Note to the reader: This is a post, not a scientific paper. Hence, my selection of literature is biased, and I may easily have overlooked something crucial. Admittedly, I used this opportunity to publish some reconstructions that never saw the light of day (so to say), for various reasons (like my reluctance to shoosh my brain-child into the obscurity of the Forest of Reviews so it may be judged by the Wizards of the Forest).
You are free to rectify or comment: the comment option is anonymous (only Google and possibly the NSA will be able to trace you down). I do not encourage anonymous comments: scientists should be able to openly express their opinion on scientific matters but the reality of confidential peer-review (in and beyond palaeobotany) demonstrates that this is not the case. As a matter of course, none of the authors of papers cited here have interacted with me regarding the content of this post. I am solely to blame 😈
Technical note: For some reason, Blogger replaces the internal links by extra-internal links when saving. I haven't found a fix for that except for re-copying the raw html-code, so links may bring you to a blank page (or Blogger's log-in page).
- Wang's “critique” of Herendeen et al. (2017)
- “Palaeobotanical Redux” ... would have been nice
- Angiosperms must root deep
- The thing about dating
- Late Jurassic is a good guess for the angiosperm crown age
- The (cryptic) sister lineages of angiosperms
- What a palaeobotanical redux on the age of angiosperms could look like
Wang’s paper is a comment to a review on the angiosperm fossil record by Herendeen et al. (2017) with the promising title "Palaeobotanical Redux: Revisiting the Age of Angiosperms"; published in March in one of Nature’s many online (this one is not open access) off-shots, Nature Plants, a "natureresearch journal".
|Price of access to Nature Plants|
Five bucks is a bit cheap for a Springer-Nature publication, though (probably not really a seller, yet, this Nature Plants).
Furious and entertainingly unprofessional with a true core: Wang's critique of Herendeen et al. (2017)Not interested, jump to next section
The first sentence of Wang's abstract summarises well the content of his – well – opinion piece: “A recently published review by Herendeen et al. is misleading, self-centered, self-praising, and self-conflicting.” You wouldn’t get this statement past the High Wizards of the Forest of Review, but it is true to a worrying degree. It is even more true for Wang’s short but fiery piece. Seems to be a commonly shared pattern among palaeobotanists interested in early angiosperms (never has been my cup of tea; curious but spurious data, especially when it comes to analysis, example provided below).
On the six pages, Wang ...
- ... shows the usual not-showing-much pictures (see also Herendeen et al. figs 3, 4; note the black and blue arrows in fig. 3A) that make many palaeobotanical papers entirely uninteresting to non-experts. The purpose of the figures is to back up some overly detailed discussion of why the interpretation of shadows, bulges and grooves by others were wrong culminating into dissection of phrases and descriptions in the literature that are seemingly in conflict with themselves.
- ... identified a "formidable trend in current palaeobotany ... misinterpreting data according to their own academics needs". Funny, because this has been done since the dawn of palaeobotanical research (compare e.g. Nathorst’s published drawings with the original, photo-realistic pencil drawings of his illustrator; Denk et al. 2011) and applies as much to Herendeen et al. as it applies to Wang's papers, or papers of other leading palaeobotanists (e.g. Rothwell & Nixon 2006; Rothwell et al. 2009; Crepet & Stevenson 2010). Although based on stones, palaeontology is, inevitably, the softest of all naturals sciences.
- ... gets generally lost, criticising Herendeen et al. being biased by their own research, rejecting results of others, and overlooking or downplaying important finds from other fields of science – by doing exactly the same.
|The motto of Herendeen et al.'s review paper|
"Palaeobotanial redux: revisiting the age of the angiosperms" ... would have been nice, indeedNot interested, jump to next section
Herendeen et al. write (abstract): "Their [the angiosperms] evolutionary and ecological appearance is therefore of considerable interest and has significant implications for understanding patterns of diversification in other lineages, including insects and other animals." and point out (here and there) the importance of the fossil record for other biological disciplines such as dating. Cited are only negative dating examples, of course, and not e.g. this one: Magallón et al. (2015). Which does much more for reviving palaeobotany than Herendeen et al.'s review paper and would have fully fit in their line of argumentation. And the four authors, acting as the Horsemen of Palaeobotany, are not only "... leaving the impression that they were only authoritative on the origin and early history of angiosperms" (Wang's abstract), they effectively are (for very good and some bad reasons). So, the minimum one could expect – regarding the title and with the authors' expertise and decades of research on early angiosperms – would have been a table or electronic supplement listing all the fossils that may represent early angiosperms or have falsely (according to the authors) be addressed as such.
- Names, current and original, with the appropriate references (original description, emendation);
- currently accepted ages, not a few fossil strata have been re-dated;
- botanical affinity according to the original authors and the opinion of the authors as experts on the topic.
