Recurrent Evolution of Dioecy in Bryophytes

McDaniel, Stuart F.; Atwood, John J.; Burleigh, J. Gordon

doi:10.1111/j.1558-5646.2012.01808.x

Cited by 70 publications

(56 citation statements)

References 56 publications

(71 reference statements)

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“…New Phytologist (McDaniel et al, 2013) and angiosperms (Weller & Sakai, 1999;Renner, 2015) and we detected such lability only across the shallowest nodes of the liverwort phylogeny where the phylogenetic signal in sexual systems tended to decrease. The pattern of increasing lability of the sexual condition towards the tips of the tree is paralleled by the complete absence of phylogenetic signal in sexual systems within certain genera such as Radula (Devos et al, 2011) and Diplasiolejeunea (Dong et al, 2012).…”

Section: Researchmentioning

confidence: 64%

Increased diversification rates follow shifts to bisexuality in liverworts

et al. 2016

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SummaryShifts in sexual systems are one of the key drivers of species diversification. In contrast to angiosperms, unisexuality prevails in bryophytes. Here, we test the hypotheses that bisexuality evolved from an ancestral unisexual condition and is a key innovation in liverworts.We investigate whether shifts in sexual systems influence diversification using hidden state speciation and extinction analysis (HiSSE). This new method compares the effects of the variable of interest to the best-fitting latent variable, yielding robust and conservative tests.We find that the transitions in sexual systems are significantly biased toward unisexuality, even though bisexuality is coupled with increased diversification. Sexual systems are strongly conserved deep within the liverwort tree but become much more labile toward the present.Bisexuality appears to be a key innovation in liverworts. Its effects on diversification are presumably mediated by the interplay of high fertilization rates, massive spore production and long-distance dispersal, which may separately or together have facilitated liverwort speciation, suppressed their extinction, or both. Importantly, shifts in liverwort sexual systems have the opposite effect when compared to angiosperms, leading to contrasting diversification patterns between the two groups. The high prevalence of unisexuality among liverworts suggests, however, a strong selection for sexual dimorphism.

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Section: Researchmentioning

confidence: 64%

Increased diversification rates follow shifts to bisexuality in liverworts

et al. 2016

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“…Lastly and importantly, our study of sexual system switches in hornworts, together with the data on such switches available for liverworts [18,19] and mosses [43,44], makes clear that suggestions of dioicy being ancestral in “bryophytes” (at the time assumed to be a monophylum) and of monoicy being the derived sexual system [2] need to be put to rest. Instead, sexual systems in the three lineages of haploid-dominant land plants are highly labile, and there is no single preferential direction.…”

Section: Resultsmentioning

confidence: 99%

Correlates of monoicy and dioicy in hornworts, the apparent sister group to vascular plants

Villarreal

Renner

2013

BMC Evol Biol

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BackgroundWhether male and female gametes are produced by single or separate individuals shapes plant mating and hence patterns of genetic diversity among and within populations. Haploid-dominant plants (“bryophytes”: liverworts, mosses and hornworts) can have unisexual (dioicous) or bisexual (monoicous) gametophytes, and today, 68% of liverwort species, 57% of moss species, and 40% of hornwort species are dioicous. The transitions between the two sexual systems and possible correlations with other traits have been studied in liverworts and mosses, but not hornworts. Here we use a phylogeny for 98 of the 200 species of hornworts, the sister group to vascular plants, representing roughly equal proportions of all monoicous and all dioicous species, to test whether transitions in sexual systems are predominantly from monoicy to dioicy as might be expected based on studies of mosses. We further investigate possible correlations between sexual system and spore size, antheridium number, ploidy level, and diversification rate, with character selection partly based on findings in mosses and liverworts.ResultsHornworts underwent numerous transitions between monoicy and dioicy. The transition rate from dioicy to monoicy was 2× higher than in the opposite direction, but monoicous groups have higher extinction rates; diversification rates do not correlate with sexual system. A correlation important in mosses, that between monoicy and polyploidy, apparently plays a small role: of 20 species with chromosome counts, only one is polyploid, the monoicous Anthoceros punctatus. A contingency test revealed that transitions to dioicy were more likely in species with small spores, supporting the hypothesis that small but numerous spores may be advantageous for dioicous species that depend on dense carpets of gametophytes for reproductive assurance. However, we found no evidence for increased antheridium-per-chamber numbers in dioicous species.ConclusionsSexual systems in hornworts are labile, and the higher number of extant monoicous species (60%) may be largely due to frequent transitions to monoicy.

