Annual Research & Review in Biology 9(6): 1-8, 2016, Article no.ARRB.24354 ISSN: 2347-565X, NLM ID: 101632869

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Evolutionary Trends in

Alice Benzecry 1* and Sheila Brack-Hanes 2

1Fairleigh Dickinson University, School of Natural Sciences, H-DH4-03, 1000 River Road, Teaneck, New Jersey 07666, USA. 2Eckerd College, Collegium of Natural Sciences, 4200 54th Ave. South, St. Petersburg, Florida 33711, USA.

Authors’ contributions

This work was carried out in collaboration between both authors. Authors AB and SBH designed the study, wrote the protocol and interpreted the data. Author AB anchored the field study, gathered the initial data and performed preliminary data analysis. Authors AB and SBH managed the literature searches and produced the initial draft. Both authors read and approved the final manuscript.

Article Information

DOI: 10.9734/ARRB/2016/24354 Editor(s): (1) George Perry, Dean and Professor of Biology, University of Texas at San Antonio, USA. Reviewers: (1) Flavio de Almeida Alves Junior, Universidade Federal de Pernambuco, Brazil. (2) Manuel Mendoza Carranza, El Colegio de la Frontera Sur (ECOSUR), Mexico. (3) Romulo Diego de Lima Behrend, Unicesumar, Brazil. Complete Peer review History: http://sciencedomain.org/review-history/13642

Received 16 th January 2016 nd Mini-review Article Accepted 2 March 2016 Published 11 th March 2016

ABSTRACT

This paper provides evidences of the evolutionary pathway followed by one of the main groups of marine angiosperms, the Hydrocharitaceae . Current molecular data has confirmed the aquatic origin of these . The Hydrocharitaceae group has a cosmopolitan distribution and is well represented in the fossil record in Europe and North America. Morphological and phylogenetic data has shown dramatic differences between the Hydrocharitaceae and the other marine angiosperms. Furthermore, it supports the hypothesis that aquatic monocot ancestors were able to adapt to a continuously changing environment caused by widespread continental flooding in the Period when seagrasses first occur, to a gradual regression of inland seas during the leading to subsequent adaptation to a completely submerged marine environment within the subfamily Hydriloideae .

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*Corresponding author: E-mail: [email protected];

Benzecry and Brack-Hanes; ARRB, 9(6): 1-8, 2016; Article no.ARRB.24354

Keywords: Hydrocharitaceae; seagrasses; marine monocots; evolutionary trends.

1. INTRODUCTION examining monocot characteristics at the generic level came to a conclusion quite opposite that of Marine angiosperms (seagrasses) are Arber [12] and Cronquist [13]. Den Hartog [14] taxonomically confined to 60 in 13 concluded that land plants, such as those that genera, assigned to five different monocot are found in mangrove communities, became salt families within the single order , tolerant in the first place and then established aquatic subclass Alismatidae (alismatids). themselves in the marine environment. Seagrasses are known to inhabit the sea Furthermore, he speculated that the marine worldwide with the exception of Antarctica, plants then evolved into brackish ones, and representing the utmost adaptive radiation of finally, into freshwater aquatics. freshwater plants on Earth [1]. Physical drivers, such as climate change, currents and Using genetic analysis Les et al. [15], Wissler et tectonic events, have been influential in their al. [16], Chen et al. [17] and Ross et al. [18] distribution. To date there are no studies concluded that seagrasses adaptation to examining patterns of biodiversity change of complete submersion into the sea could have seagrasses over global or regional scales. followed three separate adaptation linages. This According to Barret et al. [2] and Les [3] aquatic paper will concentrate on adaptations followed by vascular plants in general have been reported as the Hydrocharitaceae representatives . having a conservative macro-evolutionary pattern due to their low genetic variability and population 2. METHODOLOGY differentiation below the species level. This study is largely based on a review of the Aquatic monocots have been indubitably present available literature on the aquatic since the early Cretaceous as confirmed by the with emphasis on the oldest fossils assigned to this clade, 110-120 Hydrocharitaceae Family including the four million years old [4,5]. Monocot fossil records seagrasses: Enhalus, , Halophila and also confirm the early divergence of seagrasses the fossil Thalassites and three freshwater during this time [5]. Using molecular clocks, the submerged genera: Najas, Nechamandra and monocots have been dated between 124--141 Vallisneria; and observations made on our own MYA [6-11]. The origin and evolution of (in part unpublished) material and results. The monocots and of those especially known to hydrocharitacean Floridian fossil inhabit the seas is an intriguing subject that has Thalassites parkavonensis was examined for evoked several hypotheses; Arber [12], clues that would lead to the evolutionary trends Cronquist [13], Den Hartog [14], Les et al. [15], in the Hydrocharitaceae seagrasses following the Wissler et al. [16] and Chen et al. [17]. The report of Benzecry [19] which compared the evolutionary pathway of seagrasses is still presence of paracytic stomata in members of the conjectural. Thalassia testudinum (Hydrocharitaceae seagrass) and Vallisneria sp., a close freshwater Arber [12] outlined very specialized features that submerged relative. were necessary for plants to have in order to exist and reproduce in marine environments. Her References will be made to representatives of ideas were established from characteristics the other seagrass families, Potamogetonaceae/ at the species level. She also suggested that Zosteraceae, Cymodoceaceae, Posidoniaceae marine angiosperms were indirectly derived from and Rupiaceae in order to better understand the land plants that became long adapted to aquatic evolutionary trends of the order Alismatales . conditions and subsequently adapted further into salt tolerant or even brackish species, leading to 2.1 Molecular Phylogeny completely submerged marine species. Cronquist [13] believed that the origin of Marine angiosperms polyphyletic origins were monocots was aquatic and that terrestrial confirm by molecular phylogenetic analyses at monocots are derived from aquatic pre- the family level [20,21]. Genetic studies of the monocots. He also suggested that terrestrial rbcL gene [1,15,17,22,23] and complete plastid monocots then conversely, gave rise, repeatedly, genomes [18] have determined that marine to aquatic groups. Among the new aquatic angiosperms evolved in three monophyletic groups, some progressively adapted to a marine clades: The Hydrocharitaceae , the habitat. Den Hartog [14] on the other hand, by Potamogetonaceae/ Zosteraceae, and the

