Fossils, Clocks and the Origin of Angiosperms.

Figure 1.          A Plant Family Tree. A stylised tree showing the basic evolution of plants, from single celled algae to the beautiful diversity of plants we see today. The plants included, in order clockwise from 1 o’ clock, are: Green Algae; Umbrella liverwort (Marchantia berteroana); Swan-Necked Thread Moss (Mnium hornum); Spikemoss (Selaginella sp.); Fern; Cycad (Encephalartos sp.); Maidenhair Tree (Ginkgo biloba); Pine Tree (Pinus sp.); Gnetum urens; Wielandiella angustifolia; Archaefructus liaoningensis; Magnolia sp. By Julian Kiely.

Greetings All,

I hope you’re keeping well. Sorry for the long gap between posts again; it’s coming towards the end of the year at University, and the exams and deadlines are coming thick and fast at the moment so I haven’t had much time for blogging recently. However, I’ve had just enough time to get this quick blog post out. Some interesting new things have come out recently which I just had to talk about, so read on to see what’s new in the world of palaeobotany!

Palaeontology is a very broad science and thus every week tens of new and interesting papers are released, but some weeks seem to be better than others, and this last week has been one of the best in recent months, at least for me and my interests. Every day it seems we’ve had at least one, and sometimes more fascinating new papers for me to read about. We began the week with the release of Suskityrannus hazelae, a new small (and rather complete) specimen of tyrannosauroid from the early Late Cretaceous (Nesbitt et al, 2019). This was closely followed by Ambopteryx longibrachium, the second dinosaur to be discovered with a membranous wing (Wang et al, 2019)!!! We then had papers on the repeated evolution of flightlessness in rails (Hume and Martill, 2019), an ammonite in amber (yes, and actual ammonite in amber!!! Yu et al, 2019) and even a second Urvogel from Solnhofen, which is even more derived than Archaeopteryx (Rauhut, Tischlinger and Foth, 2019)!!! Even checking my inbox now, at the time of writing this, I see a new paper on some beautifully preserved pterosaur trackways (Elgh, Pieńkowski and Niedźwiedzki, 2019) which I need to check out. The last week or so has been Fantastic!

Ahh, “But where are the plants?” I hear you ask; well, last Monday (6^th May 2019) an exciting new paper was released by the journal Nature Plants, which has some interesting, yet not wholly unexpected, implications for palaeobotany. This paper was entitled “Origin of angiosperms and the puzzle of the Jurassic gap” (Li et al, 2019) and it presents a new comprehensive time-calibrated phylogeny* for angiosperms (the flowering plants). While phylogenetic and molecular clock studies are relatively common, what sets this study apart is the sheer size of it! A total of 2,882 plastomes (chloroplast genomes) were used in this study, which represented 163 species of gymnosperms (non-flowering seed plants such as conifers and cycads) and 2,351 species of angiosperms, with representatives from 85% of angiosperm families. This phylogeny was then calibrated against 62 fossils which represent the oldest reliable occurrence of their particular clade; for instance, they used a 273 million year old cycad, a 113 million year old water lily, and a Prunus which last saw the sun’s light 49.4 million years ago. The resulting phylogenetic tree was then plotted against an axis of time, and showed the relative ages of each divergence. Now, this is where it gets really interesting; the phylogeny showed that the origination of the crown-angiosperms likely occurred in the Late Triassic (Rhaetian), around 209 Ma (Mega annum or millions of years ago)!!! It is generally held that the angiosperms likely originated in the Late Jurassic, as their earliest unequivocal fossils hail from the Lower Cretaceous Jehol deposits of China (Chang et al, 2008), with definite angiosperm pollen from only slightly older deposits. However, there is now a growing body of evidence to suggest that the origin of the flowering plants lies much further back in time than what has been generally accepted.

*For those who don’t know, a phylogeny is a ‘family tree’ constructed for organisms based on certain features. In this study they have used genetics from modern plants to construct the tree (phylogenies can also use an organisms morphology to construct a tree). The time-calibrated element means that they have used the rate at which genes change, coupled with fossil evidence to estimate the ages of divergence for different clades.