Age. The age of crown-group Nymphaeales is around 125 m.y. (Magallón et al. (2015), (133.2-)126.7(-120.6) m.y.a. (Iles et al. 2014), as little as (176.6-)97.7(-42.8) m.y.a. (Zhou et al. 2014), or as much as ca 164 (Z. Wu et al. 2014), ca 188 m.y. (Tank et al. 2015) or ca 209 m.y. (Foster et al. 2016a: q.v. for details). The curious fossil Archaefructus, probably an aquatic plant and about 124 m.y. old, has been linked with Hydatellaceae in morphological analyses (Doyle & Endress 2007, 2010; Doyle 2008b). Although they have very little in common in terms of overall appearance, Archaefructus may be another early aquatic angiosperm with very unconventional floral morphology. Hydatellaceae may be represented in the pollen record from the Isle of Wight in rocks of some 130 m.y. of age (Hoffmann & Zetter 2010). Numerous other fossils [Stevens' list all Herendeen et al.'s fossils] have been identified as members of Nymphaeales; these are discussed below under Cabombaceae and Nymphaeaceae [here you'll find Monetianthus].In Herendeen you just can read: "The uncertainty over the phylogenetic position of Archaefructus provides a case in point." for "...the possibility that such fossils were actually on the angiosperm stem group rather than in the crown group" and citing three papers, but only one (Doyle & Endress 2014, the add-on to Doyle & Endress 2010 cited by Stevens, showing the same) that tried to place Archaefructus in an explicit phylogenetic context. Whereas the (neo)botanist Stevens (2001 onwards) provides a review of the earliest fossil record and, hence, demonstrates the use of palaeobotanical research, the expert palaeobotanists are busy to point out that fossils are so difficult to place (too many uncertainties around them) that they are essentially useless to neighbouring scientific fields. Not really a "redux", but what you'd expect from the Four Horsemen.
|Possible classification concepts for angiosperms. Blue cloud: not really (crown) angiosperms according to Herendeen et al.'s definition: "...crowngroup angiosperms, defined as the most recent common ancestors [plural? Hybrid or multiple origin(s) or mistype?] of all living angiosperms and its derivatives". Later in the text, Herendeen et al. argue that any fossil that cannot be reliably assigned to one of the modern, crown-group lineages (i.e. Amborellales to magnoliids), should also not be considered as a crown-group angiosperm, in violation of their own node-based definition (red cloud). Grey bar, Hennig's cladistic paradox (discrepancy between phylogenetic and cladistic classification systems; see also this recent post by D. Morrison)|
- Since none of the pre-Cretaceous fossils can be reliably associated with crown (!) angiosperms, they are likely not angiosperms at all.
PS Something Wang over-read (or did want to over-read) and, I may humbly add, a near-literal quote of what I told Horseman #2–#4 about a decade ago, when #2 made me a co-author (Friis et al. 2007; to the growing despair of #4, who prevented us from publishing this nonsense).
|A graphic depiction Herendeen et al.'s fuzzy logic:|
Why pre-Cretaceous pollen cannot be angiosperm pollen
Angiosperms have no close living relatives, hence must root deepNot interested, jump to next section
The basic situation is pretty simple. Molecular data clearly showed (and from the very start) that the angiosperm crown node (the Horsemen's training field) is far away from the angiosperm stem (root) node (which the Horsemen not really bother about); the angiosperm root length covers most of the crown-tip distances in all-angiosperm or all-spermatophyte (all living seed plants) trees. The figure below shows a ML tree inferred from a curated (much updated) data subset (same gene sample, less taxa) of Soltis et al. (2011), the molecular-phylogenetic paper cited in the Herendeen et al. A tree, I inferred about five years ago for an abandoned little project with a total-evidence dater and that I showed Horseman #2 (and others on occasion).
Even when we assume massive rate shifts (which are likely, note the branch-length imbalance in the ML tree above; see also Magallón et al. 2015), it is clear that the first member of the angiosperm lineage – the ancestor of modern angiosperms and their putative, so far cryptic sister lineages (but see below) as defined by the angiosperm stem (root) node – lived long before the last common ancestor of all modern (living) angiosperms – defined by the angiosperm crown node.
The thing with dating
Not interested, jump to next section
(why palaeobotanists should partake in it instead of ranting about it)
The combination of an extremely long-root, a condensed proximal part, and partly inflated distal part, explains the problem in dating stem (root) and crown ages and their vulnerability to sampling bias. Why it would have been crucial that the Horsemen would have put some effort in evaluating the fossil age constraints used for the many molecular dating studies when revisiting the age (crown and stem) of angiosperms. Who else is qualified to point to problematic constraints?
Let me illustrate the problem with a very crude dating experiment using Monetianthus, the fossil Wang gets lost about. Monetianthus has been character-wise and phylogenetically placed within the Nymphaeales, it's close to the Nymphaeaceae (Friis et al. 2009; see also Stevens 2010 onwards) and is probably (and "provisionally" as we write on p. 1091) late Aptian-early Albian, i.e. ~ 113 Ma (Cohen et al. 2013, updated). Ultrametrising the ML tree above and assuming a simple strict clock, we would infer
- a minimum angiosperm crown age of 270 Ma, mid-Permian, implausible and likely wrong, but a crown age not too far from the dating papers cited by the Horsemen (and published in peer-reviewed journals, likely without being reviewed by palaeobotanists);
- an angiosperm stem (root) age beyond the possible: c. 580 Ma; the time of the Ediacara biota, the first complex biocoenosis (marine naturally, the land was still barren).
|Crude, strict-clock estimates for root (stem; "Origin") and crown age ("MRCA") of the angiosperm lineage |
using Monethianthus' phylogenetic position within the Nymphaeales (Friis et al. 2009)
- Obviously there were rate shifts between the Nymphaeaceae crown and root and deeper branches, so applying a strict clock is fundamentally flawed.
- If we could sample the DNA of Monetianthus, we would likely find sequences much closer to the MRCA (tree distance = cumulative branch-length) than seen in the ultrametrised tree (same would apply for coeval members of the Trithuria and Amborella lineages).
- fix a minimum angiosperm crown age of 113 Ma; and we would
- estimate a Middle Triassic stem (root) age of 245 Ma.
|Same as above, but fixing the age of the MRCA|
of modern angiosperms to the age of Monetianthus.
- wind-dispersed – animal-dispersed pollen is generally rare(r), and often has patchy fossil records (even post-Early Cretaceous, when angiosperms already dominated the world);
- did not evolve their pollen sculpture in 50–100 Ma – which is something traditional palaeobotanists like to reject as possibility in more recent context per se when being confronted with > 50 Ma old pollen exactly looking like (lineage-diagnostic) modern counterparts.
