Evolution of sexual systems and growth habit in Mussaenda (Rubiaceae): Insights into the evolutionary pathways of dioecy

Duan, Tingting; Deng, Xiaojie; Shi, Chen; Luo, Zhi-Ming; Zhao, Zhongtao; Tu, Tieyao; Khang, Nguyen Sinh; Razafimandimbison, Sylvain G.; Zhang, Dianxiang

doi:10.1016/j.ympev.2018.02.015

Cited by 18 publications

(13 citation statements)

References 87 publications

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“…Li et al ., ; Watanabe et al ., ). The shifts have occurred on multiple occasions (Duan et al ., ) and always appear to involve the L‐morph becoming female and the S‐morph becoming male, consistent with asymmetrical pollen transfer as a prelude to the spread of sterility mutations (Fig. a(vii)).…”

Section: Evolutionary Breakdownsupporting

confidence: 67%

‘A most complex marriage arrangement’: recent advances on heterostyly and unresolved questions

2019

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Summary Heterostylous genetic polymorphisms provide paradigmatic systems for investigating adaptation and natural selection. Populations are usually comprised of two (distyly) or three (tristyly) mating types, maintained by negative frequency‐dependent selection resulting from disassortative mating. Theory predicts this mating system should result in equal style‐morph ratios (isoplethy) at equilibrium. Here, I review recent advances on heterostyly, focusing on examples challenging stereotypical depictions of the polymorphism and unresolved questions. Comparative analyses indicate multiple origins of heterostyly, often within lineages. Ecological studies demonstrate that structural components of heterostyly are adaptations improving the proficiency of animal‐mediated cross‐pollination and reducing pollen wastage. Both neutral and selective processes cause deviations from isoplethy in heterostylous populations, and, under some ecological and demographic conditions, cause breakdown of the polymorphism, resulting in either the evolution of autogamy and mixed mating, or transitions to alternative outcrossing systems, including dioecy. Earlier ideas on the genetic architecture of the S‐locus supergene governing distyly have recently been overturned by discovery that the dominant S‐haplotype is a hemizygous region absent from the s‐haplotype. Ecological, phylogenetic and molecular genetic data have validated some features of theoretical models on the selection of the polymorphism. Although heterostyly is the best‐understood floral polymorphism in angiosperms, many unanswered questions remain.

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Section: Evolutionary Breakdownsupporting

confidence: 67%

‘A most complex marriage arrangement’: recent advances on heterostyly and unresolved questions

2019

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“…Using a corrected version of the sister clade analysis on an updated dataset, dioecious species were found to have higher species richness than non-dioecious sister clades in angiosperms, contrary to previous observation (9). Using a phylogenetic method to study trait evolution and species diversification (BiSSe, 10) on several genera with dioecious species, dioecy was not found to be associated with an increased extinction rate (11,12). Another hypothesis has been put forward to explain the rareness of dioecy in angiosperms, which posits that reversion from dioecy to other breeding systems is frequent and that dioecy is more labile than previously thought (7).…”

Section: Introductionmentioning

confidence: 85%

Dioecy in plants: an evolutionary dead end? Insights from a population genomics study in the Silene genus

Muyle

Martin

Zemp

et al. 2018

Preprint

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About 15,000 angiosperm species (~6%) have separate sexes, a phenomenon known as dioecy.Early work reported a lower species richness in dioecious compared to non-dioecious sister clades, which was taken to suggest that dioecy might be an evolutionary dead end. More recently, phylogenetic analyses using different methodologies have challenged this conclusion. Here, we used a population genomics approach to look for evidence of evolutionary handicaps of dioecy in the Silene genus at the molecular level. We obtained RNA-seq data of individuals from several populations in 13 closely related species with different breeding systems: seven dioecious, three hermaphroditic and three gynodioecious species. We show that dioecy is associated with increased genetic diversity and a higher selection efficacy both against deleterious and for beneficial mutations while controlling for differences in population size. We conclude that, in the Silene genus, dioecious species bear no sign of mutational burden or upcoming extinction. On the contrary, dioecious species harbor a higher potential for adaptation than their non-dioecious relatives. Our results do not support the evolutionary dead end hypothesis and re-open the question why dioecy is rare in angiosperms. Significance statement:Dioecy (=separate sexes) is much rarer in flowering plants compared to animals and other organisms. The "dead-end hypothesis" states that dioecious plant populations might experience evolutionary handicaps such as low seed dispersal (as only 50% of the individuals, the females, contribute), which might cause high genetic drift, low adaptation and ultimately extinction. Here we tested this hypothesis by focusing on the genus Silene and by comparing the population genetics of 13 dioecious and non-dioecious species. We found that dioecious Silene species exhibit lower genetic drift and more adaptation compared to their non-dioecious relatives. Our results thus reject the dead-end hypothesis and re-open the question of why dioecy is rare in flowering plants. Evolution of separate sexes in plantsdesigned for such data was applied to perform 21,22). The SNPs were then analyzed to estimate genetic diversity and the efficacy of selection in each species.

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“…The availability of a robust phylogeny is a prerequisite to accurately study trait evolution at different taxonomic levels (family, subfamily, tribe or genus). This is the case, for instance, when mapping morphological and functional traits in Gardenieae [9], when investigating the evolution of sexual systems and growth habit in Mussaenda [18], or when studying the evolution of caffeine content in Coffea [19]. Since two decades, advances in next-generation sequencing (NGS) technologies have revolutionized the field of biology by providing, at reduced cost, huge amounts of data for an increased number of plant species.…”

Section: Introductionmentioning

confidence: 99%

Chloroplast genomes of Rubiaceae: Comparative genomics and molecular phylogeny in subfamily Ixoroideae

Garavito

Block

et al. 2020

PLoS ONE

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Evolution of sexual systems and growth habit in Mussaenda (Rubiaceae): Insights into the evolutionary pathways of dioecy

Cited by 18 publications

References 87 publications

‘A most complex marriage arrangement’: recent advances on heterostyly and unresolved questions

‘A most complex marriage arrangement’: recent advances on heterostyly and unresolved questions

Dioecy in plants: an evolutionary dead end? Insights from a population genomics study in the Silene genus

Chloroplast genomes of Rubiaceae: Comparative genomics and molecular phylogeny in subfamily Ixoroideae

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