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“…Mating systems and dispersal traits were, however, shown to shift states very quickly along moss and liverwort phylogenies McDaniel, Atwood & Burleigh 2013). This suggests that the phylogenetic component of trait evolution is low, decreasing the chance of type I errors (Hardenberg & Gonzalez-Voyer 2013).…”

Section: A T a A N A L Y S I Smentioning

confidence: 99%

“…Bryophytes further display a wide range of mating systems with an unparalleled evolutionary lability, with at least 133 transitions between sexual systems in mosses (McDaniel, Atwood & Burleigh 2013). The application of Baker's law in the group is, however, challenged by the fact that selection for selfing is reduced when multiple founder events occur (Busch 2011), a condition that has been reported in several instances (Hutsem ekers et al 2011;Laenen et al 2011; but see Karlin et al 2011).…”

Section: Introductionmentioning

confidence: 99%

Baker's law and the island syndromes in bryophytes

et al. 2013

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Summary1. The evolution of island syndromes has long served as a model to understand the mechanisms accounting for phenotypic differentiation. Combining literature data with actual observations, we determine whether typical syndromes such as the loss of dispersal power and the bias towards selfcompatibility (Baker's law) apply to vagile organisms, using bryophytes as a model. 2. The life-history traits (LHTs) observed in oceanic island floras were statistically different from those observed on continents, evidencing the evolution of island syndromes. In contrast, LHTs of continental and continental island floras were similar, pointing to differences in migration intensity between continents, continental islands and oceanic islands. 3. The proportion of bisexual species was significantly higher on oceanic islands than on continents. A significant proportion of species that are unisexual or bisexual on continents shifted towards exclusive bisexuality on oceanic islands, suggesting that Baker's law applies to bryophytes. The underlying mechanisms, however, probably differ from in situ selection for selfing. 4. The proportion of species producing specialized asexual diaspores, which are assumed to play a role in short-distance dispersal (SDD), was higher on oceanic islands than on continents. The proportion of species producing spores, which are involved in long-distance dispersal (LDD), exhibited the reverse trend, suggesting a shift in the prevalent reproductive strategy to favour SDD on oceanic islands. Approximately 50% of the species, however, maintained the ability to produce sporophytes on oceanic islands, and the relative frequency of fertile shoots within collections of four model species was even higher on islands than on continents. 5. Synthesis. Bryophytes exhibit typical island syndromes, indicating that migration rates between oceanic islands and continents are not sufficient to prevent the effects of genetic drift and contradicting the view that the sea does not impede migration in the group. Significant shifts in life-history traits (LHTs) towards increased production of specialized asexual diaspores and decreased sporophyte production on oceanic islands indeed point to a global loss of long-distance dispersal (LDD) ability. The maintenance of traits characteristic for LDD in a large number of species has, however, substantial consequences for our understanding of island plant evolution, and in particular, for our vision of islands as evolutionary dead ends.

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Recurrent Evolution of Dioecy in Bryophytes

Cited by 70 publications

References 56 publications

Increased diversification rates follow shifts to bisexuality in liverworts

Increased diversification rates follow shifts to bisexuality in liverworts

Correlates of monoicy and dioicy in hornworts, the apparent sister group to vascular plants

Baker's law and the island syndromes in bryophytes

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