Monetianthus is not the first angiosperm, there are older ones, but – the Horsemen's objective is destruction not revitalisation – Herendeen et al. prefer to not present them in a concise fashion (again see Magallón et al. 2015: fig. 1; much older clock-based estimates in contrast to the rule: node-based estimates should be – by principle – too young). In fact, the "redux" doesn't even provide or discuss candidates for the very earliest (crown or stem) angiosperms (but see Friis et al. 2011). Maybe because these candidates have been described by their competitors (Wang's opinion), maybe because they have simply no idea, maybe they are afraid to express it (my opinion; it could be wrong as in the case of Friis et al. 2001, what an opportunity for their enemies to get old-testimonial). Errare humanum est, but not an option for the demi-gods in their ivory towers.
Just for fun, let's assume Monetianthus is the first representative of the Nymphaeales s.str. (excluding the long-branched, potentially first-diverged and strongly derived Hydatellaceae; see also this post on misleading, long-branched roots). Result: crown age > 150 Ma, i.e. Late Jurassic; stem age > 320 Ma (mid-Carboniferous).
|One more, treating Monetianthus as the oldest record of the Nymphales s.str|
This does, however, not mean that Monetianthus is the first common ancestor of all Nymphaeales s.str., but that placing it there gives one more realistic root-crown-tip distances (i.e. compensates to some degree for the rate change). Fossils and molecular clocks can be co-informative and used to test hypothesis (and interpretations; see e.g. Bomfleur et al. 2015). Would possibly have been an important point to make in a "palaeobotanical redux" ...
Angiosperm crown-age? Late Jurassic is a good guessNot interested, jump to next section
A Late Jurassic crown-age, inferred by not a few old but also recent dating studies – none of which the Horsemen cite, following the 10th of the Holy Commandments of True Palaeobotany: Thou shalt not leave Thy Ivory Tower – makes sense when one tries to accommodate late Early/early Late Cretaceous angiosperm fossils in a phylogenetic framework, e.g. using a Bayesian total-evidence approach.
. See e.g. this 2017 (open access) paper by Sauquet, von Balthazar, ... & Schöneberger, published in another of Nature’s off-shots for an analysis-based reconstruction of how the flower of the MRCA of all modern angiosperms may have looked like. In contrast to many early (crown) angiosperm fossils, it is a "perfect flower", one of the synapomorphies of (modern) angiosperms, see e.g. Stevens' (2010) list.
All major lineages of extant angiosperms are known from the Early (mid-)Cretaceous, including sublineages relatively high-up in the currently accepted angiosperm tree. Herendeen et al. cite a couple of them (mostly those they described themselves for natural reasons). The root-proximal short branches (in molecular or combined trees) evidence that the initial radiation and diversification of the angiosperm crown group was fast. But, no angiosperm lineage evolved, radiated, and diversified within a few million years (see e.g. Magallón et al. 2015), thus, it is unlikely that the lineage including the common ancestor of all modern angiosperms, was a near-contemporary of the known, derived fossils.
The (cryptic) sister lineages are crucial to discuss age of angiospermsNot interested, jump to last section
Another way to define more sensible angiosperm root ages is to identify their sistergroup(s), in order to add informed "shadow-nodes" to the angiosperm root. Nodes that divide the root branch into the actual angiosperm root and the stem branch(es) of angiosperms and their putative sister clades.
The Horsemen point to "Caytonia [is] a well-known case", without providing any reference (the scope of Nature Plants is all plant-related research, so their reader may not be familiar with the well-known – in palaeobotany – case). Maybe to avoid citing their enemies (?) such as this study (officially peer-reviewed, but not by someone experienced in phylogenetic reconstructions): Rothwell, Crepet & Stockey (2009). Caytonia was resolved and well-supported (signal-wise) as sister of the angiosperms (Hilton & Bateman 2006; see also supplement to Friis et al. 2007). Fiercely disagreeing with Friis et al. (2007)’s conclusions and interpretations, Rothwell et al. put a lot of effort in re-coding the earlier matrix and re-scoring Caytonia to demonstrate that Caytonia is not a sister of the angiosperms. While doing so, they also decreased the amplitude of discriminating signal in the matrix (Grimm 2017a, 2017c), which lead (in their consensus trees) to a collapse of several unchallenged clades.
|Two neighbour-nets based on mean morphological distances inferred from Rothwell et al.'s 'matrix 5' (A, including the debated Erdtmanithecales) and their preferred ‘matrix 3’ (B). Values show non-parametric bootstrap (BS) support under the least-squares (via neighbour-joining) and parsimony optimality criteria (10,000 BS replicates) for compatible and competing phylogenetic splits. Green = splits in agreement with ..., blue = best-supported but not resolved in ..., and red = in conflict with the strict-consensus trees shown by the authors (see also this post on the principal problem with such matrices).|
This was collateral damage as Rothwell et al. mainly aimed to destroy the Erdtmanithecales, which linked the Bennettitales to the Gnetales. The Erdtmanithecales is the taxon Herendeen et al. use as example that pollen originally associated with angiosperms occurs in groups not related to angiosperms.
Nonetheless, the Erdtmanithecales, good taxon or not, and pollen associated with them, require further studies. Is it identical to the monosulcate pollen of living angiosperms? Is it possible that non-related gymnosperms and angiosperms (monosulcate pollen is typically found in five of the six main angiosperm lineages) evolved in parallel? Or is it an evidence for a shared common origin, a deep synapomorphy?
