POLLINATION SYSTEMS, DISPERSAL MODES, LIFE FORMS, AND DIVERSIFICATION RATES IN ANGIOSPERM FAMILIES

An important aspect of evolution in higher order taxa, such as mammals, molluscs, and plants, is the rate of diversification (R), i.e., the rate at which the number of species increases over evolutionary time (Darwin, 1859; Simpson, 1944; Mayr, 1963; Pieiou, 1979; Stanley, 1979, 1989). Stanley (1979) presented an extensive summary and analysis of data pertaining to this issue, and he advocated two tentative causal mechanisms behind variation in R among taxa. First, R should increase in association with increased "adaptive complexity. " The occurrence of complex behavior, of any kind, increases the rate of speciation because it fosters reproductive isolation. On the other hand, adaptive complexity also promotes extinction risk due to ecological specialization. This implies increased species turnover, which is characteristic for lineages with high R (Stanley, 1979). A similar idea was mentioned by Darwin (1859) as an explanation for the difference in evolutionary rate he perceived between terrestrial and marine organisms, the former ones exhibiting higher rates than the latter ones. Second, increased dispersal ability should decrease R. There are two rationales for this mechanism. Speciation rate is expected to decrease with increased dispersal ability because geographic isolation is not easily maintained ifspecies disperse widely (Mayr, 1963). Furthermore, dispersal ability correlates positively with species longevity (Mayr, 1963; Jackson, 1974), and species longevity is in turn inversely related to R (Stanley, 1979). In comparison with some animal taxa, the diversification rates exhibited by angiosperms are poorly known. They were not included in Stanley (1979), and only a few attempts have been made to estimate R values for higher plants (Niklas et aI., 1985). Despite the scarcity ofconclusive evidence, several authors have suggested reproductive and life form features associated with high diversification rates among angiosperms. Grant (1949) argued that pollination by animals is a prevalent isolating mechanism between plant species. Occurrence of"faithful pollinators" would thus promote species diversification (Stebbins, 1981; Crepet, 1984). In the fossil record, insect pollination is associated with angiosperm diversification during Late Cretaceous and Early Tertiary (Friis and Crepet, 1987; Crepet and Friis, 1987). The "insect (animal) pollination hypothesis" was considered by Stanley (1979) as the "plant analogue" to the hypothesis that R increases in association with increased adaptive complexity. Under the assumption that pollination by animals is more efficient than wind pollination in sparse populations, Raven (1977) argued that animal pollinated plants would experience reduced extinction risks under conditions when population density becomes reduced. Regal (1977), Burger (1981), and Crepet (1984) further proposed that the combined effect of pollination by animals, and dispersal by animals, promotes species diversification because dispersal by animals would create a population structure in which animal pollination is advantageous. However, this proposal has some weaknesses. If local populations become isolated by distances exceeding the flight distances of pollinators, it is not obvious that animal pollination is advantageous compared with wind pollination. Furthermore, ifcross pollination does occur between widely scattered individuals, it might hinder rather than promote speciation (Stebbins, 1981). Apart from the suggested "animal pollination/animal dispersal" mechanism, the possession ofanimal dispersed seed, in itself, has been viewed as increasing species diversification rates. If dispersal by animals increases long distance dispersal, this would promote establishment of isolated populations in which speciation may take place (Snow, 1981; Tiffney, 1984, 1986). There is evidence that fruit dispersal by birds enhances long distance dispersal. Ridley (1930) described prevalence of fleshy fruited species on oceanic island. Moreover, in the family Rubiaceae, genera possessing drupes are over-represented both on oceanic islands and among genera with transoceanic distributions (Bremer and Eriksson, in press). In addition to reproductive features, the life form of plants might influence diversification rate. Short-lived plants, especially herbs, are expected to exhibit a high rate ofdiversification due to their comparatively short generation time (Tiffney, 1986). Furthermore, populations of short lived plants are often semi-isolated, occupy transient habitats, and experience unpredictable fluctuations, conditions that all may promote R (Levin, 1984; Niklas et aI., 1985). The empirical basis for scrutinizing the hypotheses