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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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Related in: MedlinePlus

Phylogenetic tree, optimized under maximum likelihood (ML), showing unambiguously resolved relationships among extant Osmundaceae and the conflicting root-placement (outgroup-inferred) signals from individual gene regions. Based on the molecular matrix compiled and employed by Metzgar et al. [32]. All backbone branches received full maximum-likelihood bootstrap support (BSML = 100) based on the concatenated data; support for leaf-branches not shown (see Additional file 1 [ESA])
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Fig10: Phylogenetic tree, optimized under maximum likelihood (ML), showing unambiguously resolved relationships among extant Osmundaceae and the conflicting root-placement (outgroup-inferred) signals from individual gene regions. Based on the molecular matrix compiled and employed by Metzgar et al. [32]. All backbone branches received full maximum-likelihood bootstrap support (BSML = 100) based on the concatenated data; support for leaf-branches not shown (see Additional file 1 [ESA])

Mentions: The gene jackknifing and single-gene analyses reveal ambiguity concerning the position of the Osmundaceae root in the data of Metzgar et al. [32] (Fig. 10). As in the original analysis [32], support for backbone branches is effectively unambiguous based on the concatenated data, and the outgroup-inferred root is placed between Osmundastrum and the remainder of the family, resolving the traditional genus Osmunda (Osmunda s.l.) as a grade (‘paraphyletic Osmunda scenario’). The signal for this root placement stems from the two coding plastid gene regions (atpA and rbcL). In the more (but not most) variable spacer regions (atpB-rbcL, rbcL-accD, and trnL-trnF to a lesser degree), however, a competing signal is found resolving Osmunda s.l. as a clade (‘monophyletic Osmunda scenario’). The most variable non-coding spacer regions (trnG-trnR; rps4-trnS; and trnL-trnF to some degree) provided only ambiguous signals including potential outgroup-branch placements deep within the Leptopteris-Todea and Osmunda sub-trees or showed a preference for an Osmundastrum-Leptopteris-Todea clade as sister to Osmunda s.str.Fig. 10


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)

Phylogenetic tree, optimized under maximum likelihood (ML), showing unambiguously resolved relationships among extant Osmundaceae and the conflicting root-placement (outgroup-inferred) signals from individual gene regions. Based on the molecular matrix compiled and employed by Metzgar et al. [32]. All backbone branches received full maximum-likelihood bootstrap support (BSML = 100) based on the concatenated data; support for leaf-branches not shown (see Additional file 1 [ESA])
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig10: Phylogenetic tree, optimized under maximum likelihood (ML), showing unambiguously resolved relationships among extant Osmundaceae and the conflicting root-placement (outgroup-inferred) signals from individual gene regions. Based on the molecular matrix compiled and employed by Metzgar et al. [32]. All backbone branches received full maximum-likelihood bootstrap support (BSML = 100) based on the concatenated data; support for leaf-branches not shown (see Additional file 1 [ESA])
Mentions: The gene jackknifing and single-gene analyses reveal ambiguity concerning the position of the Osmundaceae root in the data of Metzgar et al. [32] (Fig. 10). As in the original analysis [32], support for backbone branches is effectively unambiguous based on the concatenated data, and the outgroup-inferred root is placed between Osmundastrum and the remainder of the family, resolving the traditional genus Osmunda (Osmunda s.l.) as a grade (‘paraphyletic Osmunda scenario’). The signal for this root placement stems from the two coding plastid gene regions (atpA and rbcL). In the more (but not most) variable spacer regions (atpB-rbcL, rbcL-accD, and trnL-trnF to a lesser degree), however, a competing signal is found resolving Osmunda s.l. as a clade (‘monophyletic Osmunda scenario’). The most variable non-coding spacer regions (trnG-trnR; rps4-trnS; and trnL-trnF to some degree) provided only ambiguous signals including potential outgroup-branch placements deep within the Leptopteris-Todea and Osmunda sub-trees or showed a preference for an Osmundastrum-Leptopteris-Todea clade as sister to Osmunda s.str.Fig. 10

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
Related in: MedlinePlus