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Osmunda pulchella sp. nov. from the Jurassic of Sweden--reconciling molecular and fossil evidence in the phylogeny of modern royal ferns (Osmundaceae).

Bomfleur B, Grimm GW, McLoughlin S - BMC Evol. Biol. (2015)

Bottom Line: Osmunda pulchella is likely a precursor of the Osmundastrum lineage.The recently proposed root placement in Osmundaceae-based solely on molecular data-stems from possibly misinformative outgroup signals in rbcL and atpA genes.We conclude that the seemingly conflicting evidence from morphological, anatomical, molecular, and palaeontological data can instead be elegantly reconciled under the assumption that Osmunda is indeed monophyletic.

View Article: PubMed Central - PubMed

Affiliation: Department of Palaeobiology, Swedish Museum of Natural History, Stockholm, Sweden. benjamin.bomfleur@nrm.se.

ABSTRACT

Background: The classification of royal ferns (Osmundaceae) has long remained controversial. Recent molecular phylogenies indicate that Osmunda is paraphyletic and needs to be separated into Osmundastrum and Osmunda s.str. Here, however, we describe an exquisitely preserved Jurassic Osmunda rhizome (O. pulchella sp. nov.) that combines diagnostic features of both Osmundastrum and Osmunda, calling molecular evidence for paraphyly into question. We assembled a new morphological matrix based on rhizome anatomy, and used network analyses to establish phylogenetic relationships between fossil and extant members of modern Osmundaceae. We re-analysed the original molecular data to evaluate root-placement support. Finally, we integrated morphological and molecular data-sets using the evolutionary placement algorithm.

Results: Osmunda pulchella and five additional Jurassic rhizome species show anatomical character suites intermediate between Osmundastrum and Osmunda. Molecular evidence for paraphyly is ambiguous: a previously unrecognized signal from spacer sequences favours an alternative root placement that would resolve Osmunda s.l. as monophyletic. Our evolutionary placement analysis identifies fossil species as probable ancestral members of modern genera and subgenera, which accords with recent evidence from Bayesian dating.

Conclusions: Osmunda pulchella is likely a precursor of the Osmundastrum lineage. The recently proposed root placement in Osmundaceae-based solely on molecular data-stems from possibly misinformative outgroup signals in rbcL and atpA genes. We conclude that the seemingly conflicting evidence from morphological, anatomical, molecular, and palaeontological data can instead be elegantly reconciled under the assumption that Osmunda is indeed monophyletic.

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Anatomical and cytological details of Osmunda pulchella sp. nov. from the Lower Jurassic of Skåne, southern Sweden (A–F, I: NRM-S069656; G, H, J, K: NRM-S069658). a Detail showing pith parenchyma (bottom), stelar xylem cylinder dissected by complete leaf gaps, triangular section of phloem projecting into leaf gap, and parenchymatous inner cortex (top); note mesarch leaf-trace protoxylem initiation in the stelar xylem segment on the right. b Detail of (a) showing peripheral pith parenchyma and stem xylem. c Detail of stem xylem showing tracheid pitting. d Endarch leaf trace emerging from the stele and associated with a single root. e Leaf trace in the inner cortex of the stem showing single, endarch protoxylem cluster. f Leaf trace immediately distal to initial protoxylem bifurcation in the outermost cortex of the stem. g Root vascular bundle showing well-preserved scalariform pitting of metaxylem tracheids. h Well-preserved pith parenchyma showing membrane-bound cytoplasm with cytosol particles and interphase nuclei containing nucleoli. i, j Nuclei with conspicuous nucleoli (in interphase: I) or with distinct chromatid strands (in prophase: J). k Transverse section through root showing diarch vascular bundle, parenchymatous inner cortex with isolated fibre strands, and prominent fibrous outer cortex. Scale bars: (a) = 100 μm; (b, e, f, h) = 50 μm; (c, g) = 25 μm; (d) = 200 μm; (i, j) = 5 μm; (k) = 250 μm
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Fig4: Anatomical and cytological details of Osmunda pulchella sp. nov. from the Lower Jurassic of Skåne, southern Sweden (A–F, I: NRM-S069656; G, H, J, K: NRM-S069658). a Detail showing pith parenchyma (bottom), stelar xylem cylinder dissected by complete leaf gaps, triangular section of phloem projecting into leaf gap, and parenchymatous inner cortex (top); note mesarch leaf-trace protoxylem initiation in the stelar xylem segment on the right. b Detail of (a) showing peripheral pith parenchyma and stem xylem. c Detail of stem xylem showing tracheid pitting. d Endarch leaf trace emerging from the stele and associated with a single root. e Leaf trace in the inner cortex of the stem showing single, endarch protoxylem cluster. f Leaf trace immediately distal to initial protoxylem bifurcation in the outermost cortex of the stem. g Root vascular bundle showing well-preserved scalariform pitting of metaxylem tracheids. h Well-preserved pith parenchyma showing membrane-bound cytoplasm with cytosol particles and interphase nuclei containing nucleoli. i, j Nuclei with conspicuous nucleoli (in interphase: I) or with distinct chromatid strands (in prophase: J). k Transverse section through root showing diarch vascular bundle, parenchymatous inner cortex with isolated fibre strands, and prominent fibrous outer cortex. Scale bars: (a) = 100 μm; (b, e, f, h) = 50 μm; (c, g) = 25 μm; (d) = 200 μm; (i, j) = 5 μm; (k) = 250 μm

