vol. 156, no. 3 the american naturalist september 2000 Lower Species Richness in Dioecious Clades Jana C. Heilbuth* Department of Zoology, University of British Columbia, have evolved as a mechanism to reduce inbreeding (Baker Vancouver, British Columbia V6T 1Z4, Canada 1959; Carlquist 1966, 1974; Charlesworth and Charles- worth 1978) and/or to improve resource allocation (Bawa Submitted October 6, 1999; Accepted April 6, 2000 1980; Givnish 1980). Various authors (Baker 1959; Wil- liams 1975) have argued that dioecy is an easier route to outbreeding, both genetically and physiologically, and em- pirical evidence suggests that it is a more ef®cient means abstract: Despite the extensive research on the potential bene®ts of avoiding inbreeding than gametophytic self-incompat- of dioecy to individuals, little is known about the long-term success ibility (Anderson and Stebbins 1984). As well, theoretical of dioecious lineages in relation to their hermaphroditic or mon- oecious relatives. This study reports on the evolutionary success of studies show that plants carrying a mutation conferring worldwide dioecious ¯ora in light of recent phylogenetic work by male or female sterility can be favored in a hermaphroditic performing sister-group comparisons of species richness between population (Charnov 1982) when a division of labor into clades of angiosperms with different breeding systems. Whether this males and females allows each individual to ful®ll its roles analysis is performed at the family or genus level, species richness more ef®ciently. is generally far lower in dioecious taxa when compared to their Despite the many possible advantages of dioecy, dioe- hermaphroditic or monoecious sister taxa. Despite the advantages » of avoiding inbreeding depression and of allocating resources sep- cious ¯ora comprise only 6% of the world's angiosperms arately to male and female function, dioecy in angiosperms does not (Renner and Ricklefs 1995). The low representation of appear to be a key innovation promoting evolutionary radiation. A dioecy is consequently a puzzle and might be caused by potential explanation for the low representation of dioecious lineages dioecious species experiencing a higher extinction rate, is that dioecious plants may have lower colonization rates. Baker's lower speciation rate, high reversion rates back to the Law states that self-compatible lineages will have higher rates of monomorphic state (Richards 1997), or low origination successful long-range dispersal since they do not require a mate; rates. A possible explanation for the low representation of consequently, self-compatible lineages may have higher rates of al- lopatric speciation. However, identical analyses performed with her- dioecy might be that a recent environmental shift has fa- maphroditic self-incompatible angiosperms did not produce similar vored the evolution of dioecy so that dioecious groups are results, suggesting that Baker's law is not the reason for the poor fairly young but not necessarily speciating or going extinct representation of dioecy among angiosperm species. at different rates. This explanation would agree with the commonly held belief that dioecy occurs mostly on the Keywords: Baker's law, dioecy, extinction, sister-group comparison, speciation. tips of phylogenetic trees as they ªare usually more closely related to hermaphrodite species within their own genus or family than they are to each otherº (Lebel-Hardenack Dioecy, the separation of male and female function into and Grant 1997, p. 130.). This study is the ®rst to examine separate individuals, is taxonomically distributed among whether the infrequent occurrence of dioecy among an- most of the major orders of angiosperms, both primitive giosperms is due to a series of recent adaptations that arise and advanced (Thomson and Barrett 1981). Although on the tips of trees. Using phylogenetic evidence, I per- there has been considerable discussion regarding the evo- formed sister-group comparisons of species richness using lutionary forces leading to dioecy in plants (e.g., Carlquist clades that are entirely or mostly dimorphic (those with 1966, 1974; Bawa 1980; Thomson and Brunet 1990), little dioecious, polygamodioecious, gynodioecious, or sub- work has been done to determine whether dioecy is a dioecious breeding systems; see table 1 for terms) as the bene®cial evolutionary strategy. Dioecy is hypothesized to focal group and monomorphic lineages (those with bi- sexual, monoecious, andromonoecious, gynomonecious, * E-mail: [email protected]. or polygamomonoecious breeding systems) as the sister Am. Nat. 2000. Vol. 156, pp. 221±241. q 2000 by The University of Chicago. group to identify whether dioecious clades are more or 0003-0147/2000/15603-0001$03.00. All