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Evolution of floral characters and biogeography of Heloniadeae (Melanthiaceae): an example of breeding system shifts with inflorescence change.

ABSTRACT: Heloniadeae (Melanthiaceae) presents an East Asia-North America disjunct distribution. Different molecular and morphological data nevertheless support the tribe as a monophyletic group. However, their phylogenetic relationships and biogeographic history, together with the character evolution, are not clear. Therefore, we constructed a Bayesian phylogenetic tree for Heloniadeae using cpDNA and inferred the historical biogeography and floral character evolution. The results revealed that Heloniadeae was distributed in high-latitudes of East Asia and North America, originating since 22.2 mya. The East Asia clade migrated into southwest China, and subsequently colonized the Korean Peninsula, Taiwan, the Ryukyus, and spread northward to Japan and southern Sakhalin. The evolution of the inflorescence and number of flowers were phylogenetically conserved, associated with the historical biogeography of Heloniadeae. The inflorescences transferred from raceme to sub-umbel, and the number of flowers decreased during the dispersal process, which may be accompanied by changes in the breeding system. Besides, the anthesis period was more affected by the habitat environment than phylogenetic constraints. The flowering temperature of was below 20 °C in most species, except H. kawanoi. Such a low temperature might not be conductive to pollinator activities, but it could be compensated by sustaining seed production with long-lasting flowers.

SUBMITTER: Chao CT

PROVIDER: S-EPMC8563777 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Intercontinental floristic disjunction between East Asia and North America in the Northern Hemisphere has received much attention during the past decades, but few studies have focused on the family level. Melanthiaceae, containing 196 species and 17 genera circumscribed in five tribes, is disjunctly distributed in Eurasia and North America. It is one of the foremost models for studying the evolution of biogeographic patterns in this region. Here, we present a fossil-calibrated, molecular phylogeny of Melanthiaceae based on two chloroplast DNA datasets: one dataset includes extensive sampling (94 species representing all 17 genera of Melanthiaceae) of four chloroplast DNA regions (atpB, rbcL, matK, and ndhF) and the other includes six species representing all tribes of the family for 78 coding genes of the chloroplast genome. Within this framework, we infer the historical biogeography of Melanthiaceae. Both datasets produce well-resolved phylogenies of Melanthiaceae showing the monophyly of the family and the relationships among the five tribes. Melanthieae is found to be sister to the rest of the tribes of the family and the remaining taxa are divided into two major clades consisting of the Chionographideae + Heloniadeae clade and the Parideae + Xerophylleae clade. The molecular dating and the ancestral area analyses suggest that Melanthiaceae most likely originated in North America with its crown group dated at 92.1 mya in the late Cretaceous. The favored ancestral areas at the crown lineages of tribes are also in North America. In the family, seven independent migrations into East Asia from North America are inferred to have occurred in the Oligocene and the Miocene-Pliocene via historical paleo-land bridge connections. Cooling trends during the Oligocene resulted in the present East Asia-North America disjunct distribution, while the warm period during the middle Miocene and habitat heterogeneity stimulated diversification in East Asia. Our study provides the phylogenetic and biogeographical history of the Melanthiaceae and adds an example of "out of North America" migration in the biogeographic history of the Northern Hemisphere.

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Evolution of floral characters and biogeography of Heloniadeae (Melanthiaceae): an example of breeding system shifts with inflorescence change.

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