Figure 2.         Well, would you look at that! A Triassic origin of angiosperms, who’da thunk it? Well, actually, a lot of people have thought of this before, so the idea’s not new, but what is new is the size of this study. It’s almost four times the size of any previous studies estimating angiosperm origins! From Li et al, 2019 (Fig. 1| Dated phylogenetic tree showing relationships among orders of angiosperms based on a maximum likelihood partitioned analysis of 82,286 bp of DNA sequence from 80 genes of 2,881 plastomes.)

Tick Tock goes the Clock

The problem of angiosperm origins has baffled scientists for over 100 years. Charles Darwin is often quoted as referring to their sudden appearance in the fossil record as “an abominable mystery”, and even today it is a topic of much discussion. The main issue with dating the origin of angiosperms lies in the disparity between the fossil and molecular data. Firstly, let us consider the molecular data: over the years many studies have been performed which attempt to put an age to the angiosperm lineage, and in general most agree upon a pre-Cretaceous origin for angiosperms. However, this seems to be the extent of their agreement, with actual estimated ages ranging from 243 Ma to 136 Ma (Zanne et al, 2014; Magallón et al, 2015). Even two of the most recent and comprehensive studies (Magallón et al, 2015 and Barba-Montoya et al, 2018) have produced vastly different estimates with no overlap in their margin of error. So as you can see, molecular clocks can be very temperamental, and their large error margin means that any estimates must be taken with a pinch of salt, especially when trying to estimate older ages (the further back in time you try to go, the larger the error bar gets).

But there is perhaps some more molecular clock evidence which does support this earlier origination time. Firstly, a bit of background: I have recently been reading an absolutely fantastic book by Christenhusz, Fay and Chase, entitled “Plants of the World, An Illustrated Encyclopaedia of Vascular Plants” (Kew Publishing, 2017), and regular readers of the blog may start to see it being reference quite regularly. Anyway, this book basically provides an overview to every currently recognised extant family of vascular plant (yes, all 451 of them!), describing their ecology, morphology, uses and also their phylogeny and evolution; as someone interested in palaeobotany this latter section is the one which I spend the most time looking at, and it has come quite apparent to me that many clades of angiosperms which appear rather modern or derived, have their origins within the Mesozoic! Piperaceae (the Pepper family) are thought to have diverged in the mid to Late Cretaceous; the crown group of Fabaceae (peas) originated 75 million years ago, and even the Caryophyllaceae (the carnation family) has a palynological record extending back to 73 Ma (around the same time that large tyrannosaurs were wondering throughout the northern hemisphere). This high diversity of Cretaceous angiosperms has been used as evidence for an earlier origination time for the clade, and it fits perfectly in with the model presented by Li et al 2019, of an early divergence and rapid Early Cretaceous diversification.

What’s set in Stone?

So what do the fossils have to say on the matter of angiosperm origins? Again, nothing much clearer than the molecular clocks; our oldest undeniable angiosperms come from the Early Cretaceous (Barremian to Aptian, about 125 Ma) Yixian Formation of Liaoning, China, and are composed of several genera from already diverse lineages. Archaefructus (Sun et al, 1998), was the first of these to be discovered, and comes from a now extinct family of primitive aquatic angiosperms (Archaefructaceae; Sun et al, 2002). Other genera, such as Hyrcantha (“Sinocarpus”; Dilcher et al, 2007) and Leefructus (Sun et al, 2011) are also known from the Yixian, in addition to several other possible angiosperms. It is clear from this assemblage that even by the Early Cretaceous a diverse array of angiosperm lineages had already evolved, and an earlier origination for angiosperms could account for this. Alternatively, it could indicate that angiosperms underwent a stage of rapid evolution soon after their origination, producing such diverse lineages in a relatively short time. As already noted, unequivocal angiosperm pollen is known from the palynological records of slightly older rocks, up to ~139 Ma (Valanginian; Li et al, 2019), but any early than this and the evidence for angiosperms is few and far between.

Figure 3.         A reconstruction of Cratosmilax jacksoni, a basal member of Smilacaceae from the Crato Formation of Brazil (Lower Cretaceous, Aptian-Albian; De Lima et al, 2014). This is yet another example of a seemingly advanced angiosperm from the Early Cretaceous. By Julian Kiely.

