Abstract
Background and Aims The coexistence of hermaphrodites and female-sterile individuals, or androdioecy, has been documented in only a handful of plants and animals. This study reports its existence in the plant species Cardamine amara (Brassicaceae), in which female-sterile individuals have shorter pistils than seed-producing hermaphrodites.Methods Morphological analysis, in situ manual pollination, microsatellite genotyping and differential gene expression analysis using Arabidopsis microarrays were used to delimit variation between female-sterile individuals and hermaphrodites.Key Results Female sterility in C. amara appears to be caused by disrupted ovule development. It was associated with a 2.4- to 2.9-fold increase in clonal propagation. This made the pollen number of female-sterile genets more than double that of hermaphrodite genets, which fulfils a condition of co-existence predicted by simple androdioecy theories. When female-sterile individuals were observed in wild androdioecious populations, their ramet frequencies ranged from 5 to 54 %; however, their genet frequencies ranged from 11 to 29 %, which is consistent with the theoretically predicted upper limit of 50 %.Conclusions The results suggest that a combination of sexual reproduction and increased asexual proliferation by female-sterile individuals probably explains the invasion and maintenance of female sterility in otherwise hermaphroditic populations. To our knowledge, this is the first report of the coexistence of female sterility and hermaphrodites in the Brassicaceae.
Highlights
The occurrence of female-sterile individuals in hermaphroditic populations is extremely rare; in sexually reproducing populations this dimorphism is known as androdioecy (Darwin, 1877; Charlesworth, 1984; Pannell, 2002)
To test whether pistil length variation between floral morphs could be explained by delayed development in FS pistils, we observed 20 flowering ramets (10 FS and 10 H) from WP at intervals for 4 days after flower opening
Pistil length increased over this period in both morphs, FS pistils were always much reduced compared with their H counterparts (Table 2 line 3) and did not show any delayed maturation
Summary
The occurrence of female-sterile individuals (functional males) in hermaphroditic populations is extremely rare; in sexually reproducing populations this dimorphism is known as androdioecy (Darwin, 1877; Charlesworth, 1984; Pannell, 2002). Theoretical models of androdioecy explain its rarity by predicting that males must sire at least twice as many successful progeny as hermaphrodites (Lloyd, 1975a; Charlesworth and Charlesworth, 1978, 1981; Charlesworth, 1984) Despite these rather stringent conditions, several examples of androdioecious plants have been well documented [e.g. Datisca glomerata (Liston et al, 1990; Fritsch and Rieseberg, 1992; Weller and Sakai, 1999; Wolf et al, 2001); Sagittaria lancifolia (Muenchow, 1998) and Mercurialis annua (Pannell, 1997)]; interestingly, most of these examples appear to have evolved from dioecy through the spread of pollen-producing females rather than from a hermaphroditic ancestor through the spread of female-sterility mutations (reviewed in Pannell, 2002). Methods Morphological analysis, in situ manual pollination, microsatellite genotyping and differential gene expression analysis using Arabidopsis microarrays were used to delimit variation between female-sterile individuals and hermaphrodites
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