Remember: even reasonable clocks and fully constrained dated trees prefer a Carboniferous angiosperm stem age. Surely these first members of the angiosperm-lineage (from a modern-day, molecular perspective) were not only the ancestors of the angiosperms but likely some other, quite distinct, and extinct (Permian and) Mesozoic seed plants.
The association of Erdtmanithecales with Gnetales and Bennettitales is just one hypothesis. Horseman #2–#4 could have informed their first author that the matrix we used (Friis et al. 2007) prefers a BEG clade ("Erdtmanithecales-Bennettitales-Gnetales"; a good hypothesis based on the data), but that the signal was (and is; Grimm 2017b) too faint to rule out any other possibility. No matter which matrix I use (Friis et al.'s or Rothwell et al.'s), I can put the Erdtmanithecales also at the root of the angiosperms without inflicting too much pain. This would invalidate Herendeen et al.'s entire anti-angiosperm pollen argumentation, but open the avenue to treat conspicuously sculptured monosulcate pollen as unique to the angiosperm-lineage. Maybe it is even the only unique feature of modern angiosperms and their extinct precursors and direct sister lineages that can be found (traced) in the fossil record. Thus, invaluable for dating.
|Lee et al.'s (2011) phylogenomic tree showing angiosperms as sister to the gymnosperms (see also Magallón et al. 2015). Note the branch-length pattern: the angiosperm root is relatively short in comparison to within-angiosperm diversification. Based on the seen pattern a middle Carboniferous angiosperm stem age makes sense. But this may not be equivalent with the age of the first (stem) angiosperm as defined by the point where the lineage leading to the modern angiosperms diverged from its last extinct sister lineage. Age for gymnosperms taken from Earle's introductory page (see there for references). Earle cites a Late Triassic age for the so-far unplaced, extinct Bennettitales (235–202 Ma), (co-)dominant seed plants of the Mesozoic. With respect to current seed plant phylogenies (dated or undated), they are either part of the same lineage than the angiosperms or the (monophyletic) gymnosperms, or belong to a third lineage that diverged before the modern seed plants, i.e. before the mid-Carboniferous (unlikely).|
An important group – interacting between the unambiguous modern seed plant clades (angiosperms vs. gymnosperms) are the enigmatic and once dominant (mid- to high-latitudes) Bennetittales, a group severely under- and mis-represented in all all-spermatophyte matrices so far; a group difficult to place in a phylogenetic context and with unsculptured monosulcate pollen (similar to cycads, but not "angiosperm-like"; e.g. Pott, Fischer & Ashauer 2017)
With Caytonia out of the race and Bennetittales being too unique, a new candidate emerged recently that could be of use to inform the actual angiosperm (s.str.) stem node. But neither the acting Horsemen of Palaeobotany nor Wang comment on the Triassic – again, coincidence or consistent pattern? – Petriellales (Bomfleur et al. 2014). According to the most-recent spermatophyte morphological matrix (Rothwell & Stockey 2016), the Petriellales are a candidate for an (ancient) angiosperm sistergroup. If so, it would be another palaeobotanical evidence that the actual angiosperm lineage diverged by the Triassic (or before) and a point to make in a redux-review paper. Rothwell and co-workers' matrices are notoriously depleted of tree-like and discriminating signal (see this Genealogical World of Networks post), but the 2016 matrix is the first – when analysed using up-to-date methods (Coiro, Chomicki & Doyle 2017) – that prefers a placement of the Gnetidae (Gnetales) as sister to the remaining gymnosperms (Ginkgoidae, Pinidae and extinct relatives, including or excluding Cycadidae). A placement in agreement to e.g. phylogenomic analyses (e.g. Lee et al. 2011, figure above; the principal inter-seed plant relationships are a long-standing issue, see e.g. Mathews 2009; Mathews, Clements & Beilstein 2010). And the 2016 matrix places the Petriellales – their pollen is so far not known – firmly as sister to the angiosperms (Coiro et al. 2017; Grimm 2017a, b; see also the discussion in the original paper of Bomfleur et al. 2014).
What a palaeobotanical redux on the age of angiosperms could look likeWhen you read Herendeen et al. (2017), it is obvious that this review paper was not scrutinised during peer-review, but some sentences like those about Triassic "stem angiosperms" look like reluctant additions made during (quick) revision. It is clearly not a "redux", but a demonstration of we-will-stay-firm-and-ignorant-of-anything-else. This is a pity. Molecular dating done in ignorance of the fossil record is often for the bin. And more and more dater realised this.
Palaeobotanists would have a lot to offer and to throw in the ring since node dating depends strongly on placing the fossil on the right node, and using the oldest representative of a lineage. But that is only the beginning of what could become a dream-story of inter-disciplinary research.
In the last five years, two new methodologies have been proposed for which palaeobotanical expertise like that of the Four Horsemen of Palaeobotany or the Triumvirate of Hell would be crucial. Both approaches are theoretically (and in practise) superior to the traditional node dating: One is total-evidence dating (Ronquist et al. 2012), which will always be difficult using plant data sets (above; supplement to Grimm et al. 2015), and the fossilised-birth death (FBD) dating, which provided very nice (sensible) results even for flat and deep plant phylogenies (Grimm et al. 2015; Renner et al. 2016; see/cf. Denk et al. 2005; Denk & Grimm 2009; Bomfleur et al. 2015; Grímsson et al. 2016).
- Total-evidence dating needs a morphological partition that includes the fossils – something only palaeobotanists can provide (pers. experience, I can’t).
- FBD dating needs a comprehensive compilation of the fossil record – and you’ll be damned if you try to do that just by copy & paste from literature without any prior palaeobotanical knowledge.
And regarding “Palaeobotanical redux: revisiting the age of angiosperms” this should be done (not by a single person though; PB = palaeobotanists, NB = (neo)botanists, BI = (bio)informaticians):
- PB: Compile the entire Mesozoic fossil record of seed plants (taxon – age – assumed botanical affinity).
