Hiya: A new genus segregated from Hypolepis in the fern family Dennstaedtiaceae, based on phylogenetic evidence and character evolution
Graphical abstract
Introduction
Hypolepis Bernh. (Dennstaedtiaceae) was described by Bernhardi (1805), based on Lonchitis tenuifolia G. Forst. (≡Hypolepis tenuifolia (G. Forst.) Bernh. ex C. Presl), and is now recognized to comprise ca. 80 species worldwide (PPGI, 2016). It is distributed primarily in tropical and subtropical regions in both the New and Old Worlds and in various oceanic islands (Schwartsburd and Prado, 2015). Morphologically, Hypolepis is characterized by long-creeping, pubescent rhizomes, 2-pinnate-pinnatifid to 5-pinnate laminae, free veins, and marginal sori protected by an adaxial indusium that is either reflexed or plane (Bower, 1918, Tryon and Tryon, 1982, Kramer, 1990, Schölch, 2000, Becari-Viana and Schwartsburd, 2017).
Although Hypolepis is widely recognized as a natural lineage (Brownsey and Chinnock, 1984, Brownsey and Chinnock, 1987, Xing et al., 2013, Schwartsburd and Prado, 2015, Ppg, 2016), a few morphologically and cytologically aberrant species have long drawn attention as morphological outliers (Brownsey, 1983, Brownsey, 1987, Mickel and Smith, 2004). As pointed out by Brownsey (1987), three species, Hypolepis brooksiae Alderw., H. scabristipes Brownsey, and H. nigrescens Hook., differ from others in the genus by having leaves with indeterminate growth and armed with recurved black-tipped prickles. They also differ by forming fairly dense thickets of scandent leaves that exhibit rhythmic growth where successive pairs of pinnae emerge after a period of leaf elongation, similar to many Gleicheniaceae. Related to this, the basal-most pinnules are produced immediately adjacent to the developing crozier, protecting it before it elongates. These conspicuously placed pinnules have often been termed “stipule-like” because they act to protect the apical meristem like the stipules of many angiosperms. Furthermore, the species in this group for which chromosome counts have been made exhibit a base chromosome number of x = 29, whereas other Hypolepis are commonly derived from a x = 26 (Brownsey, 1983). Based on this cytological evidence, Brownsey (1987) suggested that these three species might in fact be better recognized as a distinct genus, and perhaps provide an evolutionary link between Dennstaedtia Bernh. and Hypolepis. However, these hypotheses have not yet been developed or tested phylogenetically, and analyses of ancestral states are also needed to figure out which characters can distinguish the three species morphologically.
Previous molecular phylogenetic studies have all placed Hypolepis within a strongly supported monophyletic clade (hereafter denoted as hypolepidoid, Fig. 1, Fig. 2), which includes Pteridium Gled. ex Scop., Paesia A. St.-Hil., Blotiella R.M. Tryon, and Histiopteris (J. Agardh) J. Sm. (Wolf, 1995, Smith et al., 2006, Schuettpelz and Pryer, 2007, Perrie et al., 2015, Schneider et al., 2016, Testo and Sundue, 2016). Although the genera in this clade have each been well supported as monophyletic, relationships among them remain poorly understood mainly due to the lack of informative characters in the plastid markers which these studies relied upon. Moreover, none of these studies sampled H. brooksiae, H. nigrescens, or H. scabristipes. Consequently, the monophyly of Hypolepis was tentatively accepted by PPG I (2016). In order to further investigate this question, we sampled two of the aberrant species, H. brooksiae and H. nigrescens, along with an additional 22 species of Dennstaedtiaceae. We developed a phylogeny using four plastid markers (atpA, rbcL, rpL6 and rps4-trnS IGS), aiming to: (1) test the monophyly of Hypolepis; (2) resolve phylogenetic relationships within the hypolepidoid ferns; and (3) confirm phylogenetic and taxonomical position of H. brooksiae, H. nigrescens, and H. scabristipes. Our analyses are further augmented by a reconstruction of ancestral morphological states focusing on characters emphasized in previous studies of the Dennstaedtiaceae thought to provide apomorphic states. Particular attention is paid to the evolution of the sorus, which we find, has been largely misinterpreted in systematic literature. To reflect these results, we describe below a new genus, Hiya, within the Dennstaedtiaceae. Finally, we address suites of characters associated with disturbance colonizing ferns, and describe a character syndrome associated with this niche, including long-creeping rhizomes, indeterminate and scandent leaves bearing prickles, and stipule-like pinnules that protect the expanding crozier.
Section snippets
DNA extraction, PCR amplification, and sequencing
Total genomic DNA was extracted from silica-dried leaves using a plant total genomic DNA kit (Tiangen, Beijing, China). Sequences for four chloroplast DNA regions rbcL, rps4-trnS, atpA and rpL6 were generated using protocols as described in previous studies with primers as follow: 1379R and 1F for rbcL (Little and Barrington, 2003), ESATPF412F and ESTRNR46F for atpA (Schuettpelz et al., 2006), trnS and rps4.5 for rps4-trnS, and rpL16-F-fern and rpL16-F-fern for rpL6 (Small et al., 2005).
Results
The combined dataset contained 4546 bp with 1900 variable sites and 1156 parsimony-informative sites. Maximum likelihood analysis of the combined dataset yielded an optimal tree with a −lnL = 23531.754486. Our phylogenetic analyses reveal that Hypolepis is not monophyletic as traditionally circumscribed (e.g., Tryon and Tryon, 1982, Kramer, 1990, Smith et al., 2006, Ppg, 2016). Instead, it is resolved as paraphyletic with two distantly related monophyletic groups, Hypolepis s.s. and the H.
Circumscription of the hypolepidoid genera
Our result that the hypolepidoid clade comprises six genera differs from that of Wolf (1995), who found Monachosorum as sister to the remaining genera, however, with weak bootstrap support (67%). More recently, Perrie et al. (2015) recognized Monachosorum as one of the three main clades within Dennstaedtiaceae together with the Dennstaedtioid and hypolepidoid clades. Our Bayesian tree further resolved Monachosorum as sister to all other clades of Dennstaedtiaceae with strong Bayesian posterior
Acknowledgements
We thank Yu-Feng Gu, Ke-Rui Huang, Zi-Yue Liu, Xi-Le Zhou, Zheng-Wei Wang, Hong-Mei Liu and Yea-Chen Liu for help in field investigation; Special thanks go to Hong-Jin Wei for sharing images, Chun-Xiang Li for sharing material, and Weston Testo for providing helpful comments on the manuscript. This study was supported by a grant from the National Natural Science Foundation of China (NSFC) to Hui Shang (#31700170) and to Yue-Hong Yan (#31370234), and the Scientific Research Program of
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