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Family Affiliation, Sex Ratio and Sporophyte Frequency in Unisexual Mosses bs_bs_banner Botanical Journal of the Linnean Society, 2014, 174, 163–172. With 2 figures Family affiliation, sex ratio and sporophyte frequency in unisexual mosses IRENE BISANG1*, JOHAN EHRLÉN2, CHRISTIN PERSSON1 and LARS HEDENÄS1 1Department of Botany, Swedish Museum of Natural History, Box 50007, SE – 104 05 Stockholm, Sweden 2Department of Ecology, Environment and Plant Sciences, University of Stockholm, SE – 106 91 Stockholm, Sweden Received 17 June 2013; revised 24 August 2013; accepted for publication 1 November 2013 Patterns of sex expression and sex ratios are key features of the life histories of organisms. Bryophytes are the only haploid-dominant land plants. In contrast with seed plants, more than half of bryophyte species are dioecious, with rare sexual expression and sporophyte formation and a commonly female-biased sex ratio. We asked whether variation in sex expression, sex ratio and sporophyte frequency in ten dioecious pleurocarpous wetland mosses of two different families was best explained by assuming that character states evolved: (1) in ancestors within the respective families or (2) at the species level as a response to recent habitat conditions. Lasso regression shrinkage identified relationships between family membership and sex ratio and sporophyte frequency, whereas environ- mental conditions were not correlated with any investigated reproductive trait. Sex ratio and sporophyte frequency were correlated with each other. Our results suggest that ancestry is more important than the current environment in explaining reproductive patterns at and above the species level in the studied wetland mosses, and that mechanisms controlling sex ratio and sporophyte frequency are phylogenetically conserved. Obviously, ancestry should be considered in the study of reproductive character state variation in plants. © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174, 163–172. ADDITIONAL KEYWORDS: bryophytes – phylogeny – plant sex ratio regulation – pleurocarpous mosses – sex expression – wetlands. INTRODUCTION that the optimal sex ratio should depend on the environment through effects on resource availability Patterns of sex expression and sex ratios are key and population densities. Mechanisms through which features of the life histories of organisms (e.g. Hardy, organisms can influence functional sex ratios and 2002). Sex allocation theory assumes a trade-off thereby adjust to altered conditions vary widely between the allocation of resources to the two sexual among groups of organisms and depend on their functions (e.g. Campbell, 2000) and predicts that rela- breeding systems and life histories (Hardy, 2002; tive allocation to male and female functions should West, 2009). Factors controlling sex ratios in uni- depend on resource availability and opportunities for sexual flowering plants include selfish genetic ele- mating. Under conditions of local mate competition, a ments, sex ratio distorters and pollination intensity, female-biased allocation is usually favoured. Resource which primarily have an effect on seed sex ratio, limitation should result in the overproduction of the whereas gender-specific mortalities or reproductive dispersing sex (usually males), whereas unlimited costs mainly affect later life cycle stages (Taylor, 1999; resources predict disproportionate parental allocation de Jong & Klinkhamer, 2002; Stehlik & Barrett, 2005, towards the philopatric sex (e.g. Hjernquist et al., 2006; Barrett et al., 2010). Although the environmen- 2009; West, 2009). In dioecious organisms, this means tal conditions influencing optimal sex ratios are likely to vary over many spatial and temporal scales, the *Corresponding author. E-mail: [email protected] ability of species to respond to these varying condi- © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174, 163–172 163 164 I. BISANG ET AL. tions will depend on how genetically flexible are the et al., 2000; Fuselier & McLetchie, 2004; Benassi sex-regulating mechanisms. If mechanisms are fixed, et al., 2011). Finally, Rydgren, Halvorsen & Cronberg we would expect sex ratios to be relatively constant (2010) used a modelling approach and proposed that among species and to often represent traits that rare sporophyte production causes low costs of repro- evolved in a common ancestor, i.e. to be correlated at duction for female plants, and thus a female-biased taxonomic levels higher than the species level. If sex ratio can be maintained (but see Bisang, Ehrlén & sex-regulating mechanisms are more flexible, either Hedenäs, 2006). This is contrary to the prevailing line as a result of phenotypic plasticity or of relatively of reasoning, which suggests that rare sporophyte recent and