skip to main content


Title: Large-Scale Phylogenomic Analyses Reveal the Monophyly of Bryophytes and Neoproterozoic Origin of Land Plants
Abstract The relationships among the four major embryophyte lineages (mosses, liverworts, hornworts, vascular plants) and the timing of the origin of land plants are enigmatic problems in plant evolution. Here, we resolve the monophyly of bryophytes by improving taxon sampling of hornworts and eliminating the effect of synonymous substitutions. We then estimate the divergence time of crown embryophytes based on three fossil calibration strategies, and reveal that maximum calibration constraints have a major effect on estimating the time of origin of land plants. Moreover, comparison of priors and posteriors provides a guide for evaluating the optimal calibration strategy. By considering the reliability of fossil calibrations and the influences of molecular data, we estimate that land plants originated in the Precambrian (980–682 Ma), much older than widely recognized. Our study highlights the important contribution of molecular data when faced with contentious fossil evidence, and that fossil calibrations used in estimating the timescale of plant evolution require critical scrutiny.  more » « less
Award ID(s):
1932765
NSF-PAR ID:
10314558
Author(s) / Creator(s):
; ; ; ; ; ;
Editor(s):
Battistuzzi, Fabia Ursula
Date Published:
Journal Name:
Molecular Biology and Evolution
Volume:
38
Issue:
8
ISSN:
1537-1719
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Nyssa(Nyssaceae, Cornales) represents a classical example of the well‐known eastern Asian–eastern North American floristic disjunction. The genus consists of three species in eastern Asia, four species in eastern North America, and one species in Central America. Species of the genus are ecologically important trees in eastern North American and eastern Asian forests. The distribution of living species and a rich fossil record of the genus make it an excellent model for understanding the origin and evolution of the eastern Asian–eastern North American floristic disjunction. However, despite the small number of species, relationships within the genus have remained unclear and have not been elucidated using a molecular approach. Here, we integrate data from 48 nuclear genes, fossils, morphology, and ecological niche to resolve species relationships, elucidate its biogeographical history, and investigate the evolution of morphology and ecological niches, aiming at a better understanding of the well‐known EA–ENA floristic disjunction. Results showed that the Central American (CAM)Nyssa talamancanawas sister to the remaining species, which were divided among three, rapidly diversified subclades. Estimated divergence times and biogeographical history suggested thatNyssahad an ancestral range in Eurasia and western North America in the late Paleocene. The rapid diversification occurred in the early Eocene, followed by multiple dispersals between and within the Erasian and North American continents. The genus experienced two major episodes of extinction in the early Oligocene and end of Neogene, respectively. The Central AmericanN. talamancanarepresents a relic lineage of the boreotropical flora in the Paleocene/Eocene boundary that once diversified in western North America. The results supported the importance of both the North Atlantic land bridge and the Bering land bridge (BLB) for the Paleogene dispersals ofNyssaand the Neogene dispersals, respectively, as well as the role of Central America as refugia of the Paleogene flora. The total‐evidence‐based dated phylogeny suggested that the pattern of macroevolution ofNyssacoincided with paleoclimatic changes. We found a number of evolutionary changes in morphology (including wood anatomy and leaf traits) and ecological niches (precipitation and temperature) between the EA–ENA disjunct, supporting the ecological selection driving trait evolutions after geographic isolation. We also demonstrated challenges in phylogenomic studies of lineages with rapid diversification histories. The concatenation of gene data can lead to inference of strongly supported relationships incongruent with the species tree. However, conflicts in gene genealogies did not seem to impose a strong effect on divergence time dating in our case. Furthermore, we demonstrated that rapid diversification events may not be recovered in the divergence time dating analysis using BEAST if critical fossil constraints of the relevant nodes are not available. Our study provides an example of complex bidirectional exchanges of plants between Eurasia and North America in the Paleogene, but “out of Asia” migrations in the Neogene, to explain the present disjunct distribution ofNyssain EA and ENA.

     
    more » « less
  2. Abstract Premise

    Dioecy (separate sexes) has independently evolved numerous times across the angiosperm phylogeny and is recently derived in many lineages. However, our understanding is limited regarding the evolutionary mechanisms that drive the origins of dioecy in plants. The recent and repeated evolution of dioecy across angiosperms offers an opportunity to make strong inferences about the ecological, developmental, and molecular factors influencing the evolution of dioecy, and thus sex chromosomes. The genusAsparagus(Asparagaceae) is an emerging model taxon for studying dioecy and sex chromosome evolution, yet estimates for the age and origin of dioecy in the genus are lacking.

    Methods

    We use plastome sequences and fossil time calibrations in phylogenetic analyses to investigate the age and origin of dioecy in the genusAsparagus. We also review the diversity of sexual systems present across the genus to address contradicting reports in the literature.

    Results

    We estimate that dioecy evolved once or twice approximately 2.78−3.78 million years ago inAsparagus, of which roughly 27% of the species are dioecious and the remaining are hermaphroditic with monoclinous flowers.