- BI (assisted by NB and PB): Select a set of molecular-phylogenetic hypotheses (based on recent studies, not six-year-old ones based on a data set that – partly – has been assembled 20–25 years ago and never been updated since then) and recruit a molecular data set providing sensible (on the backdrop of morphological and genetic diversity, and the fossil record) branch lengths.
- BI: Map the evolution of fossil-relevant traits onto the molecular tree(s) using a probabilistic approach to identify conserved and quick-evolving traits, and – eventually – diagnostic character suites (I'll elaborate the problem with synapomorphies in a follow-up post).
- PB + NB: Recruit and re-train a group of (systematic) botanists to trace back these traits in the fossil record, and give them unrestricted access to the material. When two doctors suggest two very different treatments (like current palaeobotanical debate), get a third, fresh opinion!
- BI: Do a fossilised-birth death dating on a taxon set that includes the least-diverged representatives of all main seed plant and angiosperm clades; if there is more than one alternative, test all of them. [I would always recruit (bio)informaticians for this job, who have no idea about the organism, hence, can work entirely unbiased]
- BI for PB: Make a series of node-dating tests to further reconcile the fossil record, the interpretation of fossils, with the molecular hypotheses – see e.g. Grimm & Renner 2013 for such an experiment and further references; and Hubert et al. (2014) for age estimates in oaks (Quercus) that fit well later palaeobotanical finds (Grímsson et al. 2015, 2016; I think both papers are examples of “palaeobotanical redux”; the only reason why there is no FBD dating yet for all Fagaceae (or all Fagales) – much needed in my opinion – is just the lack of human resources).
But as long as the few palaeobotanists with prominent positions and (obviously) research money (see acknowledgements in Herendeen et al. and Wang) spend their time (and review papers) criticising the work of others (and each other; e.g. Rothwell, Crepet & Stockey 2009; Crepet & Stevenson 2010; Herendeen et al. 2017; Wang 2017) rather than come together, haggle it out, and make a call to provide something useful for non-palaeobotanists … well, make an appointment with the undertaker.
References (bold font = open access)Bomfleur B, Decombeix A-L, Schwendemann AB, Escapa IH, Taylor EL, Taylor TN, McLoughlin S. 2014. Habit and ecology of the Petriellales, an unusual group of seed plants from the Triassic of Gondwana. International Journal of Plant Sciences 175:1062–1075.
Bomfleur B, Grimm GW, McLoughlin S. 2015. Osmunda pulchella sp. nov. from the Jurassic of Sweden—reconciling molecular and fossil evidence in the phylogeny of modern royal ferns (Osmundaceae). BMC Evolutionary Biology 15:126. http://dx.doi.org/10.1186/s12862-015-0400-7
Bomfleur B, Grimm GW, McLoughlin S. 2017. The fossil Osmundales (Royal Ferns)—a phylogenetic network analysis, revised taxonomy, and evolutionary classification of anatomically preserved trunks and rhizomes. PeerJ 5:e3433. https://peerj.com/articles/3433/
Cohen KM, Finney SC, Gibbard PL, Fan J-X. 2013 (updated). The ICS International Chronostratigraphic Chart. Episodes 36:199–204. http://www.stratigraphy.org/ICSchart/ChronostratChart2016-04.pdf
Coiro M, Chomicki G, Doyle JA. 2017. Experimental signal dissection and method sensitivity analyses reaffirm the potential of fossils and morphology in the resolution of seed plant phylogeny. bioRxiv DOI:10.1101/134262 http://biorxiv.org/content/early/2017/06/07/134262
Crepet WL, Stevenson DM. 2010. The Bennettitales (Cycadeoidales): a preliminary perspective of this arguably enigmatic group. In: Gee CT, ed. Plants in Mesozoic Time: Morphological Innovations, Phylogeny, Ecosystems. Bloomington: Indiana University Press, p. 215–244.
Denk T, Grimm GW. 2009. The biogeographic history of beech trees. Review of Palaeobotany and Palynology 158:83–100.
Denk T, Grimm GW, Hemleben V. 2005. Patterns of molecular and morphological differentiation in Fagus: implications for phylogeny. American Journal of Botany 92:1006-1016.
Denk T, Grímsson F, Zetter R, Símonarson LA. 2011. Art Meets Science–The Unpublished Drawings by Carl Hedelin and Thérèse Ekblom. Late Cainozoic Floras of Iceland. Heidelberg, New York: Springer, p. 723–824.
Doyle JA, Endress PK. 2010. Integrating Early Cretaceous fossils into the phylogeny of living angiosperms: Magnoliidae and eudicots. Journal of Systematics and Evolution 48:1–35.
Doyle JA, Endress PK. 2014. Integrating Early Cretaceous fossils into the phylogeny of living angiosperms: ANITA lines and relatives of Chloranthaceae. International Journal of Plant Sciences 175:555–600.
Earle CJ. 2010 onwards. The Gymnosperm Database. http://www.conifers.org/.
Friis EM, Crane PR, Pedersen KR, Bengtson S, Donoghue PCJ, Grimm GW, Stampanoni M. 2007. Phase-contrast X-ray microtomography links Cretaceous seeds with Gnetales and Bennettitales. Nature 450:549-552.
