The ecology and evolution of gender strategies in plants: the example of Australian Wurmbea (Colchicaceae)

Abstract

Angiosperms possess diverse sexual systems, often with different combinations of hermaphroditic, pistillate and staminate flowers. Despite this sexual diversity, most populations are either monomorphic or dimorphic with respect to gender strategy, where gender refers to the relative contribution that individuals make to fitness through female and male function. An important problem in evolutionary biology is to determine how and why variation in gender strategies originates and is maintained. Wurmbea (Colchicaceae), a genus of insect-pollinated geophytes, has recently become the focus of ecological and evolutionary studies aimed at understanding these issues. Phylogenetic reconstructions suggest dispersal from Africa to Australia, then New Zealand, and multiple transitions between monomorphic and dimorphic sexual systems within Australia. Microevolutionary studies of W. dioica and W. biglandulosa, two wide-ranging taxa with monomorphic and dimorphic populations, provide insights into the selective mechanisms governing transitions between sexual systems. Dimorphic populations of these taxa likely comprise independent origins of dimorphism via the gynodioecious pathway by invasion of females into monomorphic populations. Shifts in pollination biology and flower size, and their consequent effects on mating patterns, may have contributed to the evolution of gender dimorphism. Pollinator-mediated selfing and inbreeding depression provide a sufficient fertility advantage for females to be maintained in dimorphic populations. Once dimorphism establishes, increasing gender specialisation is associated with invasion of more arid environments. Inbreeding avoidance, particularly under stressful ecological conditions, is the most likely selective mechanism maintaining gender dimorphism in Wurmbea. We conclude our review by suggesting avenues for future research that might provide a more comprehensive picture of the evolution of gender strategies in Wurmbea.

A Phylogenetic Study of Evolutionary Transitions in Sexual Systems in AustralasianWurmbea(Colchicaceae)

“…These findings, in conjunction with population-level studies, can support hypotheses that specific ecological factors favor transitions from gender monomorphism to dimorphism (reviewed in Ashman 2006; Barrett and Case 2006). If our plastid-based estimate of phylogeny represents species relationships accurately, then there were numerous transitions in sexual system in the Australian clade of Wurmbea.…”

“…biglandulosa and I. novae-zelandiae. This is not surprising, given the extensive sexual inconstancy within Wurmbea species (Barrett et al 1999;Ramsey and Vaughton 2001;Barrett and Case 2006). It would be interesting to know what features of Australian Wurmbea biology make the clade so unusually sexually labile.…”

“…48 species of perennial, geophytic herbs (Nordenstam 1978(Nordenstam , 1986(Nordenstam , 1998Macfarlane 1980Macfarlane , 1986Macfarlane , 1987Bates 1995Bates , 2007Macfarlane and van Leeuwen 1996)-has drawn much recent attention (Barrett 1992;Vaughton and Ramsey 1998, 2003, 2004Barrett et al 1999;Case and Barrett 2001, 2004a, 2004bJones and Burd 2001;Vaughton 2001, 2002;Barrett and Case 2006;Ramsey et al 2006aRamsey et al , 2006b. Most of this work has been conducted on Wurmbea dioica and Wurmbea biglandulosa, two wide-ranging polymorphic species that exhibit considerable intraspecific variation in sexual systems, including hermaphroditism, gynodioecy, subdioecy and dioecy (Barrett 1992;Vaughton and Ramsey 2002;Case and Barrett 2004a).…”

Cryptic species in Pagamea coriacea sensu lato (Rubiaceae): evidence from morphology, ecology and reproductive behavior in a sympatric context

“…The sexual systems of both groups, with pistillate, staminate and hermaphroditic plants, can be characterized as a transition from dioecious to gynodioecious systems (Barrett and Case 2006). While "pistillate" plants were completely unisexual, the fruit production by "staminate" plants, and the individual with hermaphroditic and homostylous flowers, may represent a reversal in the sterility of the gynoecium, and a transition from unisexual condition to hermaphroditism.…”

Does inbreeding avoidance maintain gender dimorphism in Wurmbea dioica (Colchicaceae)?

“…The genus Wurmbea (Colchicaeae) consists of about 47 species of small, insect‐pollinated geophytes occurring in temperate Africa and Australia. African species are uniformly cosexual, whereas at least 10 of the approximately 30 Australian taxa are gender dimorphic (Macfarlane, 1987; Barrett & Case, 2006). Recent phylogenetic work indicates that gender dimorphism in Wurmbea has probably evolved independently on several occasions (A. L. Case, S. W. Graham, T. D. Macfarlane and S. C. H. Barrett, unpublished data).…”