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Cymodoceaceae complex (Cymodoceaceae, relation to the presence of stomata, their Posidoniaceae and Rupiaceae). Based on these pollination mechanisms and pollen morphology results, Les et al. [15], Chen et al. [17] and Ross as described by Chen, et al. [17], Waycott, et al. et al. [18] proposed that marine angiosperm [27], and Tanaka et al. [28]. Hydrocharitaceae is ancestors were either freshwater plants or a fully aquatic monocot family; witch migrated perhaps a mixture of freshwater and salt-tolerant from fresh water to the sea. It consists of 17 species. genera with approximately 127 species including freshwater, brackish water and marine Comparisons of orthologous gene sequences of representatives with paracytic stomata, a two seagrasses ( Posidonia oceanica (L.) Delile character considered to be of great importance and Zostera marina L.) within the order for its identification of its freshwater Alismatales and eight terrestrial angiosperms representatives [13,29,30]. It is worthwhile to species by Wissler et al. [16] revealed that note that even though the other families seagrass genes have diverged from their containing marine representatives, terrestrial counterparts via an initial aquatic stage Posidoniaceae, Cymodoceaceae, Ruppiaceae characteristic of the order Alismatales and to the and Zosteraceae also contain freshwater and derived fully-marine stage characteristic of brackish water representatives; they are usually seagrasses. Sequence analyses of DNA by Les devoid of stomata [29,30]; indicating a different et al. [15], Chen et al. [17] and Ross et al. [18] evolutionary adaptation trend. have shown strong evidence of a monophyletic freshwater origin within the Hydrocharitaceae . Records indicate that stomatal apparatus Based on different phylogenetic analyses development occurred at least four hundred incorporating single and multiple gene million years ago (400 MYA) during the sequences of cpDNA, mtDNA, nrDNA, rbcL and early evolution of plants [31]. At that time ndh, and morphological characteristics; Les & epidermal cells became interrupted by minute Tippery [1] and Ross et al. [18] confirmed their openings delimited by two specialized cells, the aquatic origin as well as the inclusion of the three guard cells. Stomata are common to living marine genera ( Thallasia, Halophila and plants in both land and fresh water environments, Enhalus ) into a single clade [1,15,18,24]. but previously unknown in seagrasses Contrary to other seagrasses in the Core [14,29,30]. In terrestrial plants, it is believed Alismatids, pseudogenization of ndh genes that these specialized structures are involved in between the seagrasses ( Thallasia, Halophila the exchange of gases between the plant and and Enhalus ) and their close freshwater relative its environment due to the difference in osmotic Vallisneria was confirmed with 100% bootstrap pressure between the leaves and the roots. support [18]. In submerged aquatic plants, these same

