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Ancient Aquatic Angiosperms Flow from the Fossil Record Donald H

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Ancient Aquatic Angiosperms Flow from the Fossil Record Donald H COMMENTARY COMMENTARY Water from the rock: Ancient aquatic angiosperms flow from the fossil record Donald H. Les1 the rapid rise of angiosperms has intrigued Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, CT 06269 paleoecologists and evolutionary biologists, who have strived to elucidate underlying ex- planations for their successful radiation. La- The world of 120 million years ago was one dominant global floristic element, a transfor- mented by Charles Darwin as “an abomina- of dynamic biological processes. During that mative event that ultimately altered the char- ble mystery” (1), the abrupt appearance of time the flowering plants emerged as the acter of the entire planet. Understandably, angiosperms and their sudden burst of diver- sification in the fossil record continues to captivate contemporary plant systematists, who have sought a solution by incorporating massive amounts of DNA sequence data in comparative phylogenetic studies of extant species. However, despite extensive techno- logical advances in genetics, genomics, and bioinformatics, which have revolutionized plant research over the past decades, our comprehension of life on earth during such ancient times continues to rely primarily on one data source: the fossil record. In PNAS, Gomez et al. (2) uncover an important clue to Darwin’s mystery by their analyses of Monteschia vidalii,anenigmaticplantfossil from Barremian deposits in Spain. Their re- interpretation of these fossils provides a new perspective that allies Monteschia not only with the angiosperms, but specifically with extant members of the order Ceratophyllales, a group of considerable interest in debates concerning the origin of flowering plants. The characterization of these early plants as highly specialized aquatics also offers novel interpretations regarding the ecological char- acteristics of early angiosperms. Prior ecological interpretations of early Cretaceous environments have been based primarily on terrestrial plant species, which vastly dominate the paleobotanical record. In some fossil floras, aquatic angiosperms do notappearuntilthemiddletolateAlbian stage (3) and these typically depict floating- leaved plants similar in habit to that of the modern order Nymphaeales, which resolves phylogenetically at or near the base of the angiosperm tree of life. Because floating- leaved species are thought to represent an intermediate evolutionary stage between ter- restrial plants and true hydrophytes, one Author contributions: D.H.L. wrote the paper. The author declares no conflict of interest. Fig. 1. Ceratophyllum submersum (shown here) is an extant aquatic species of Ceratophyllales, the order to which See companion article 10.1073/pnas.1509241112. Barremian fossils of M. vidalii have been assigned. 1Email: [email protected]. www.pnas.org/cgi/doi/10.1073/pnas.1514280112 PNAS Early Edition | 1of2 Downloaded by guest on September 28, 2021 might reasonably conclude that entirely sub- many phylogenetic datasets often results in angiosperms whereas Ceratophyllum plus mersed species did not evolve until later. In- the presentation of results without adequate monocots resolve as a clade (13). Analysis deed, fossils similar to the submersed genus analysis of the characters included. How- of low-copy nuclear genes strongly associates Ceratophyllum (Fig. 1), another ancestral an- ever, more critical evaluation of DNA char- Ceratophyllaceae and Chloranthaceae rather giosperm candidate, first appear in the late acters has reduced confidence in the basal than Piperaceae (14). Moreover, a position of Albian (4). However, an earlier presence of placement of Amborella (9) and has dem- Ceratophyllum (rather than Amborella)asthe hydrophytes was documented by the discov- onstrated that the incorporation of highly angiosperm sister group is maintained in ery of the aquatic angiosperm Archaefructus analyses of xanthine dehdrogenase data (15) from Barremian deposits (5). The contempo- Fossils such as those and selected cpDNA data in large-scale tax- Monteschia rary occurrence of from that same reported for Monteschia onomic analyses (16). Given these inconsist- time period not only indicates an early deri- can only help to unravel encies, it seems premature to simply dismiss vation of the aquatic and submersed habits, other potential candidates such as Cerato- but also that some of the very earliest angio- the evolutionary and phyllales (e.g., Ceratophyllum and its fossil sperms were already well adapted to aquatic ecological events that ally Monteschia) as the sister lineage of an- conditions. Furthermore, by their association Ceratophyllum Monteschia accompanied the rise of giosperms. Certainly, it