Mixed mating systems and gynodioecy in Hawaiian Bidens

Abstract

All species of Bidens endemic to the Hawaiian Islands evolved from a single common ancestor through adaptive radiation. Morphological differentiation among these species includes differences in floral features which influence their mating systems. Twelve taxa of Hawaiian Bidens were studied to assess the extent of variation in floral features. Outcrossing rates were estimated for 15 populations of eight species using allozyme gene markers in progenies. All species studied had intermediate outcrossing rates ranging from 58.0%-72.8%. Outcrossing rate was not correlated with flower size, degree of protandry or seed set in the absence of pollinators, but did appear to be correlated with inflorescence type. Strong protandry efficiently prevents self-fertilization within flowers, but numerous simultaneously flowering heads promote geitonogamy, which brings about a substantial level of selfing. The intermediate rates of self-fertilization in all species studied do not support the prediction of a bimodal distribution of outcrossing rates by Lande and Schemske (1985). The amount and structure of genetic variation was investigated using allozyme data for 21 populations of ten species of Hawaiian Bidens. Genetic variation within populations was low. Genetic identities among populations was high, probably because of their common ancestry. For the three commonly polymorphic loci, Pgi-1, Pgi-2, and Skdh-3, there was a substantial amount of genetic differentiation among populations. This suggests that founder effects as well as the mating system have influenced the distribution of genetic variation. There was a significant heterozygote deficiency at one or more allozyme loci in most populations in comparison with the Hardy-Weinberg expectations. The heterozygote deficiency was primarily caused by inbreeding, but a 'heterozygosity paradox' was also detected in these populations, suggesting the effect of other evolutionary factors on genetic structure of Bidens populations. Thirteen of the 27 taxa of Hawaiian Bidens are gynodioecious. Abortion of microsporogenesis in females is caused by an early abnormal vacuolation of tapetal cells which leads to premeiotic degeneration of microspore mother cells. Microsporogenesis was developmentally similar in all nine taxa studied. Genetic studies provided evidence that male sterility is controlled by two recessive nuclear genes, and these genes are allelic in all gynodioecious species. Cytoplasmic factors are apparently also involved. Both developmental and genetic data suggest that male sterility in Hawaiian Bidens is homologous. The evolution of gynodioecy most likely occurred autochthonously, and all gynodioecious taxa are probably the products of adaptive radiation of one ancestral gynodioecious species. In gynodioecious populations, females must have some selective advantage to counteract the disadvantage caused by reducing the fitness of male gametes to zero. Theoretical studies of the maintenance of gynodioecy hypothesize that females are maintained because of their outcrossing advantage or reproductive superiority as seed parents. There was a significant correlation between selfing rates of hermaphrodites and frequencies of females in eight gynodioecious populations of Hawaian Bidens. This result provides the first empirical evidence that supports the outcrossing hypothesis. Heterozygosity at allozyme loci was higher in the progenies of females than in the progenies of hermaphrodites. I conclude that females are maintained in gynodioecious populations because of their obligate outcrossing, and the consequence of gynodioecy is that it raises the levels of outcrossing and heterozygosity in self-compatible populations. However, estimated selfing rates of hermaphrodites cannot by themselves account for the observed high frequencies of females in these populations. Females must have some additional selective advantage. Measurement of several fitness components of the two sexes failed to reveal significant differences in most cases. Information on the relative fitness of the two sexes in nature is needed to understand the maintenance of females in gynodioecious species of Hawaiian Bidens.