedea and Alsinidendron, 26 species, Caryophyllaceae), Hedyotis (20 species, Rubiaceae), Myrsine (20 species, Myrsinaceae), and one colonist of Peperomia (20 species, Piperaceae).

Dimorphic colonists resulting in only dimorphic Hawaiian species account for 10% (29/291) of the colonists, suggesting that dimorphism is high in part because colonists were dimorphic (Table 2). Over half (111/201) of current dimorphic species arose from dimorphic colonists. Monomorphic colonists resulting in only monomorphic species constitute 82% (238/291) of the colonists. Of the colonists leading to endemic [TABULAR DATA FOR TABLE 2 OMITTED] species, 11% (19/173 colonists) were dimorphic and gave rise to only dimorphic species. Of the indigenous colonists, 8% (10/119 colonists) were dimorphic. Colonists that gave rise to endemic species were no more likely than indigenous colonists to be dimorphic (N = 285, [mean] = 0.64, df = 1, P = 0.43).

Although 10% of the colonists were dimorphic, 20.7% of current species are dimorphic, indicating that either dimorphic lineages have led to more species/ colonist, or that dimorphism has arisen autochthonously [TABULAR DATA FOR TABLE 3 OMITTED] (in situ). Our analysis suggests that the latter is true; approximately one-third (31.8%) of current dimorphic species arose from monomorphic colonists. At least 12 monomorphic colonists evolved dimorphism autochthonously [the Hawaiian Alsinoideae (Schiedea), Bidens, Broussaisia, Cyrtandra, Hedyotis, Neraudia, Perrottetia, 2 Psychotria (Rubiaceae) colonists, Psydrax, Santalum, and Wikstroemia (Table 3)]. In Neraudia, dioecy appears to have evolved from monoecy. In the two Psychotria colonists, separate sexes probably were derived from heterostyly. In the other nine colonists, separation of the sexes appears to have evolved from hermaphroditism or in lineages with hermaphroditism and gynodioecy. All 12 of these lineages (with the exception of Psydrax) contain only endemic species. In five other cases, dimorphism may have evolved from monomorphism, but we have conservatively listed the breeding system of the colonist as unknown (Table 3).

Other colonists had changes in breeding system within monomorphic or within dimorphic systems (Table 3). In two cases [Rhus (Anacardiaceae) and Melicope (Rutaceae)], evolution in the opposite direction apparently has occurred, and hermaphroditism has arisen from a presumably functionally dimorphic ancestor.

Lineage size was similar for dimorphic colonists that gave rise to only dimorphic species ([mean] = 2.3 dimorphic species/colonist) and monomorphic colonists that gave rise to only monomorphic species ([mean] = 2.9 monomorphic species/colonist; Fig. 1), but the 12 monomorphic colonists that gave rise to dimorphic species were significantly different in lineage size ([mean] = 9.25 species/ colonist, Fig. 1; N = 267, df = 2, [mean] = 11.0, P = 0.004, Kruskal-Wallis test). A number of colonists with unknown breeding systems could affect this latter distribution if they were to be included. Because of this, we did not try to distinguish why the lineages that evolved dimorphism were apparently larger. Lineages that evolved dimorphism may be larger because factors associated with speciation may also favor the evolution of dimorphism in species-rich lineages. Alternatively, each species may have a similar probability of evolving dimorphism regardless of lineage size, and thus larger lineages will tend to have more autochthonous evolution of dimorphism, simply because they have more species.

DISCUSSION

Our work shows that the incidence of dioecy in the Hawaiian Islands is not as high as originally estimated, but remains the highest of any flora where similar data are available. The percentage of dioecious species is slightly higher than that of New Zealand (12-13%), another insular flora with some tropical elements (Godley 1979, Webb and Kelly 1993). The high incidence of dioecy in the Hawaiian Islands is the result of a number of dimorphic colonists as well as autochthonous evolution of dimorphism within the archipelago. Of the 291 presumed colonists, 10% were dimorphic, considerably higher than the worldwide average for dioecy of [approximately equal to]4% (Yampolsky and Yampolsky 1922). Over half of the native Hawaiian flora has Malesian, Austral, or Pacific affinity (Fosberg 1948; W. L. Wagner, unpublished data), and this higher percentage of dioecy may reflect a higher incidence of dimorphism in the source floras, although these areas (especially Malesia) are not well studied. Other sources include pantropical elements as well as temperate areas (North America, Australia, New Zealand) and a few boreal elements (Wagner et al. 1990). Further studies of breeding systems (particularly in tropical source floras) are needed to determine if dioecious colonists are over-represented relative to the source flora, or conversely, if hermaphroditic taxa are disproportionately represented as colonists, as predicted by Baker's (1967) law. The number of dimorphic colonists to the Hawaiian Islands, however, suggests that dioecy has not been a severely limiting factor in dispersal and colonization of the Hawaiian Islands. Lloyd (1985) also found that most of the dimorphism in the New Zealand flora resulted from dimorphic colonists; only 5 of the 72 dimorphic genera were the result of autochthonous evolution of dimorphism.