Mentions: The stem is ca 7.5 mm in diameter, and consists of an ectophloic-dictyoxylic siphonostele surrounded by a two-layered cortex (Figs. 1d, e, 2, 3, 7a). The pith is ca 1.5 mm in diameter and entirely parenchymatous (Fig. 2). A thin region at the outermost periphery of the pith consists of a few rows of parenchyma cells that are considerably more slender (ca 20–30 μm wide) than those in the central portion of the pith (usually ≥ 50 μm wide; Figs. 3, 4a, b). Furthermore, cell walls in some regions of the pith periphery may be thicker and more clearly visible than in the centre (Figs. 3, 4b). However, there is no evidence for the presence of an internal endodermis or internal phloem. Given that endodermal layers are recognizable in the stem and petiole cortices (e.g. Fig. 5f), we are certain that the absence of an internal endodermis is an original feature, and not the result of inadequate preservation. The xylem cylinder is ca 0.4 mm and ca 8–12 tracheids thick, and dissected by narrow, mostly complete, immediate leaf gaps into about 20 xylem segments in a given transverse section. The phloem forms an entire ring around the stele; it is most easily recognizable opposite a leaf gap, where it forms a narrow wedge-shaped patch of large, thin-walled cells that projects slightly towards the gap in transverse section (Figs. 3, 4a).Fig. 2


Osmunda pulchella sp. nov. from the Jurassic of Sweden--reconciling molecular and fossil evidence in the phylogeny of modern royal ferns (Osmundaceae).

Bomfleur B, Grimm GW, McLoughlin S - BMC Evol. Biol. (2015)

Anatomical and cytological details of Osmunda pulchella sp. nov. from the Lower Jurassic of Skåne, southern Sweden (A–F, I: NRM-S069656; G, H, J, K: NRM-S069658). a Detail showing pith parenchyma (bottom), stelar xylem cylinder dissected by complete leaf gaps, triangular section of phloem projecting into leaf gap, and parenchymatous inner cortex (top); note mesarch leaf-trace protoxylem initiation in the stelar xylem segment on the right. b Detail of (a) showing peripheral pith parenchyma and stem xylem. c Detail of stem xylem showing tracheid pitting. d Endarch leaf trace emerging from the stele and associated with a single root. e Leaf trace in the inner cortex of the stem showing single, endarch protoxylem cluster. f Leaf trace immediately distal to initial protoxylem bifurcation in the outermost cortex of the stem. g Root vascular bundle showing well-preserved scalariform pitting of metaxylem tracheids. h Well-preserved pith parenchyma showing membrane-bound cytoplasm with cytosol particles and interphase nuclei containing nucleoli. i, j Nuclei with conspicuous nucleoli (in interphase: I) or with distinct chromatid strands (in prophase: J). k Transverse section through root showing diarch vascular bundle, parenchymatous inner cortex with isolated fibre strands, and prominent fibrous outer cortex. Scale bars: (a) = 100 μm; (b, e, f, h) = 50 μm; (c, g) = 25 μm; (d) = 200 μm; (i, j) = 5 μm; (k) = 250 μm
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4487210&req=5

