A dwarf conifer tree from the Triassic of Antarctica: the first fossil evidence of suppressed growth in a favorable climate?

BACKGROUND AND AIMS: The complexity of fossil forest ecosystems is difficult to reconstruct due to the fragmentary nature of the fossil record. However, detailed morpho-anatomical studies of well-preserved individual fossils can provide key information on tree growth and ecology, including in biomes with no modern analog such as the lush forests that developed in the polar regions during past greenhouse climatic episodes. METHODS: We describe an unusual-looking stem from Middle Triassic (ca 240 Ma) deposits of Antarctica with over 100 very narrow growth-rings and conspicuous persistent vascular traces through the wood. Sections of the specimen were prepared using the cellulose acetate peel technique to determine its systematic affinities and analyse its growth. KEY RESULTS: The new fossil shows similarities with the form genus Woodworthia and with conifer stems from the Triassic of Antarctica, and is assigned to the conifers. Vascular traces are interpreted as those of small branches retained on the trunk. Growth-ring analyses reveal one of the slowest growth rates reported in the fossil record, with an average of 0.2 mm/season. While the tree was growing within the Triassic polar circle, sedimentological data and growth-ring information from other fossil trees, including from the same locality, support the presence of favorable conditions in the region. CONCLUSIONS: The specimen is interpreted as a dwarf conifer tree that grew under a generally favorable regional climate but whose growth was suppressed due to stressful local site conditions. This is the first time that a tree with suppressed growth is identified as such in the fossil record, providing new insights on the structure of polar forests under greenhouse climates and, more generally, on the complexity of tree communities in deep time.

Using more than the oldest fossils: dating osmundaceae with three Bayesian clock approaches.

A major concern in molecular clock dating is how to use information from the fossil record to calibrate genetic distances from DNA sequences. Here we apply three Bayesian dating methods that differ in how calibration is achieved-"node dating" (ND) in BEAST, "total evidence" (TE) dating in MrBayes, and the "fossilized birth-death" (FBD) in FDPPDiv-to infer divergence times in the royal ferns. Osmundaceae have 16-17 species in four genera, two mainly in the Northern Hemisphere and two in South Africa and Australasia; they are the sister clade to the remaining leptosporangiate ferns. Their fossil record consists of at least 150 species in ∼17 genera. For ND, we used the five oldest fossils, whereas for TE and FBD dating, which do not require forcing fossils to nodes and thus can use more fossils, we included up to 36 rhizomes and frond compression/impression fossils, which for TE dating were scored for 33 morphological characters. We also subsampled 10%, 25%, and 50% of the 36 fossils to assess model sensitivity. FBD-derived divergence ages were generally greater than those inferred from ND; two of seven TE-derived ages agreed with FBD-obtained ages, the others were much younger or much older than ND or FBD ages. We prefer the FBD-derived ages because they best fit the Osmundales fossil record (including Triassic fossils not used in our study). Under the preferred model, the clade encompassing extant Osmundaceae (and many fossils) dates to the latest Paleozoic to Early Triassic; divergences of the extant species occurred during the Neogene. Under the assumption of constant speciation and extinction rates, the FBD approach yielded speciation and extinction rates that overlapped those obtained from just neontological data. However, FBD estimates of speciation and extinction are sensitive to violations in the assumption of continuous fossil sampling; therefore, these estimates should be treated with caution.

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

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.

Fossilized spermatozoa preserved in a 50-Myr-old annelid cocoon from Antarctica.

The origin and evolution of clitellate annelids--earthworms, leeches and their relatives--is poorly understood, partly because body fossils of these delicate organisms are exceedingly rare. The distinctive egg cases (cocoons) of Clitellata, however, are relatively common in the fossil record, although their potential for phylogenetic studies has remained largely unexplored. Here, we report the remarkable discovery of fossilized spermatozoa preserved within the secreted wall layers of a 50-Myr-old clitellate cocoon from Antarctica, representing the oldest fossil animal sperm yet known. Sperm characters are highly informative for the classification of extant Annelida. The Antarctic fossil spermatozoa have several features that point to affinities with the peculiar, leech-like 'crayfish worms' (Branchiobdellida). We anticipate that systematic surveys of cocoon fossils coupled with advances in non-destructive analytical methods may open a new window into the evolution of minute, soft-bodied life forms that are otherwise only rarely observed in the fossil record.

Triassic leech cocoon from Antarctica contains fossil bell animal.

Our understanding of the evolution of life on Earth is limited by the imperfection of the fossil record. One reason for this imperfect record is that organisms without hard parts, such as bones, shells, and wood, have a very low potential to enter the fossil record. Occasionally, however, exceptional fossil deposits that preserve soft-bodied organisms provide a rare glimpse of the true biodiversity during past periods of Earth history. We here present an extraordinary find of a fossil ciliate that is encased inside the wall layer of a more than 200 Ma leech cocoon from Antarctica. The microfossil consists of a helically contractile stalk that attaches to a main body with a peristomial feeding apparatus and a large C-shaped macronucleus. It agrees in every aspect with the living bell animals, such as Vorticella. Vorticellids and similar peritrichs are vital constituents of aquatic ecosystems worldwide, but so far have lacked any fossil record. This discovery offers a glimpse of ancient soft-bodied protozoan biotas, and also highlights the potential of clitellate cocoons as microscopic "conservation traps" comparable to amber.

Dying in the Sun: Direct evidence for elevated UV-B radiation at the end-Permian mass extinction.

