Evolution of Unisexuality in the Hawaiian Flora: A Test of Microevolutionary Theory

Abstract

Abstract.-The evolution of separate sexes as a means of avoiding self-fertilization requires the controversial coexistence of large inbreeding depression and high selfing rate in the ancestral hermaphrodite population. Fitness components of adult females and hermaphrodites in nature, of their open-pollinated progeny, and of experimental selfs and outcrosses onto hermaphrodites were compared in endemic Hawaiian Bidens sandvicensis, all of whose known populations are gynodioecious, consisting of a mixture of females and hermaphrodites. Multilocus selfing rates of hermaphrodites were also estimated, and sex morph ratio monitored over four seasons in three populations of B. sandvicensis and one population of gynodioecious B. cervicata. Total mean inbreeding depression in seed set (in the glasshouse), germination rate (in an open-air nursery on Kauai), and first year survivorship and fecundity in the field were estimated as 0.94 (SE 0.04), and occurred primarily in drought months. Lower survivorship and fecundity of selfs were partially explained by their consistently smaller size. Open-pollinated seed of females had significantly lower germination rate, proportion flowering, and fecundity than outcrossed progeny of hermaphrodites, suggesting moderate biparental inbreeding in females and a lack of any non-outcrossing advantage to progeny of females. In all fitness components, open-pollinated progeny of hermaphrodites were inferior to those of females and to outcrosses, and in most components were superior to selfs. Total performance of open-pollinated progeny of females relative to those of hermaphrodites was calculated as 2.3 (SE = 0.4), but since inflorescences of females also set 20% to 50% more seed than those of hermaphrodites, their total relative ovule success was estimated as 3.2 (SE = 0.5). If inheritance of male sterility is nuclear, this superiority is sufficient to maintain females in frequencies over 20% in populations, whose actual frequencies ranged from 14% to 33%. In four populations, selfing rates of hermaphrodites, assayed in seedlings, were 0.50, 0.45, 0.25, and 0.30, but since substantial inbreeding depression occurred prior to germination, the mean selfing rate of hermaphrodite ovules exceeded 0.57. Female frequencies were significantly higher in the two populations with higher hermaphrodite selfing rate. These results suggest that inbreeding depression can exert a profound influence on the mating system of self-compatible plants on Hawaii and perhaps other oceanic islands, and can be sufficiently strong to electively favor the elimination of the male function.

Outcrossing rates and inferred levels of inbreeding depression in gynodioecious Cucurbita foetidissima (Cucurbitaceae)

“…However, our data showing high rates of inbreeding depression despite frequent self-fertilization are consistent with estimates of inbreeding depression and outcrossing rates in at least one other gynodioecious perennial (Bidens sandvicensis; Schultz & Ganders, 1995) and in many other plants with more conventional breeding systems. Husband & Schemske (1995) compiled estimates from the literature on inbreeding depression and its correlation with outcrossing rate and life history (annual, shrubby perennial, woody perennial).…”

“…In their study, as in this one, inbreeding depression values measured by the experimental approach were lower than those estimated by electrophoresis, although both approaches suggested that the fitness consequences of selfing were severe. In Bidens sandvicensis, the mean level of inbreeding depression measured experimentally was 0.91 whereas electrophoretic evidence indicated no excess homozygosity relative to Hardy-Weinberg expectations among adult plants despite populationlevel selfing rates averaging 0.61 (Schultz & Ganders, 1995). Thus inferred levels of inbreeding depression in Bidens, if calculated, would not differ from unity and would slightly exceed values measured experimentally.…”

“…While this difference was not statistically significant, it could indicate that seeds of females suffer some deleterious effects of biparental inbreeding. In gynodioecious Hawaiian Bidens, Schultz & Ganders (1995) also found slightly lower fitness of naturally pollinated seeds from females compared with those from crossfertilized hermaphrodites whereas both seed types had considerable fitness advantages over seifed seeds. Using hand-pollinations among siblings, Ashman (1992) demonstrated that biparental inbreeding could significantly reduce the fitness of seeds produced by females of gynodioecious Sidalcea oregana spp.…”

“…While the combined effects of selfing and inbreeding depression appear to contribute strongly to the maintenance of females in C. foetidissima, this is by no means a general result in studies of gynodioecious taxa. Inbreeding depression appears to play a leading role in the maintenance of females in gynodioecious Bidens (Schultz & Ganders, 1995) and Shiedea (Sakai et a!., 1989). However, in many other gynodioecious species, females gain advantages from either maternal effects on seed survival or from direct benefits of male sterility genes on survival, growth and reproduction rather than through inbreeding avoidance (see for example van Damme & van Delden, 1984;Shykoff, 1988;Delph 1990a,b;Ashman, 1992;Eckhart, 1992).…”

Mating system, sex ratio, and persistence of females in the gynodioecious shrub Daphne laureola L. (Thymelaeaceae)

“…Furthermore, stable persistence of male-sterility factors in the absence of a fecundity advantage would require a combination of very high levels of inbreeding depression and extensive hermaphrodite selfing (Lloyd, 1975;Charlesworth and Charlesworth, 1978). Simultaneous occurrence of extensive selfing of hermaphrodites and high inbreeding depression has also been reported for other gynodioecious plants like Plantago coronopus (Wolff et al, 1988), Cucurbita foetidissima (Kohn, 1988;Kohn and Biardi, 1995), Bidens sandvicensis (Schultz and Ganders, 1996), and Schiedea adamantis (Sakai et al, 1997). Results of this study are fully consistent with these expectations and indicate that explanations for the persistence of females in gynodioecious D. laureola need not be sought beyond the conventional theoretical framework.…”