Fig4: Anatomical and cytological details of Osmunda pulchella sp. nov. from the Lower Jurassic of Skåne, southern Sweden (A–F, I: NRM-S069656; G, H, J, K: NRM-S069658). a Detail showing pith parenchyma (bottom), stelar xylem cylinder dissected by complete leaf gaps, triangular section of phloem projecting into leaf gap, and parenchymatous inner cortex (top); note mesarch leaf-trace protoxylem initiation in the stelar xylem segment on the right. b Detail of (a) showing peripheral pith parenchyma and stem xylem. c Detail of stem xylem showing tracheid pitting. d Endarch leaf trace emerging from the stele and associated with a single root. e Leaf trace in the inner cortex of the stem showing single, endarch protoxylem cluster. f Leaf trace immediately distal to initial protoxylem bifurcation in the outermost cortex of the stem. g Root vascular bundle showing well-preserved scalariform pitting of metaxylem tracheids. h Well-preserved pith parenchyma showing membrane-bound cytoplasm with cytosol particles and interphase nuclei containing nucleoli. i, j Nuclei with conspicuous nucleoli (in interphase: I) or with distinct chromatid strands (in prophase: J). k Transverse section through root showing diarch vascular bundle, parenchymatous inner cortex with isolated fibre strands, and prominent fibrous outer cortex. Scale bars: (a) = 100 μm; (b, e, f, h) = 50 μm; (c, g) = 25 μm; (d) = 200 μm; (i, j) = 5 μm; (k) = 250 μm
Mentions: The stem is ca 7.5 mm in diameter, and consists of an ectophloic-dictyoxylic siphonostele surrounded by a two-layered cortex (Figs. 1d, e, 2, 3, 7a). The pith is ca 1.5 mm in diameter and entirely parenchymatous (Fig. 2). A thin region at the outermost periphery of the pith consists of a few rows of parenchyma cells that are considerably more slender (ca 20–30 μm wide) than those in the central portion of the pith (usually ≥ 50 μm wide; Figs. 3, 4a, b). Furthermore, cell walls in some regions of the pith periphery may be thicker and more clearly visible than in the centre (Figs. 3, 4b). However, there is no evidence for the presence of an internal endodermis or internal phloem. Given that endodermal layers are recognizable in the stem and petiole cortices (e.g. Fig. 5f), we are certain that the absence of an internal endodermis is an original feature, and not the result of inadequate preservation. The xylem cylinder is ca 0.4 mm and ca 8–12 tracheids thick, and dissected by narrow, mostly complete, immediate leaf gaps into about 20 xylem segments in a given transverse section. The phloem forms an entire ring around the stele; it is most easily recognizable opposite a leaf gap, where it forms a narrow wedge-shaped patch of large, thin-walled cells that projects slightly towards the gap in transverse section (Figs. 3, 4a).Fig. 2

Bottom Line: Osmunda pulchella is likely a precursor of the Osmundastrum lineage.The recently proposed root placement in Osmundaceae-based solely on molecular data-stems from possibly misinformative outgroup signals in rbcL and atpA genes.We conclude that the seemingly conflicting evidence from morphological, anatomical, molecular, and palaeontological data can instead be elegantly reconciled under the assumption that Osmunda is indeed monophyletic.

View Article: PubMed Central - PubMed

Affiliation: Department of Palaeobiology, Swedish Museum of Natural History, Stockholm, Sweden. benjamin.bomfleur@nrm.se.

ABSTRACT

Background: The classification of royal ferns (Osmundaceae) has long remained controversial. Recent molecular phylogenies indicate that Osmunda is paraphyletic and needs to be separated into Osmundastrum and Osmunda s.str. Here, however, we describe an exquisitely preserved Jurassic Osmunda rhizome (O. pulchella sp. nov.) that combines diagnostic features of both Osmundastrum and Osmunda, calling molecular evidence for paraphyly into question. We assembled a new morphological matrix based on rhizome anatomy, and used network analyses to establish phylogenetic relationships between fossil and extant members of modern Osmundaceae. We re-analysed the original molecular data to evaluate root-placement support. Finally, we integrated morphological and molecular data-sets using the evolutionary placement algorithm.

Results: Osmunda pulchella and five additional Jurassic rhizome species show anatomical character suites intermediate between Osmundastrum and Osmunda. Molecular evidence for paraphyly is ambiguous: a previously unrecognized signal from spacer sequences favours an alternative root placement that would resolve Osmunda s.l. as monophyletic. Our evolutionary placement analysis identifies fossil species as probable ancestral members of modern genera and subgenera, which accords with recent evidence from Bayesian dating.

Conclusions: Osmunda pulchella is likely a precursor of the Osmundastrum lineage. The recently proposed root placement in Osmundaceae-based solely on molecular data-stems from possibly misinformative outgroup signals in rbcL and atpA genes. We conclude that the seemingly conflicting evidence from morphological, anatomical, molecular, and palaeontological data can instead be elegantly reconciled under the assumption that Osmunda is indeed monophyletic.

Show MeSH