Land plants can adjust the concentration of protective ultraviolet B (UV-B)-absorbing compounds (UACs) in the outer wall of their reproductive propagules in response to ambient UV-B flux. To infer changes in UV-B radiation flux at Earth's surface during the end-Permian mass extinction, we analyze UAC abundances in ca. 800 pollen grains from an independently dated Permian-Triassic boundary section in Tibet. Our data reveal an excursion in UACs that coincide with a spike in mercury concentration and a negative carbon-isotope excursion in the latest Permian deposits, suggesting a close temporal link between large-scale volcanic eruptions, global carbon and mercury cycle perturbations, and ozone layer disruption. Because enhanced UV-B radiation can exacerbate the environmental deterioration induced by massive magmatism, ozone depletion is considered a compelling ecological driver for the terrestrial mass extinction.

Response to Comment on "Dying in the Sun: Direct evidence for elevated UV-B radiation at the end-Permian mass extinction".

Seddon and Zimmermann have raised questions about the evidence for increased UV-B flux across the end-Permian mass extinction (EPME) that was presented in our recent study, specifically regarding the measurement of UV-B-absorbing compound (UAC) levels in fossil pollen. We respond to these points, arguing that the comparison of FTIR spectra of >250 million-year-old Permian fossil pollen with ~700-year-old subfossil pollen is not valid and that negligible nonrandom interference derived from water vapor fluctuations during data generation cannot coincidentally produce a substantial UAC peak during the EPME. Furthermore, we refute the suggestion that the measured aromatic peak at 1600 cm-1 could have been influenced by diagenetic products from other organic constituents of pollen. The most productive route forward will be to generate sporomorph geochemical data from additional Permian-Triassic boundary sections to test the results put forward in our study.

A hidden cradle of plant evolution in Permian tropical lowlands.

The latitudinal biodiversity gradient today has deep roots in the evolutionary history of Earth's biota over geologic time. In the marine realm, earliest fossil occurrences at low latitudes reveal a tropical cradle for many animal groups. However, the terrestrial fossil record-especially from drier environments that are thought to drive evolutionary innovation-is sparse. We present mixed plant-fossil assemblages from Permian equatorial lowlands in present-day Jordan that harbor precocious records of three major seed-plant lineages that all became dominant during the Mesozoic, including the oldest representative of any living conifer family. These finds offer a glimpse of the early evolutionary origins of modern plant groups in disturbance-prone tropical habitats that are usually hidden from observation.

The fossil Osmundales (Royal Ferns)-a phylogenetic network analysis, revised taxonomy, and evolutionary classification of anatomically preserved trunks and rhizomes.

The Osmundales (Royal Fern order) originated in the late Paleozoic and is the most ancient surviving lineage of leptosporangiate ferns. In contrast to its low diversity today (less than 20 species in six genera), it has the richest fossil record of any extant group of ferns. The structurally preserved trunks and rhizomes alone are referable to more than 100 fossil species that are classified in up to 20 genera, four subfamilies, and two families. This diverse fossil record constitutes an exceptional source of information on the evolutionary history of the group from the Permian to the present. However, inconsistent terminology, varying formats of description, and the general lack of a uniform taxonomic concept renders this wealth of information poorly accessible. To this end, we provide a comprehensive review of the diversity of structural features of osmundalean axes under a standardized, descriptive terminology. A novel morphological character matrix with 45 anatomical characters scored for 15 extant species and for 114 fossil operational units (species or specimens) is analysed using networks in order to establish systematic relationships among fossil and extant Osmundales rooted in axis anatomy. The results lead us to propose an evolutionary classification for fossil Osmundales and a revised, standardized taxonomy for all taxa down to the rank of (sub)genus. We introduce several nomenclatural novelties: (1) a new subfamily Itopsidemoideae (Guaireaceae) is established to contain Itopsidema, Donwelliacaulis, and Tiania; (2) the thamnopteroid genera Zalesskya, Iegosigopteris, and Petcheropteris are all considered synonymous with Thamnopteris; (3) 12 species of Millerocaulis and Ashicaulis are assigned to modern genera (tribe Osmundeae); (4) the hitherto enigmatic Aurealcaulis is identified as an extinct subgenus of Plenasium; and (5) the poorly known Osmundites tuhajkulensis is assigned to Millerocaulis. In addition, we consider Millerocaulis stipabonettiorum a possible member of Palaeosmunda and Millerocaulis estipularis as probably constituting the earliest representative of the (Todea-)Leptopteris lineage (subtribe Todeinae) of modern Osmundoideae.

Fossilized nuclei and chromosomes reveal 180 million years of genomic stasis in royal ferns.

Rapidly permineralized fossils can provide exceptional insights into the evolution of life over geological time. Here, we present an exquisitely preserved, calcified stem of a royal fern (Osmundaceae) from Early Jurassic lahar deposits of Sweden in which authigenic mineral precipitation from hydrothermal brines occurred so rapidly that it preserved cytoplasm, cytosol granules, nuclei, and even chromosomes in various stages of cell division. Morphometric parameters of interphase nuclei match those of extant Osmundaceae, indicating that the genome size of these reputed "living fossils" has remained unchanged over at least 180 million years-a paramount example of evolutionary stasis.

Thalloid organisms and the fossil record: New perspectives from the Transantarctic Mountains.

Thalloid body plans occur in several groups of organisms, including bryophytes, lichens and algae. While many aspects of the biology and ecology of extant thalloid organisms are well understood today, knowledge about the evolutionary history, palaeobiology and palaeoecology of these life forms remains limited. The recently discovered thalloid fossil Litothallus ganovex from the Triassic of Antarctica consists of fused vertical cell filaments forming a pseudoparenchymatous crust-like body, and most likely represents a freshwater macroalga. Other cuticle fragments from Antarctica are tentatively interpreted as remains of thallose liverworts. These unexpected new finds indicate that thalloid organisms are more frequent in the fossil record than previously assumed, and contribute to a better understanding of the palaeobiodiversity of ancient non-marine ecosystems.