The Hydrocharitaceae group has a cosmopolitan specialized structures allow the plants to distribution and is well represented in the fossil extrude water in a liquid form. However, record in Europe and North America. The only recently have we begun to understand divergence time of Hydrocharitaceae is still a and identify some of the environmental subject of debate and two competing ages (one factors that control stomatal development much more recent than the other) have been [32-35]. proposed. Kato et al. [25] dated the seagrasses within Hydrocharitaceae at 119±11 MYA by The presence of more advanced stomatal types analyses using the substitution rates of rbcL and such as the paracytic stomatal complex (in which matK. However, this time overlaps with the subsidiary cells that flank the stoma are parallel generally accepted age of the order Alismatales with the long axis of the guard cells) and the thus putting the validity of the results of that tetracytic stomatal complex (where guard cells study into doubt [26]. Janssen & Bremer [10] are surrounded by four subsidiary cells) are placed the crown node age of this family in the common among freshwater monocots [36] but Late Cretaceous (75 MYA) by analyses using believed to be absent among marine species rbcL and fossil calibrations also confirmed by seagrasses [14,29,30]. A recent report [19] on Chen et al. [17]. the presence of paracytic stomata in Thalassia testudinum Banks ex König marine plants 2.2 Morphological Characters growing in the proximities of coastal freshwater intrusions raises the question of the possible The marine Hydrocharitaceae differ dramatically evolutionary pathway of the Hydrocharitaceae from other marine angiosperm lineages in seagrasses.

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Futher examination of the Floridian fossil a marine environment can cause a change in the seagrass Thalassites parkavonensis Benzecry & marine plant’s hydrostatic pressure, thereby Brack-Hanes ( Hydrocharitaceae ) [37] which is inducing the phenotypic expression of sto mata. also believed to have occurred in areas of “leaky coastal margins” [38,39] , have shown to contain Several environmental factors such as light, paracytic stomata (Fig. 1) similar to those of temperature, dissolved oxygen and ionic other Hydrocharitaceae species as described by concentration can, indeed, influence the [13,19,36,40-42] and others. expression of anatomical characters in plants. Allsopp [52] and Sculthorpe [53] reported that These discoveries as well as the current environmental factors such as water stress or a environmental conditions where seagrasses are change in light conditions have induced a found may indicate that phenotypic plasticity is heterophyllous switch in freshwater aquatic operating in seagrasses just as it has in many plants and that those changes are reversible. aquatic and terrestrial plants [33 ,43-46]. To Experiments by Ueno et al. [54], Bowes & accurately determine patterns of plasticity and to Salvucci [55], Reiskind et al. [56] and Sultan [57], investigate their ecological and evolutionary demonstrate d that a change from C3 to C4 implications, we need to better understand the metabolism can occur within a plant when carbon environmental context in which phenotypes are dioxide is limited in the water. This biochemical expressed. change also causes structural changes such as the induction of Kranz anatomy in submerged 2.2.1 Sample examined amphibious plants [58].

Fossil, Thalassites parkavonensis Benzecry & Brack-Hanes [37], Fairleigh Dickinson University Paleobotanical Collection, specimen Holotype - AP Series # 267Ac and 267Bc (part and counterpart), Paratypes – AP Series # 268Ab, 268Ca, 268Cb, 268Cc, 268Cd, 268Ce, 275C, 276A. Samples collected at the dolomite/limestone quarry, approximately 1.5 miles south of Gulf Hammock (sec. 28, T14s, R16s), Le vy County, Florida. Stratigraphy: Avon Park Formation, Claiborne Stage, Late Middle Eocene (38 MYA) [47].

2.3 Ecological and Environmental Conditions

The Atlantic Coastal Plain of Florida is underlain by a blanket of Miocene and post -Miocene siliciclastic deposits that overlie a thick sequence of Tertiary carbonates composed of Eocene to Miocene limestone and dolostone. Florida's limestone bedrock is co ntinuously dissolved by Fig. 1. Thalassites parkavonensis Benzecry & moving water on the surface and underground, Brack-Hanes thus forming its karst topography. Submarine (Fossil Leaf sample # 267Ac, Fairleigh Dickinson groundwater discharges (SGD) and other karst University Paleobotanical Collection) SEM micrograph of leaf epidermis and paracytic stomata. Stomatal features present today along the apparatus comprised of two small guard cells (GC) coasts and extending below sea level, occurred 32 µm x 12 µm each, with prominent poral thickenings du ring a low stand of the Pleistocene sea when surrounded by two large (43µm x 17µm ) reniform the top of the saturated zone stood lower than subsidiary cells (SC). Scale bar = 10µm the bottom of the deepest natural wells [48 -50]. Carruthers et al. [51] reported that outflow from Vallisneria and Hydrilla species are vital submarine springs present both in Mexico and components of many freshwater habitats that can Florida may be influ encing nutrient processes tolerate moderately short-term exposure to within Thalassia testudinum meadows. It is mesohaline conditions have become the main plausible, therefore, that an influx of freshwater in subject of numerous salt tolerance studies