In recent years there have been a number of reports of Jurassic angiosperms (Liu and Wang, 2015; Han et al, 2016; Liu and Wang, 2016), but until very recently, none have stood up to scrutiny (I plan to do a fuller blog to discuss this at a later stage). There is one, however which just might represent a plant along the angiosperm lineage. Nanjinganthus dendrostyla is a ‘flower’ described from the South Xiangshan Formation of the Lower Jurassic, from 198 individual ‘flowers’, and it does, superficially at least, resemble a small (<1cm across) flower, with a large, branching organ interpreted as a style (Fu et al, 2018). Now, I’ve been a little sceptical of the interpretation of this fossil since it came out, as despite looking like a flower, it was also very reminiscent of another supposed Jurassic angiosperm called Euanthus panii (Liu and Wang, 2015), which has more recently been considered a disintegrated pine cone (Herendeen et al, 2017); thus, I was not surprised when similar claims of misidentification were made by Coiro, Doyle and Hilton, 2019 for N. dendrostyla. However, I would still say that the arguments presented for N. dendrostyla being a ‘flower’ are still more conclusive that those made against it thus far.

So, back to what this means for angiosperm origins: we have mounting molecular clock data indicating a likely Late Triassic origin for angiosperms, with fossils of very diverse angiosperm lineages from as far back as the Early Cretaceous, and now we have a likely primitive angiosperm (or in my opinion more likely a stem-angiosperm) from the Early Jurassic (~180 Ma), of an age and grade which would fit perfectly in with the timings of Li et al ’s new phylogenetic tree. It now seems that there is a substantial body of evidence to indicate a Late Triassic (or perhaps at least an Earliest Jurassic) origin for crown angiosperms, with the likely possibility of stem-angiosperms extending back slightly further into the Triassic. But this does presents some problems, most notably the apparent lack of angiosperms throughout the Jurassic.

So, Where are all our Jurassic Angiosperms?

The ‘puzzle of the Jurassic gap’ is the next problem that we encounter: if angiosperms did indeed originate in the Triassic, why is it that we lack a fossil record for them during the Jurassic? There are likely several contributing factors to this with a major one being the likely ecology of early angiosperms. There are several hypotheses about the ecology of the original angiosperms, with some suggesting small trees or shrubs, herbaceous perennials or aquatic plants (Willis and McElwain, 2014). The earliest angiosperm fossils we have are of small herbaceous or aquatic plants, which seem to support the latter two hypotheses. This could indicate that early angiosperms remained small, minor components of most ecosystems throughout the Jurassic, perhaps hanging on in riparian or other disturbed habitats, where they out-competed other plants by having a short lifespan and rapid reproduction (Candeias and Arens, 2018). While some riparian habitats can be conducive to fossil formation, in many instances small, delicate plants would likely be destroyed or would decay rapidly before preservation could occur, and in disturbed woodland habitats (such as animal trails and clearings – back then probably created by dinosaurs) the potential for preservation is almost zero. Even in an aquatic setting, the preservation potential of plants is very low (Willis and McElwain, 2014).

Another reason for their seeming non-existence is also possibly due to the incompleteness of the fossil record. The rarer an organism is and the more readily it decays, the less likely it is to enter an environment where preservation could occur (assuming that an environment conducive to preservation is even present nearby). That sediment must then survive for millions of years to then also be found by someone who is able to identify an angiosperm. This overall makes the chances of any uncommon organism being described very unlikely. It does happen though, and some deposits, for example the Daohugou beds of China, preserve a vast diversity of flora from a forested, sub-tropical lake basin environment (Na et al, 2017), and it is probably within these deposits that we are most likely to discover true Jurassic Angiosperms. Until we discover them however, it looks like we’re stuck with just molecular clocks and speculations about what, where, when and how they lived, but for the moment, I think it’s justified to imagine the occasional small, simple flower, sticking out of the foliage of the Jurassic forest understory, or poking out of the water’s surface at the edge of a small, ephemeral pond, perhaps accompanied by a couple of horsetails with a dragonfly or two dashing around.