Friis EM, Pedersen KR, Crane PR. 2001. Fossil evidence of water lilies (Nymphaeales) in the Early Cretaceous. Nature 410:357–360. https://doi.org/10.1038/35066557
Friis EM, Pedersen KR, von Balthazar M, Grimm GW, Crane PR. 2009. Monetianthus mirus gen. et sp. nov., a nymphaealean flower from the early Cretaceous of Portugal. International Journal of Plant Sciences 170:1086-1101. http://www.jstor.org/stable/10.1086/605120
Goremykin VV, Hirsch-Ernst KI, Wölfl S, Hellwig FH. 2003. Analysis of the Amborella trichopoda choroplast genome sequence suggests that Amborella is not a basal angiosperm. Molecular Biology and Evolution 20:1499-1505.
Goremykin VV, Nikiforova SV, Cavalieri D, Pindo M, Lockhart PJ. 2015. The root of flowering plants and total evidence. Systematic Biology 64:879–891.
Grimm G. 2017a. Morphology-based neighbour-net of seed plants: quick exploratory data analysis of the matrix of Rothwell & Stockey (2016). figshare. https://doi.org/10.6084/m9.figshare.5143732.v1
Grimm GW. 2017b. Morphology-based neighbour-net of seed plants. figshare. https://doi.org/10.6084/m9.figshare.5111062.v1
Grimm GW. 2017c. Should we infer trees on treeunlikely matrices? In: Morrison DA, editor. The Genealogical World of Phylogenetic Networks. http://phylonetworks.blogspot.fr/2017/07/should-we-try-to-infer-trees-on.html
Grimm GW. 2018. A basic total evidence matrix for basal angiosperms — combining Soltis et al. (2011) with Doyle & Endress (2010). Fileset. Figshare. https://doi.org/10.6084/m9.figshare.5997656.v1
Grimm GW, Kapli P, Bomfleur B, McLoughlin S, Renner SS. 2015. Using more than the oldest fossils: Dating Osmundaceae with the fossilized birth-death process. Systematic Biology 64:396–405.
Grimm GW, Renner SS. 2013. Harvesting GenBank for a Betulaceae supermatrix, and a new chronogram for the family. Botanical Journal of the Linnéan Society 172:465–477.
Grímsson F, Grimm GW, Zetter R. 2017. Tiny pollen grains: first evidence of Saururaceae from the Late Cretaceous of western North America. PeerJ 5:e3434 [e-pub]. https://peerj.com/articles/3434
Grímsson F, Grimm GW, Zetter R, Denk T. 2016. Cretaceous and Paleogene Fagaceae from North America and Greenland: evidence for a Late Cretaceous split between Fagus and the remaining Fagaceae. Acta Palaeobotanica 56:247–305. http://dx.doi.org/10.1515/acpa-2016-0016
Grímsson F, Kapli P, Hofmann C-C, Zetter R, Grimm GW. 2017. Eocene Loranthaceae pollen pushes back divergence ages for major splits in the family. PeerJ 5:e3373 [e-pub]. https://peerj.com/articles/3373/
Grímsson F, Zetter R, Grimm GW, Krarup Pedersen G, Pedersen AK, Denk T. 2015. Fagaceae pollen from the early Cenozoic of West Greenland: revisiting Engler's and Chaney's Arcto-Tertiary hypotheses. Plant Systematics and Evolution 301:809–832. http://dx.doi.org/10.1007/s00606-014-1118-5
Heimhofer U, Hochuli PA, Burla S, Weissert H. 2007. New records of Early Cretaceous angiosperm pollen from Portuguese costal deposits: Implications for the timing of the early angiosperm radiation. Review of Palaeobotany and Palynology 144:39-76. http://www.sciencedirect.com/science/article/B6V6W-4KRY903-1/2/32eb034bf8edc42d7e002d2ff9021e0d
Herendeen PS, Friis EM, Pedersen KR, Crane PR. 2017. Palaeobotanical redux: revisiting the age of the angiosperms. Nature Plants 3, article no. 17015. https://dx.doi.org/10.1038/nplants.2017.15
Hilton J, Bateman RM. 2006. Pteridosperms are the backbone of seed-plant phylogeny. Journal of the Torrey Botanical Society 133:119-168.
Hochuli PA, Feist-Burkhardt S. 2004. A boreal early cradle of angiosperms? Angiosperm-like pollen from the Middle Triassic of the Barents Sea (Norway). Journal of Micropalaeontology 23:97–104.
Hochuli PA, Feist-Burkhardt S. 2013. Angiosperm-like pollen and Afropollis from the Middle Triassic (Anisian) of the Germanic Basin (Northern Switzerland). Frontiers in Plant Science DOI:10.3389/fpls.2013.00344.
Hubert F, Grimm GW, Jousselin E, Berry V, Franc A, Kremer A. 2014. Multiple nuclear genes stabilize the phylogenetic backbone of the genus Quercus. Systematics and Biodiversity 12:405–423.
Lee EK, Cibrian-Jaramillo A, Kolokotronis S-O, Katari MS, Stamatakis A, Ott M, Chiu JC, Little DP, Stevenson DW, McCombie WR, Martienssen RA, Coruzzi G, DeSalle R. 2011. A functional phylogenomic view of the seed plants. PloS Genetics 7:e1002411. https://doi.org/10.1371/journal.pgen.1002411Magallón S, Gómez-Acevedo S, Sánchez-Reyes LL, Hernández-Hernández T. 2015. A metacalibrated time-tree documents the early rise of ﬂoweringplant phylogenetic diversity. New Phytologist 207:437–453.
Manchester SR, Grímsson F, Zetter R. 2015. Assessing the fossil record of asterids in the context of our current phylogenetic framework. Annals of the Missouri Botanical Garden 100:329–363.
Mathews S. 2009. Phylogenetic relationships among seed plants: Persistent questions and the limits of molecular data. American Journal of Botany 96:228–236.
Mathews S, Clements MD, Beilstein MA. 2010. A duplicate gene rooting of seed plants and the phylogenetic position of flowering plants. Philosophical Transactions of the Royal Society B 365:383–395.