rights reserved. less species rich than their hermaphroditic sister taxa. A 222 The American Naturalist sister-group comparison (®g. 1) uses a phylogeny to de- termine the difference in number of species between a focal group (in this case, a dimorphic clade) and its sister group (a monomorphic clade). If dioecy is a recent ad- aptation, then both the dimorphic and the monomorphic clades in the sister-group comparison should be small but equally species rich. These sister-group comparisons were performed at the family and generic levels and, at both levels of analysis, dioecious clades were found to be far less species rich than their nondioecious sister groups, in- Figure 1: A sister-group comparison. Focal group and sister group have dicating that dioecious lineages have lower speciation rates existed for the same amount of time (i.e., since their divergence from a common ancestor) and, hence, should have equal numbers of species on and/or higher extinction rates. average unless the trait in question (here, dimorphic breeding system) The possibility that dioecious lineages experience low- has a direct or indirect effect on speciation and/or extinction rates. ered speciation rates is consistent with Baker's law (Baker 1953), which states that a self-compatible hermaphrodite will be a better colonizer than a dioecious plant owing to were as species rich as their sister groups, implying that the fact that it does not need a mate. Long-range dispersers Baker's law is not a large factor in determining divergence can found new populations that may diverge and form rates. new species allopatrically. If dioecious populations accom- The evidence gained in this study agrees with studies plish this long-range dispersal less often than hermaph- done on local ¯ora, such as that on the Hawaiian ¯ora roditic populations, it could potentially lead to a lower (Sakai et al. 1995a), which suggest that Baker's law does speciation rate among dioecious clades. To examine this not reduce the amount of dioecious colonizers. In fact, possibility, I have again used the sister-group comparison Sakai et al. (1995b) found that the high proportion of approach, this time using self-incompatible taxa as the dioecious ¯ora in Hawaii is due in part to a dispropor- focal group against self-compatible sister taxa. Self-incom- tionately high (»10%) percentage of dioecious colonizers. patibility is achieved in approximately half of the non- However, our results do differ from those of Sakai et al. dioecious angiosperms through a variety of morphological (1995b) in that their comparisons of lineage size in the (e.g., heterostyly) and molecular (e.g., gametophytic and Hawaiian Islands show no trend for higher extinction rates sporophytic self-incompatibility) means. Self-incompati- or lower speciation rates: dimorphic genera are as species ble species are subject to the same dif®culties as dioecious rich as monomorphic genera. Several factors may con- ones when dispersing to a new area where mates may be tribute to dioecy being relatively more successful on the either nonexistent or in short supply. If Baker's law plays Hawaiian Islands. The prevalence of dioecy has been a large role in determining diversi®cation rates, these in- shown to be correlated with tropical environments (Ren- compatible groups should also show lowered species rich- ner and Ricklefs 1995), a correlation that may result from ness than dioecious clades do when examined phyloge- dioecious species having higher speciation rates or lower netically using the same methods. However, this study extinction rates in tropical environments. Furthermore, found no evidence for this as the self-incompatible lineages the numbers of dimorphic and monomorphic species on Table 1: Quick reference for breeding systems in angiosperms Breeding system De®nition Dimorphism: Dioecy Male and female plants Gynodioecy Hermaphroditic and female plants Androdioecy Hermaphroditic and male plants Subdioecy Hermaphroditic, male, and female plants Polygamodioecy Synonymous with subdioecy Monomorphism: Hermaphroditism Bisexual ¯owers Monoecy Male and female ¯owers on each plant Andromonoecy Male and bisexual ¯owers on each plant Gynomonoecy Female and bisexual ¯owers on each plant Polygamomonoecy Male and/or female and bisexual ¯owers on each plant Polygamous Polygamomonoecious and/or polygamodioecious Lower Species Richness in Dioecious Clades 223 Hawaii may not re¯ect long-term expectations given the found by referring to Takhtajan (1997). When this source relatively recent (maximum 5.7 MYA; MacDonald et al. was ambiguous, other sources were found, usually that 1983) nature of the present-day islands. For example, di- given on the DELTA Web site (Watson and Dallwitz 1992) oecious plants may be more successful