Figure 4.         A quick and rather speculative reconstruction of Nanjinganthus dendrostyla, here depicted as a shrubby herbaceous perennial, with large inflorescences of ‘flowers’ protruding above the leaves and stems. The large number of Nanjinganthus ‘flowers’ found in association with each other, seems to indicate that there was a local abundance of them. Perhaps they were all lost from a single plant in full bloom, or perhaps there were many small plants, currently, we don’t know. By Julian Kiely.

References

Barba-Montoya, J., Dos Reis, M., Schneider, H., Donoghue, P. C. J., Yang, Z. (2018). Constraining uncertainty in the timescale of angiosperm evolution and the veracity of Cretaceous terrestrial revolution. New Phytologist, vol. 218, iss. 2, pp. 819–834, doi: 10.1111/nph.15011

Candeias, M., Arens, N. C. (2018).  Ep. 188 - On the Origin of Flowering Plants. Retrieved from  http://www.indefenseofplants.com/podcast/2018/11/25/ep-188-on-the-origin-of-flowering-plants

Chang, M. (Ed)., Chen, P., Wang, W., Wang, Y. (2008). The Jehol Fossils: The Emergence of Feathered Dinosaurs, Beaked Birds and Flowering Plants. Academic Press.

Christenhusz, M. J. M., Fay, M. F., Chase, M. W. (2017). Plants of the World, An Illustrated Encyclopaedia of Vascular Plants. Kew Publishing, Royal Botanic Gardens, Kew. 

Coiro, M., Doyle, J. A., Hilton, J. (2019). How deep is the conflict between molecular and fossil evidence on the age of angiosperms? New Phytologist, (in press), doi: doi.org/10.1111/nph.15708

De Lima, F. J., Saraiva, A. A. F., Da Silva, M. A. P., Bantim, R. A. M., Sayão, J. M. (2014). A new angiosperm from the Crato Formation (Araripe Basin, Brazil) and comments on the Early Cretaceous Monocotyledons. Annals of the Brazilian Academy of Sciences, vol. 86, iss. 4, pp. 1657-1672, doi: 10.1590/0001-3765201420140339

Dilcher, D. L., Sun, G., Ji, Q., Li, H. (2007). An early infructescence Hyrcantha decussate (comb. nov.) from the Yixian Formation in northeastern China. PNAS, vol. 104, iss. 22, pp. 9370-9374, doi: 10.1073/pnas.0703497104

Elgh, E., Pieńkowski, G., Niedźwiedzki, G. (2019). Pterosaur track assemblages from the Upper Jurassic (lower Kimmeridgian) intertidal deposits of Poland: Linking ichnites to potential trackmakers. Palaeogeography, Palaeoclimatology, Palaeoecology, (in press), doi: 10.1016/j.palaeo.2019.05.016

Fu, Q., Bienvenido Diez, J., Pole, M., García Ávila, M., Liu, Z., Chu, H., Hou, Y., Yin, P., Zhang, G., Du, K., Wang, X. (2018). An unexpected noncarpellate epigynous flower from the Jurassic of China. eLife, vol. 7, iss. 38827, pp. 1-24, doi: 10.7554/eLife.38827

Han, G., Liu, Z., Liu, X., Mao, L., Jacques, F. M. B., Wang, X. (2016). A Whole Plant Herbaceous Angiosperm from the Middle Jurassic of China. Acta Geologica Sinica, vol. 90, iss. 1, pp. 19-29

Herendeen, P. S., Marie Friis, E., Raunsgaard Pedersen, K., Crane, P. R. (2017). Palaeobotanical redux: revisiting the age of the angiosperms. Nature Plants, vol. 3, art. 17015, pp. 1-8, doi: 10.1038/nplants.2017.15

Hume, J. P., Martill, D. (2019). Repeated evolution of flightlessness in Dryolimnas rails (Aves: Rallidae) after extinction and recolonization on Aldabra. Zoological Journal of the Linnean Society, pp. 1-7, doi:  10.1093/zoolinnean/zlz018