The high incidence of dimorphism in the Hawaiian Islands has not resulted from different rates of speciation of dimorphic and monomorphic colonists as suggested by Bawa (1982), at least as measured by the current number of species per colonist. Two-thirds of the colonizations resulted in only one species, but in a few notable cases (Asteraceae, Campanulaceae, Caryophyllaceae, Lamiaceae, Myrsinaceae, Rubiaceae, and Rutaceae), colonizations have led to a remarkable number and diversity of species, for both dimorphic and monomorphic colonists. Carlquist (1974: 526) reported that the average number of species per genus was twice as great in dioecious genera as the flora at large; in contrast, we found similar numbers of species per genus for monomorphic and dimorphic genera, with apparently more species per colonist in lineages where dimorphism has arisen in situ. This difference related in part to taxonomic differences in the data sets used. Further studies are needed to elucidate whether evolution of dimorphism has been associated with changes in addition to breeding system that resulted in greater speciation in these lineages than in lineages of colonists that did not evolve dimorphism.

Although over half of the dimorphism in current species is the result of dimorphic colonists, selective pressures have presumably been sufficient to promote a diversity of pathways to dimorphism in the Hawaiian flora, and about one-third of the dimorphic species occur in lineages from a monomorphic colonist. Dioecious and dimorphic breeding systems apparently have been derived from heterostyly, from monoecy, or most commonly directly from hermaphroditism or from hermaphroditism via gynodioecy. In two cases, hermaphroditism apparently arose from a functionally dimorphic ancestor. Further study of the presumed colonist, phylogeny, and breeding system of these taxa (Rhus, Melicope) is needed. In general, the assumption has been that evolution of breeding systems away from dioecy is extremely difficult, and very few cases of this have been documented [e.g., androdioecy from dioecy in Datisca (Datiscaceae), Rieseberg et al. 1992]. Hermaphroditic plants in some Hawaiian populations of Wikstroemia (Thymeliaceae) may be secondarily derived as hybrids from individuals with different modes of control of dioecy or from the breakdown of dioecy (Mayer and Charlesworth 1992). Within the Hawaiian Alsinoideae, some species may have secondarily evolved hermaphroditism from gynodioecious ancestors (Wagner et al. 1995, Weller et al. 1995). Strong self-incompatibility in the Hawaiian flora is known only in one lineage of the Hawaiian Madiinae (Compositae; Carr et al. 1986). In general, the evolution of dioecy and the apparent lack of self-incompatibility in the endemic flora support the notion that dioecy may be easier to evolve than self-incompatibility (Thomson and Barrett 1981, Charlesworth 1985), although few Hawaiian taxa have been investigated for the occurrence of self-incompatibility.

The limited number of lineages comprising the Hawaiian angiosperm flora also creates a unique opportunity for detailed studies within lineages of the number of independent origins of dioecy and associated traits (e.g., Sakai et al. 1995, Wagner et al. 1995, Weller et al. 1995). Better knowledge of phylogenetic patterns and further ecological studies, particularly within those groups evolving dioecy autochthonously, are needed to determine causality.

ACKNOWLEDGMENTS

This work was supported in part by NSF grants BSR88-17616, BSR89-18366, DEB92-07724 (S. G. Weller and A. K. Sakai, Co-P.I.s), with a Research Experience for Undergraduates supplement for D. M. Ferguson. It was also supported by a Smithsonian Institution Scholarly Studies grant to W. L. Wagner. We wish to thank R. Shannon for help with word-processing, F. Ganders for providing information on Bidens, and S. Mayer for information on Wikstroemia, S. Weller for helpful comments throughout the project, and D. Charlesworth, J. Brunet, and V. Eckhart for manuscript review.

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Date:Dec 1, 1995
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