Origins of dioecy in the Hawaiian flora

Ecology, Dec, 1995 by Ann K. Sakai, Warren L. Wagner, Diane M. Ferguson, Derral R. Herbst

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.