    Conclusions

    Our findings support previous work implicating a young age and the possibility of two origins of dioecy inAsparagus, which appear to be associated with rapid radiations and range expansion out of Africa. Lastly, we speculate that paleoclimatic oscillations throughout northern Africa may have helped set the stage for the origin(s) of dioecy inAsparagusapproximately 2.78−3.78 million years ago.

     
    more » « less
  3. Abstract Aim

    We sought to illuminate the history of the arachnid orders Schizomida and Uropygi, neither of which have previously been subjected to global molecular phylogenetic and biogeographical analyses.

    Location

    Specimens used in this study were collected in all major tropical and subtropical areas where they are presently found, including the Americas, Africa, Australia and the Indo‐Pacific region.

    Methods

    From field‐collected specimens, we sequenced two nuclear and two mitochondrial markers, combined these with publicly available data, and conducted multi‐gene phylogenetic analyses on 240 Schizomida, 24 Uropygi and 12 other arachnid outgroups. Schizomid specimens included one specimen from the small family Protoschizomidae; other schizomid specimens were in Hubbardiidae, subfamily Hubbardiinae, which holds 289 of the order's 305 named species. We inferred ancestral areas using the Dispersal‐Extinction‐Cladogenesis model of range evolution, and we used fossil calibrations to estimate divergence times.

    Results

    We recovered monophyletic Schizomida and Uropygi as each other's sister group, forming the clade Thelyphonida, and terminals from the New World were usually positioned as the earliest diverging lineages. The ancestral area for schizomids reconstructed unambiguously to the region comprised of Mexico, Southern California and Florida (the xeric New World subtropics). Optimal trees suggested a single colonization of the Indo‐Pacific in both orders, although this did not receive bootstrap support. Molecular dating gave an Upper Carboniferous origin for each order, and a mid‐Cretaceous expansion of Schizomida, including the origin and initial diversification of those in the Indo‐Pacific.

    Main conclusions

    Ancestral area reconstructions, molecular dating and fossil evidence all support an Upper Carboniferous, tropical Pangean origin for Thelyphonida, Schizomida and perhaps Uropygi. Much of this region became unsuitable habitat for these arachnids during the breakup of Pangea, but they persisted in the area that is now Meso‐ and South America. From there they then expanded to the Indo‐Pacific, where schizomids today display an idiosyncratic combination of microendemism and long‐range dispersal.

     
    more » « less
  4. Premise

    Phylogenetic trees of bryophytes provide important evolutionary context for land plants. However, published inferences of overall embryophyte relationships vary considerably. We performed phylogenomic analyses of bryophytes and relatives using both mitochondrial and plastid gene sets, and investigated bryophyte plastome evolution.

    Methods

    We employed diverse likelihood‐based analyses to infer large‐scale bryophyte phylogeny for mitochondrial and plastid data sets. We tested for changes in purifying selection in plastid genes of a mycoheterotrophic liverwort (Aneura mirabilis) and a putatively mycoheterotrophic moss (Buxbaumia), and compared 15 bryophyte plastomes for major structural rearrangements.

    Results

    Overall land‐plant relationships conflict across analyses, generally weakly. However, an underlying (unrooted) four‐taxon tree is consistent across most analyses and published studies. Despite gene coverage patchiness, relationships within mosses, liverworts, and hornworts are largely congruent with previous studies, with plastid results generally better supported. Exclusion ofRNAedit sites restores cases of unexpected non‐monophyly to monophyly forTakakiaand two hornwort genera. Relaxed purifying selection affects multiple plastid genes in mycoheterotrophicAneurabut notBuxbaumia. Plastid genome structure is nearly invariant across bryophytes, but thetufA locus, presumed lost in embryophytes, is unexpectedly retained in several mosses.

    Conclusions

    A common unrooted tree underlies embryophyte phylogeny, [(liverworts, mosses), (hornworts, vascular plants)]; rooting inconsistency across studies likely reflects substantial distance to algal outgroups. Analyses combining genomic and transcriptomic data may be misled locally for heavilyRNA‐edited taxa. TheBuxbaumiaplastome lacks hallmarks of relaxed selection found in mycoheterotrophicAneura. Autotrophic bryophyte plastomes, includingBuxbaumia, hardly vary in overall structure.

     
    more » « less
  5. Summary

    Extant land plants consist of two deeply divergent groups, tracheophytes and bryophytes, which shared a common ancestor some 500 million years ago. While information about vascular plants and the two of the three lineages of bryophytes, the mosses and liverworts, is steadily accumulating, the biology of hornworts remains poorly explored. Yet, as the sister group to liverworts and mosses, hornworts are critical in understanding the evolution of key land plant traits. Until recently, there was no hornwort model species amenable to systematic experimental investigation, which hampered detailed insight into the molecular biology and genetics of this unique group of land plants. The emerging hornwort model species,Anthoceros agrestis, is instrumental in our efforts to better understand not only hornwort biology but also fundamental questions of land plant evolution. To this end, here we provide an overview of hornwort biology and current research on the model plantA. agrestisto highlight its potential in answering key questions of land plant biology and evolution.

     
    more » « less