easily evolving genetic changes, we would formation is an effect of the female bias, i.e. of male expect to see a stronger correlation with the present rarity (e.g. Longton & Schuster, 1983). environmental conditions. There is evidence that mechanisms determining sex To achieve a broad understanding of the factors ratios in plants are heritable (e.g. Shaw & Beer, 1999; influencing sex expression and sex ratios, we need to Stehlik et al., 2007) and could have evolved as a investigate patterns over a wide spectrum of organ- response to either extant or ancient environmental isms. We selected bryophytes (mosses, liverworts and conditions (Barrett, 2002; Field et al., 2013). Renner hornworts) because they possess a suite of reproduc- & Ricklefs (1995) found the dioecious breeding system tive characteristics that are unique or rare among in flowering plants to be concentrated in certain green land plants, which makes them particularly superorders and subclasses, suggesting that they important in this context. They are the only land evolved in common ancestors. Other authors studied plants with a haploid-dominant life cycle. Genetic sex the relationship between sex ratio and life history determination occurs at meiosis, rather than at attributes, taking into account phylogenetic informa- syngamy, as in higher plants and in many animal tion to control for the non-independence of species groups. Sex determination is based on a chromosomal traits as a result of shared ancestry. They found sex system in many species (Ono, 1970; Ramsay & Berrie, ratio to be associated with life cycle traits in uni- 1982; McDaniel, Willis & Shaw, 2007). Somewhat sexual flowering plants (Field et al., 2013) and more than one-half of all bryophyte taxa worldwide animals (e.g. Fellowes, Compton & Cook, 1999; Benito have separate sexes (dioecious, unisexual) (Wyatt, & González-Solís, 2007; Pomfret & Knell, 2008) after 1982), which is in sharp contrast with the 4–6% of controlling for phylogenetic relatedness. However, to dioecious taxa reported among seed plants (Renner & the best of our knowledge, the effect of phylogenetic Ricklefs, 1995; de Jong & Klinkhamer, 2005). Many history, in terms of systematic position, on sex ratios species do not or only rarely form reproductive has not been addressed in dioecious bryophytes or in organs, and many populations consist of non-sex- other plants to date. We thus largely lack knowledge expressing gametophytes only (Bisang & Hedenäs, about the evolutionary flexibility of plant sex ratio 2005). The majority of investigated unisexual bryo- regulation. One likely explanation for the lack of phyte taxa exhibit a female-biased gender ratio studies is that it requires both large data collecting (Bisang & Hedenäs, 2005; I. Bisang & L. Hedenäs, efforts and well-resolved phylogenies for the study unpubl. data), whereas a male bias is more common taxa. For each species, many specimens or field occur- in seed plants (Delph, 1999; Barrett et al., 2010; rences need to be examined to obtain a reliable sex Field, Pickup & Barrett, 2013). In a few bryophytes, ratio. In bryophytes, sound quantitative sex expres- the female bias was found to be a consequence of sion data are currently available for relatively few gender-specific sex expression rates (Newton, 1971; and only distantly related taxa (Bisang & Hedenäs, Cronberg, 2002; Cronberg et al., 2003) or to reflect 2005). differences in genetic sex ratio (Hedenäs et al., 2010; In this study, we ask whether mechanisms that Stark, McLetchie & Eppley, 2010; Bisang & Hedenäs, control sex expression, sex ratios and sporophyte fre- 2013). Many of the mechanisms suggested to control quency in bryophytes are phylogenetically conserved sex ratios in bryophytes are affected by resource and the traits relatively constant among closely availability and population density. They act at dif- related species, or whether these mechanisms are ferent ontogenetic stages and include gender-specific evolutionarily flexible and the observed variation differences in germination, clonal growth, mortality among species is more directly related to recent envi- or reproduction and physiological traits (e.g. Shaw & ronmental conditions. We use pleurocarpous wetland Gaughan, 1993; McLetchie & Puterbaugh, 2000; mosses as model organisms to test our hypotheses. McLetchie, 2001; Pohjamo & Laaka-Lindberg, 2003; Specifically, we investigate ten species belonging to Stark & McLetchie, 2006). Differences in habitat use Amblystegiaceae and Calliergonaceae, using a total of or microhabitat specialization have also been pro- 2100 specimens. The study species differ in distribu- posed to affect the relative frequency of male and tion and density of populations at the landscape level. female plants (Cameroon & Wyatt, 1990; Bowker
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