Liu, Z., Wang, X. (2015). A perfect flower from the Jurassic of China. Historical Biology, vol. 28, iss. 5, pp. 707-719, doi: 10.1080/08912963.2015.1020423

Liu Z., Wang, X. (2016). Yuhania: a unique angiosperm from the Middle Jurassic of Inner Mongolia, China. Historical Biology, vol. 29, iss. 4, pp. 431-441, doi: 10.1080/08912963.2016.1178740

Li H., Yi, T., Gao L., Ma, P., Zhang, T., Yang, J., Gitzendanner, M. A., Fritsch, P. W., Cai, J., Luo, Y., Wang, H., van der Bank, M., Zhang, S., Wang, Q., Wang, J., Zhang, Z., Fu, C., Yang, J., Hollingsworth, P. M., Chase, M. W., Soltis, D. E., Soltis, P. S., Li, D. (2019). Origin of angiosperms and the puzzle of the Jurassic gap. Nature Plants, vol. 5, pp. 461-470, doi: 10.1038/s41477-019-0421-0

Magallón, S., Gómez-Acevedo, S., Sánchez-Reyes, L. L., Hernández- Hernández, T. (2015). A metacalibrated time-tree documents the early rise of flowering plant phylogenetic diversity. New Phytologist, vol. 207, iss. 2, pp. 437–453, doi: 10.1111/nph.13264

Na, Y., Sun, C., Wang, H., Dilcher, D. L., Li, Y., Li, T. (2017). A brief introduction to the Middle Jurassic Daohugou Flora from Inner Mongolia, China. Review of Palaeobotany and Palynology, vol. 247, pp. 53-67, doi: 10.1016/j.revpalbo.2017.08.003

Nesbitt, S. J., Denton, R. K., Loewen, M. A., Brusatte, S. L., Smith, N. D., Turner, A. H., Kirkland, J. I., McDonald, A. T., Wolfe, D. G. (2019). A mid-Cretaceous tyrannosauroid and the origin of North American end-Cretaceous dinosaur assemblages. Nature Ecology & Evolution, doi: 10.1038/s41559-019-0888-0

Rauhut, O. W. M., Tischlinger, H., Foth, C. (2019). A non-archaeopterygid avialan theropod from the Late Jurassic of southern Germany. eLife, vol. 8, iss. 43789, doi: 10.7554/eLife.43789

Sun, G., Dilcher, D. L., Zheng, S., Zhou, Z. (1998). In Search of the First Flower: A Jurassic Angiosperm, Archaefructus, from Northeast China. Science, vol. 282, iss. 5394, pp. 1692-1695, doi: 10.1126/science.282.5394.1692

Sun, G., Ji, Q., Dilcher, D. L., Zheng, S., Nixon, K. C., Wang, X. (2002). Archaefructaceae, a New Basal Angiosperm Family. Science, vol. 296, iss. 5569, pp. 899-904, doi: 10.1126/science.1069439

Sun, G., Dilcher, D. L., Wang, H., Chen, Z. (2011). A eudicot from the Early Cretaceous of China. Nature, vol. 471, pp. 625-628, doi: 10.1038/nature09811

Wang, M., O’Connor, J. K., Xu, X., Zhou, Z. (2019). A new Jurassic scansoriopterygid and the loss of membranous wings in theropod dinosaurs. Nature, vol, 569, pp. 256–259, doi: 10.1038/s41586-019-1137-z

Willis, K. J., McElwain, J. C. (2014). The Evolution of Plants (second edition). Great Clarendon Street, Oxford, OX2 6DP, United Kingdom. Oxford University Press

Yu, T., Kelly, R., Mu, L., Ross, A., Kennedy, J., Broly, P., Xia, F., Zhang, H., Wang, B., Dilcher, D. (2019). An ammonite trapped in Burmese amber. PNAS, pp. 1-6, doi:  10.1073/pnas.1821292116

Zanne, A. E., Tank, D. C., Cornwell, W. K., Eastman, J. M., Smith, S. A.,  FitzJohn, R. G. … Beaulieu, J. M. (2014). Three keys to the radiation of angiosperms into freezing enviroments. Nature, vol. 506, pp. 89–92