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[59-63]. Experiments dealing with chronic or sub- water environment to a submerged marine lethal salinity exposure of submerged aquatic environment within the Subfamily Hydrilloideae. vegetation have resulted in physiological changes [64] and population level changes [65]. ACKNOWLEDGEMENT Larkin et al. [66] studies of Thalassia testudinum revealed low levels of genetic diversity and This investigation was supported by a Fairleigh differentiation among Thalassia populations. Dickinson University Research Grant to Alice However, Hackney and Durako [67] and Kahn Benzecry. and Durako [68] reported that regional environmental differences in Florida Bay have COMPETING INTERESTS significantly affected trends in the morphology of Thalassia testudinum. A series of temperature Authors have declared that no competing and salinity stress tolerance experiments in interests exist. Thalassia testudinum [68-72] have confirmed the ability of this species to adapt to environmental REFERENCES changes leading to the full modification necessary for a harsh marine environment. The 1. Les DH, Tippery NP. In time and with occurrence of stomata in some marine water the systematics of alismatid hydrocharitaceans ( Thalassia testudinum and monocotyledons. In Wilki, P. & Mayo SJ. Thalassites parkavonensis ) growing in “leaky editors. Early events in monocot evolution . coastal margins” provides evidence for Published by Cambridge University Press. phylogenic pathways in that family, but does not The Systemic Association. 2013;118-164; address the subject of the evolution of 2. Barrett SCH, Eckert CG, Husband BC. seagrasses within other families. The fact that Evolutionary processes in aquatic plant stomata were found in only those seagrasses populations. Aquatic Botany. 1993; living in close proximity to freshwater intrusions 44(2):105-145. of coastal environments with SGD, implies that 3. Les DH. Breading systems, population freshwater influx is now and possibly was a structure and evolution in hydrophylus recurring stressful condition for the plants. Since angiosperms. Annals of the Missouri only Hydrocharitacean seagrasses collected from Botanical Gardens. 1988;75:819-835. coastal environments having freshwater 4. Friis EM, Pedersen KR, Crane PR. intrusions have been described with stomata- Araceae from the early cretaceous of bearing leaves, it becomes credible that the Portugal: Evidence on the emergence of predisposition (genetic makeup) for stomata is monocotyledons. Procedures of the present in the plant, regardless of expression. National Academy of Sciences (USA). Furthermore, the occurrence of stomata in an 2004;101:16565-1570. Eocene hydrocharitacean freshwater Hydrilla 5. Smith S. The fossil record of species [73,74] and the marine Thalassites noncommelinid monocots, In Wilki P, Mayo parkavonensis [37] from a coastal area with SGD SJ. editors. Early events in monocot demonstrates that it was a character expressed evolution. Published by Cambridge by hydrocharid in similar environments millions of University Press. The Systemic years ago (about 38 MYA) just as it is today. Association. 2013;29-59. 6. Bremer K. Early cretaceous lineages of 3. CONCLUSION monocot flowering plants. Proceedings of the National Academy of Sciences (USA). Records indicate that aquatic monocot ancestors 2000;97:4707-4711. were able to adapt to a continuously changing 7. Wikström M, Savolainene V, Chase MW. environment caused by the widespread Evolution of the angiosperms: Calibrating continental flooding during the Cretaceous the family tree. Proceedings of the Royal Period where seagrasses first occurred [4,5] to a Society of London, Biological Sciences. gradual regression of inland seas during the 2001;268:2211–2220. Eocene, leading to the subsequent adaptation 8. Chase MW. Monocot relationships: An into a complete submerged marine environment. overview of the best characterized major Hydrocharitaceae seagrasses’ aquatic ancestry, angiosperm clade. American Journal of as confirmed by molecular studies [1,17,18] and Botany. 2004;91:1645–1665. the facts outlined in this paper, further support 9. Sanderson MJ, Thorne JL, Wilk N, Bremer the idea of a complete adaptation from a fresh KG. Molecular evidence on plant

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