Pott C, Fischer T, Ashauer B. 2017. Lunzia austriaca – a bennettitalean microsporangiate structure with Cycadopites-like in situ pollen from the Carnian (Upper Triassic) of Lunz, Austria. Grana 56:321–338. https://doi.org/10.1080/00173134.2017.1282010
Renner SS, Grimm GW, Kapli P, Denk T. 2016. Species relationships and divergence times in beeches: New insights from the inclusion of 53 young and old fossils in a birth-death clock model. Philosophical Transactions of the Royal Society B DOI:10.1098/rstb.2015.0135
Ronquist F, Klopfstein S, Vilhelmsen L, Schulmeister S, Murray DL, Rasnitsyn AP. 2012. A total-evidence approach to dating with fossils, applied to the early radiation of the hymenoptera. Systematic Biology 61:973–999.
Rothwell GW, Crepet WL, Stockey RA. 2009. Is the anthophyte hypothesis alive and well? New evidence from the reproductive structures of Bennettitales. American Journal of Botany 96:296–322.
Rothwell GW, Nixon K. 2006. How does the inclusion of fossil data change our conclusions about the phylogenetic history of the euphyllophytes? International Journal of Plant Sciences 167:737–749.
Rothwell GW, Stockey RA. 2016. Phylogenetic diversification of Early Cretaceous seed plants: The compound seed cone of Doylea tetrahedrasperma. American Journal of Botany 103:923–937.
Sauquet H, von Balthazar M, Schönenberger J. 2017. The ancestral flower of angiosperms and its early diversification. Nature Communications 8, article no. 16047. https://www.nature.com/articles/ncomms16047
Soltis DE, Smith SA, Cellinese N, Wurdack KJ, Tank DC, Brockington SF, Refulio-Rodriguez NF, Walker JB, Moore MJ, Carlsward BS, Bell CD, Latvis M, Crawley S, Black C, Diouf D, Xi Z, Rushworth CA, Gitzendanner MA, Sytsma KJ, Qiu YL, Hilu KW, Davis CC, Sanderson MJ, Beaman RS, Olmstead RG, Judd WS, Donoghue MJ, Soltis PS. 2011. Angiosperm phylogeny: 17 genes, 640 taxa. American Journal of Botany 98:704–730.
Stevens PF. 2001 onwards. Angiosperm Phylogeny Website. Version 8, June 2007 [and more or less continuously updated since]. Available at http://www.mobot.org/MOBOT/research/APweb/ (accessed 18/12/2017).
Wang X. 2017. A biased, misleading review on early angiosperms. Natural Science 9:399–405. https://doi.org/10.4236/ns.2017.912037
Footnotes (background info, can be politically incorrect or completely harmless)Info to non-scientists: Nature is THE journal to publish something dealing with organisms, and the flagship publication of Springer-Nature, one of the globally leading science publishers; even for veteran Nature authors it has become quite difficult to get a paper into Nature, so Nature launched a still growing number of spin-offs, to give Nature authors or prospective future Nature authors a dissemination platform for papers rejected by Nature. The brand name ensures a certain fame; for instance, if you published something in Nature Whatever, the PR-department of your university will get an info directly from Nature publishing team and contact you. If you publish the same in a non-Nature offspring, you usually have to go to them. Go back to section
 The problem palaeobotanists face when describing new taxa is that they are supposed to make a diagnosis that fulfil the requirements of the Botanical Code. On the other hand, it is the rule that any fossil beyond a certain age, gets its own genus, and not rarely the genus diagnosis is identical to that of the new described species. So even similar fossils will get new generic epithets, or the authors have to emend the genus (which can be very tricky). Another complication is that each fossil lacks certain features, including one of the few synapomorphies. But may be indistinguishable from already described taxa. In extreme cases, the seeds and pollen found in-situ in a flower will have different generic names, and each organ will become a new species. A few palaeobotanists follow common sense, when it looks the same, give it the same name, but when you do so there is a high likelihood that the anonymous reviewer will try to shoot down your paper. Which is the reason (beyond simple sloppiness) that diagnosis and description can differ in detail. Furthermore, in the few case morphological matrices have been used to place fossils, you usually will have to generalise further, adding superficial inconsistencies (like some that Wang points out regarding Monetianthus). Go back to section
 Magallón et al. (2015) aim at identifying rates shifts within the angiosperm tree. To do so they use a “meta-calibrated” dated tree, effectively a fully constrained tree. Relying only on generally excepted fossils (a lot from Friis et al. 2011) but also the Triassic “angiosperm-like” pollen as minimum age for the angiosperm root, the infer an Early Cretaceous crown-age for the angiosperms. Go back to section
 The Horsemen of the Apocalypse also include, according to very reliable sources (see T Pratchett, N Gaiman, Good Omens), one woman. Go back to section
 Palaeontology is probably the softest of all natural sciences. A lot is interpretation, but it also depends a lot on skills and experience that cannot be quantified and are difficult to bring around. For instance, an experienced palynologist will recognise certain pollen grains on sight, but to describe them in a way that a reader can reproduce the identification can be very difficult. The same applies to mesofossils described by the Horsemen. When you worked with a fossil group, you notice important feats nearly subconsciously (human pattern recognition capacity is still not matched by computers). But since opinions are very important and the peer-review is confidential, it can be very harsh in palaeobotany. You don’t fuck with prominent people, but they can fuck you as much as they want. On various occasions in my career people like and including Herendeen (in case of my first phylogenetic paper; Denk et al. 2002) tried to kill off our papers during review. The editors, usually also palaeobotanists (it’s a niche science), cannot afford to make enemies, and – as author – you only have hints who it was this time (confidentiality). Since the review process is confidential, there is no way to say how many innovative ideas have been killed off during peer-review. Go back to section