is clear that a satis- with ,the fossils factory answer to the question of earliest rekindle an interesting question regarding flowering plants to diverging angiosperms cannot be attained theultimateageoftheCeratophyllales. global prominence. until the phylogenetic placements of both Interestingly, the phylogenetic analysis of Amborella and Ceratophyllum have been extant plant DNA sequences initially resolved saturated sites can alter the position of established much more confidently. Ceratophyllum as the sister group of all other Amborella and Ceratophyllum in phyloge- It is important to emphasize that all pro- angiosperms (6), a result hypothesized earlier neticanalyses(10,11).Thefollowingin- by analysis of nonmolecular data (7). How- consistencies are particularly noteworthy. posed schemes of angiosperm relationships ever, the recognition of Ceratophyllum as the Analyses of protein-coding gene sequences represent hypotheses, not facts (17). Al- earliest diverging angiosperm lineage met from chloroplast DNA (cpDNA) data place though they cannot be falsified, these hy- with much skepticism, due in large part to Amborella as the sister to other angio- potheses must be tested further, and not its aquatic habit, which was believed to rep- sperms while placing Ceratophyllum either simply by the exclusive incorporation of resent a highly derived condition evolution- with Piperales or distant from Piperales, molecular data. Furthermore, compara- arily. Subsequent molecular phylogenetic depending on whether different codon po- tive morphological analyses provide the studies also yielded inconsistent placements sitions or amino acid sequences are ana- only practical means of exploring phylo- of Ceratophyllum, which consistently was lyzed (12). Nuclear ribosomal DNA data genetic relationships among long-extinct characterized by a long branch in the anal- also are problematic. Analyses of 18s rDNA plants (18), where no DNA is available yses. As more DNA data were analyzed, it sequences resolve a basal angiosperm grade for molecular analysis. For this reason, the was the terrestrial genus Amborella,notCera- comprising the monocots and Ceratophyllum, continued quest for fossils such as those tophyllum, that most studies resolved as the whereas 26s rDNA place Amborella in that reported for Monteschia can only help to sister group of angiosperms. Consequently, position; combined 18s + 26s sequences yield unravel the evolutionary and ecological despite the lack of a fossil record, the ances- yet another result where Amborella and events that accompanied the rise of flower- tral position of Amborella has become ac- Nymphaeales comprise a sister clade to other ing plants to global prominence. cepted by many as fact and has been used even in the interpretation of genome-scale evolutionary factors (8). However, the un- 1 Darwin F, Seward AC (1903) More letters of Charles Darwin (John phylogenetic placements of Amborella and Ceratophyllum. J Mol usual features shared by Monteschia and Murray, London), Vol 2. Evol 68(3):197–204. Ceratophyllum (e.g., rootlessness, unitegmic 2 Gomez B, Daviero-Gomez V, Coiffard C, Martín-Closas C, 11 Xi Z, Liu L, Rest JS, Davis CC (2014) Coalescent versus Dilcher DL (2015) Montsechia, an ancient aquatic concatenation methods and the placement of Amborella as sister to angiosperm. Proc Natl Acad Sci USA 112, 10.1073/ ovules, and carpellate pore associated with water lilies. Syst Biol 63(6):919–932. pnas.1509241112. water pollination) indicates that the Cerato- 12 Ruhfel BR, Gitzendanner MA, Soltis PS, Soltis DE, Burleigh JG 3 Wing SL, Boucher LD (1998) Ecological aspects of the (2014) From algae to angiosperms-inferring the phylogeny of phyllales must have diverged from other Cretaceous flowering plant radiation. Annu Rev Earth Planet Sci green plants (Viridiplantae) from 360 plastid genomes. BMC Evol flowering plants considerably earlier than 26:379–421. 4 Dilcher DL, Wang H (2009) An Early Cretaceous fruit with affinities Biol 14:23. the Barremian, which suggests that the ques- to Ceratophyllaceae. Am J Bot 96(12):2256–2269. 13 Maia VH, Gitzendanner MA, Soltis PS, Wong GK-S, Soltis DE tion of the most ancestral angiosperm lineage 5 Sun G, et al. (2002) Archaefructaceae, a new basal angiosperm (2014) Angiosperm phylogeny based on 18S/26S rDNA sequence deserves renewed scrutiny. family. Science 296(5569):899–904. data: Constructing a large data set using next-generation sequence 6 Chase MW, et al. (1993) Phylogenetics of seed plants: an analysis data. Int J Plant Sci 175(6):613–650. Two factors complicate the molecular of nucleotide sequences from the plastid gene rbcL. Ann Mo Bot 14 Zeng L, et al. (2014) Resolution of deep angiosperm phylogeny – phylogenetic analysis of ancestral angio- Gard 80(3):528 580. using conserved nuclear genes and estimates of early divergence
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