Where Did Flowers Come From?

Are angiosperms 135 million years old, or 275 million years old?

We live among a hodgepodge of plants from different evolutionary epochs, with flowering plants being the most recent, (including the even more recently evolved grasses), alongside the more ancient conifers, cycads, ferns, mosses, and lichens. All have a place in diverse ecosystems, but what is their true history? This has been difficult to establish in more than broad outlines, due, as usual, to the patchy nature of the fossil record, and the difficulties of aligning it with what we now have as the molecular record. Angiosperms have been a particular sore spot, ever since Darwin, who recognized that the sudden appearance and radiation of flowering plants, roughly 130 million years ago, was a problem for evolutionary theory.

A paper from a few years back offered a carefully aligned molecular and fossil analysis of angiosperms, coming to the conclusion that they actually originated ~275 million years ago (MYA), and must have persisted in some cryptic fashion through the ensuing 150 MY before making a splash in the fossil record. How is this kind of analysis done? First, the best early fossils are tabulated, with secure dating and clear characteristics that include them among angiosperms. The most ancient example is a sample of pollen, from roughly 125 million years, which looks strongly like it came from angiosperms. These fossils are also assigned to plant lineages, so that their appearance can inform the branching points of the phylogenetic diagram, whether that diagram is based purely on these fossils and their morphology, or based on molecular data.

Then a set of gene sequences is collected, which are conserved between all the surveyed species, and aligned so that their changes can be fed into a program that counts all the differences. It was clear through this work that some lineages changed faster than other ones (the faster ones are marked with blue flares towards the right. Since the sampled species are all ones that exist now (time 0), being able to provide DNA, and since the branch points are in any case shared between the lineages that descend from them(at their origination points), faster change / evolution in one lineage vs another will be readily apparent, and the researchers just have to make up some rules to judge where to come down in time assignments when faced with such discrepancies. The more serious problem is that such different speeds can totally derange this kind of analysis, making a faster-changing lineage seem much older than it is. So pinpointing the branch points between lineages is extremely important to pin down such hard-to gauge branch lengths. 

Biologically, it is now well known that lineages vary substantially (up to ten fold, less so in longer lineages and time spans) in their speed of molecular change.. molecular evolution is not a clock. Faster change tends to happen when populations are small, and when big evolutionary transitions have happened. For example, plants, and specifically angiosperms, have gone through whole-genome duplications that represent major evolutionary watersheds. These duplications supplied raw material for countless diversifications and specializations of genes, with especially rapid change in molecular sequences either released from previous selective constraints, or subject to new ones via new roles.

Integrated phylogenetic diagram of the evolution of angiosperms, marking key fossils that inform branch point timing (lettered blue circles), and ranges of possible branch points derived from the molecular alignments (red circles). At bottom is time, in millions of years before present.

What can explain the big gap in estimated angiosperm origins? There are three basic hypotheses. First is that the molecular data is correct, which implies that there is an extremely long (150 million years) history of cryptic angiosperms that have not (yet) been detected in the fossil record. There are smatterings of findings in the literature that suggest that such fossils may be (or may have been) found, but I don't think these have been widely accepted yet (especially when they come from highly questionable sources).

The second hypothesis is that something about the very early evolution of angiosperms (like the very early evolution of eukaryotes, and the very early diversification of macroscopic animals) was accelerated in molecular terms, (as discussed above in terms of differing rates between lineages), rendering the apparent molecular phylogeny much longer than the real one. That includes the prodigious radiation of the many lineages in the diagram above, all before the first fossil is found.

The third hypothesis, much beloved of creationists, is that god did it. A mystery like this is ripe for invoking the solution to all mysteries, which is it does not need to be explained in the normal mechanistic terms of the natural world, but rather can be chalked up to the author of all things, god. While this hypothesis, at least for believers, solves this one nagging mystery, it brings on a few others. Why does the rest of biology through this vast lineage still follow the plodding path of gradual (if uneven) development? Why jump in to create this mystery when so many other lineages in the fossil record do not present similar mysteries? Why did god insist upon, (presumably for the ultimate appearance of us as humans), the whole four billion year process of life's plodding development, when the whole thing could have been authored at once and at the start? What amazing societies we could have developed with a four billion year head start!

It is clear, therefore, that some hypotheses create more problems than they solve. Inviting scientists to consider and comment on harebrained hypotheses is not going to end well. The solution to this problem is going to be some combination of the first two hypotheses, of rapid molecular evolution at the start of a major radiation, and some as-yet missing material in the fossil record. Innovative organisms are very likely to be rare, though whole cryptic lineages surviving for many tens of millions of years is hard to posit without more evidence. Yet it is also a given that fossils will necessarily appear after the actual events of lineage branching, thus will always post-date the calculated molecular branching point.

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