 An interesting little story to tell (a look behind the thick curtain of confidential peer-review). The paper, well-done from my perspective, was submitted to Nature and fits the journal’s needs: the imaging methodology and the fossil is spectacular, the authors are leading in their various fields, and, not surprisingly, the paper has been already cited more than 150 times, including dental medicine papers. One of the reviews, however, anonymous of course but likely from one of the sworn-enemies (scientifically) of the authors (Crepet, Nixon, Rothwell), allow me to call them the ‘Hellish Triumvirate of Palaeobotany’ (see e.g. Rothwell et al. 2009; Crepet & Stevenson 2010; and N. Gaiman, Sandman Vol. 1, for who-is the Hellish Triumvirate), did not belief the Horsemen’s interpretation unless they would provide an explicit phylogenetic reconstruction supporting their assessment. Which, from my humble perspective, wasn’t needed at all and stupid to ask for; but Einem geschenkten Gaul schaut man nicht ins Maul (German saying). Probably hoping the Horsemen wouldn’t be able to do it – the Triumvirate considers themselves (still) experts in “cladistics”, and the only ones in palaeobotany. So, Horseman #2 asked one of her trusted colleagues to do it (at the time the only palaeobotanist with properly done molecular-phylogenetic papers), who recommended me. I did a full phylogenetic analysis of the available data (largely heretic from the viewpoint of the Hellish Triumvirate and Horseman #1, no idea what #4 really thought about it, he’s 90% a politician/10% a scientist – in stark contrast to all other major protagonists, who are full-blooded scientists with a lot of expertise and knowledge in their respective focus areas). Very little of what I did sipped into the main-text, most ended up in the supplement, and the rest in the bin. Because the reconstruction that was the most honest, most revealing, and most innovative (first-timer, and liked by Horseman #2) was considered by Horseman #4 to be too risky to even put into the supplement. He was afraid the Hellish reviewer may then be able to kill the paper, which, in hind-sight, would have been a great loss for keeping up Nature’s high (and inflated, personal opinion) impact factor; and – much more importantly – I probably would not had gotten a four-year ‘forsass’ grant by the Swedish Research Council (so I’m still thankful to whoever the Hellish reviewer was). Go back to section
 The Soltis et al. (2011) matrix, which is quite a deal, was the end-product of more than two decades of research. Unfortunately, the authors never found it necessary to update/check the data of earlier versions of the matrix, they simply added one gene/taxon after the other. As consequence the oldest part of the matrix includes mediocre sequences, with more pseudomutations (editing/sequencing) artefacts than actual mutations confirmed by newer data. Also they never checked for additional data to fill the blank spots. So when I filtered the matrix to fit it with the morphological partition we had (Doyle & Endress 2010), I spend nearly a month with nothing else than replacing outdated data and filling the white spots, using e.g. data form the complete reference plastomes (the Amborella data has been completely exchanged) or, not rarely, data produced by the authors themselves and used in other studies. One consequence of the cleaning was that Amborella is preferred as sister of the Nympheales (it is less distinct, hence, lesser risk for ingroup-outgroup long-branch attraction) but not of all angiosperms (moves one not up; a long debate between Soltis et al. and e.g. Goremykin and co-workers (2003). Go back to section
 I promised Seraina Klopfstein (Ronquist et al. 2012) to dig out a plant total evidence matrix. So, I pruned down the Soltis et al. (2011) matrix to the taxa in the matrix of Doyle & Endress (2010), and – after heavy curation of the molecular data set (see footnote 7) – she run a total-evidence dating. The result was very interesting, we had an idea why total-evidence failed, but nothing you could publish in a wink without much more tests. See also footnote 11. Go back to section
 Back then, Horseman #2 was quite happy about it, and my explanations regarding instability of dating estimated and topology (branching artefacts, sample bias). But probably too shy to point it out to #1. After all, none of the Horsemen has notable competence regarding molecular data or phylogenetics. That is no shame, but then you should get into contact with people who have. For instance, Magallón would obviously have been a natural co-author for the Horsemen’s review, with respect to the 2015 paper. Go back to section
 For example, when reviewing papers showing e.g. 80 Ma old (or older) pollen with exactly the same form, size and sculpture than in certain modern counterparts. These pollen grains have to be named using artificial pollen taxa because they may not come from the same genus/family that produces them today. Go back to section
 Which is likely the reason, why our first total evidence dating run gave us a root age of 4.5 billion years for the angiosperm root, when no maximum age was defined (the age of the Earth is the in-built max. age cut-off of MrBayes 3). Illustrating the problem for MrBayes converging to max-possible ages using simulations would have been quite a deal (and difficult to publish), so we abandoned the project. Go back to section
 Many reviews (also in other fields of science) only have one main objective: citing your own stuff, advertise it, so people will take in the citations for their own work. And get an easy first authorship again, for a change (at a certain level, you are covered in admin etc.) Properly placed, such a review is worth dozens of actual scientific papers for the author. In contrast, well-done reviews bring up all literature and list the pros and contras to provide an overview. Which means a lot of work, and impact points for your enemies/competitors (just check how many papers by the Hellish Triumvirate are cited. Go back to section
 The according “cladistic test” by Rothwell et al. (separating the organs and optimise the position of each independently) is nonsense – any taxon in their matrix except the angiosperms (very distinct from everything else) would fail the test including clearly monophyletic ones such as the modern conifers (which their tree resolves as paraphyletic to Gnetales and angiosperms). A demonstration that they have little idea about the signal quality of their matrices, let alone the mechanics of phylogenetic reconstructions. Go back to section