Polyploidy and gender dimorphism.

Miller and Venable (1) claimed that polyploidy is a “trigger of unrecognized importance” for the evolution of gender dimorphism, an idea originally proposed by Jennings (2) and Baker (3). In our opinion, their phylogenetic analysis of North American Lycium (Solanaceae) does not support the claimed associations between polyploidy, self-fertility, and gender dimorphism. There is no support (bootstrap ,50%) for the sister group to the gynodioecious clade, and collapsing the nodes supported by ,50% bootstrap results in an unresolved polytomy at the base of Lycium 1 Grabowskia. Thus, the inferred ancestral state for the gynodioecious clade may not even be self-incompatibility. The limited taxonomic sampling, which encompassed 13 of some 100 species of Lycium, and limited geographic sampling, which included no Asian, African, or Australian species of Lycium, further reduces confidence in the published topology. And only a single concurrent origin of dimorphism and polyploidy was hypothesized, which makes it difficult to assess the temporal order and statistical significance of the character changes. As evidence for self-compatibility, Miller and Venable cited a greater proportion of selfed pollen tubes at the base of the style in dimorphic species relative to cosexuals [figure 4 of (1)], but they did not give the total number of pollen tubes reaching the base. Because the hermaphrodites of the dimorphic species specialize as males and set very few seeds, however, the total number of pollen tubes reaching the base of the style is likely to differ substantially between the cosexual and dimorphic species. Consequently, the log ratio of outcross to self pollen tubes reaching the base of the style is also likely to differ, and self-compatibility will easily get confounded with gender specialization in the hermaphrodites of the dimorphic species. Self-incompatibility and dioecy are known to occur in genera (4) not mentioned in table 1 of (1). Moreover, in half of the genera presented in that table, the ancestor may be polyploid rather than diploid. Miller and Venable mentioned 37 related pairs of taxa where polyploidy disrupted self-incompatibility, yet they do not discuss the frequency of gender dimorphism in these taxa. The authors claim that the combined appearance of polyploidy and consequent loss of self-incompatibility play an important role in the evolution of gender dimorphism. To demonstrate the importance of the pathway with both loss of self-incompatibility and polyploidy in the evolution of gender dimorphism, however, it is not sufficient to demonstrate that the pathway exists, as Miller and Venable have done in table 1 of (1). Instead, one must also demonstrate that gender dimorphism arises more frequently via this pathway than via other pathways. Self-incompatibility systems have been lost repeatedly, often in the absence of polyploidy (5). Indeed, theoretical modeling and empirical evidence both suggest that inbreeding depression is stronger in diploid than in polyploid species (6, 7). Hence, male sterile mutants would be even more likely to invade in diploid than in polyploid species that have lost selfincompatibility. Figure 1 schematically illustrates this issue. If gender dimorphism is equally or more frequently associated with self-compatible diploid taxa than with self-compatible polyploid taxa (each being derived from self-incompatible diploid ancestors), as depicted in Fig. 1A, the result suggests that the loss of self-incompatibility but not polyploidy is important in the evolution of gender dimorphism. If, by contrast, gender dimorphism is equally or more frequently associated with polyploid self-incompatible taxa than with polyploid self-compatible taxa (both derived from diploid selfincompatible ancestors), as depicted in Fig. 1B, the result suggests that polyploidy but not loss of self-incompatibility is important in the evolution of gender dimorphism. Johanne Brunet Aaron Liston Department of Botany and Plant Pathology Oregon State University Corvallis, OR 97331–2902, USA E-mail: [email protected]