* Katherine Valde is an assistant professor of philosophy at Wofford College. She is interested in time in the biological sciences, as well as the role the concept of “neutrality" plays in science and beyond. [Note: the above image is the Cretaceous section of Zallinger’s The Age of Reptiles (1947), showing Tyrannosaurus and friends loitering among some— in hindsight, too modern-looking— angiosperms.] Katherine writes…
In a letter to his friend and colleague J.D. Hooker, Charles Darwin described the sudden appearance and diversification of angiosperms (flowering plants) as “an abominable mystery” (Davies et al. 2004). In the almost 150 years since Darwin’s remark, scientists have sought to resolve the so-called mystery to no avail. Given the central importance of peer disagreement in science, we might imagine this field of inquiry to have been exceedingly fruitful. Helen De Cruz and Johan De Smedt (2013), for example, claim that peer disagreements are productive insofar as they (1) generate new evidence, (2) lead to the re-evaluation of existing evidence and assumptions, and (3) serve as an antidote to confirmation bias. While I’m sympathetic to De Cruz and De Smedt’s view on the virtues of disagreement, I believe a close examination of the disagreement(s) over angiosperm origins shows their analysis to be overly optimistic. In what follows, I will argue that while the scientific debate over angiosperm origins fulfills De Cruz and De Smedt’s criteria, it remains possible to regard it as far from an ideally productive disagreement.
Charles Darwin (seated, right), Joseph Hooker (seated, left) and Extinct fave Charles Lyell (standing), in Darwin’s study
The Cretaceous Terrestrial Revolution (KTR) is one of the most significant events in the history of life on earth. During the KTR, also called the “Angiosperm Terrestrial Revolution,” a massive diversification of flora and fauna took place (Benton et al., 2021). By the end of the KTR almost all crown lineages of angiosperms had evolved (Benton et al., 2021). Some authors argue that the rise of angiosperms drove the macroecological revolution that occurred on land – the diversification of angiosperms caused terrestrial organisms to change evolutionary trajectories, providing an opportunity for much evolutionary innovation (Benton et al. 2021). The co-evolution of pollinators and angiosperms, in particular, was a key dynamic in the evolution of the modern biosphere.
Historically, dating the origins of angiosperms has been the domain of paleobotanists whose expertise is the fossil record. Read literally, the fossil record tells a story about how angiosperms rose to ecological dominance, leading to the diversification of birds, insects, mammals, and seed-free land plants. As this version of the story goes, the fossil record accurately records the emergence and rapid diversification of angiosperms. Many scientists have and continue to believe that there was in fact an explosive radiation of the angiosperm clade in the early Cretaceous (van der Kooi & Ollerton 2020).
More recently, however, molecular dating methods have expanded the group of scientists who are interested in dating the origin of angiosperms. These methods have deepened the mystery as they regularly date the appearance of angiosperm to the late Triassic, around 209 Ma (van der Kooi and Ollerton 2020). Many molecular biologists believe the late appearance of angiosperms in the fossil record is either evidence of the incompleteness of the fossil record or of mistakes in reading the “text.” Thus, to all appearances we have a large gap or disagreement between the fossil and “molecular clock” evidence. Some researchers (Li et al. 2019) have even given this gap a name, “the Jurassic gap,” after the fact that the different origin dates seem to skip over the entire Jurassic Period.
In the past three decades, a great number of molecular dating analyses, based on the divergence of DNA sequences of living plants, have supported a pre-Cretaceous origin of crown-group angiosperms— that is, the ancestors of all living angiosperms. Magallón et al. (2015) compiled results from 43 molecular clock studies, almost all of which show substantially older molecular dates when compared to the oldest fossils that have been found.
Molecular and fossil-based estimates of angiosperm age. Blue bars indicate the stratigraphic interval from which the oldest fossil belonging to angiosperm orders and major clades is known.The name of the order or major clade is shown next to each bar. Red dots and bars indicate the age and/or range of angiosperm crown age estimated in molecular clock studies. The numbers next to each red bar or dot correspond to estimates in published analyses indicated in Magallón et al. (2015)
As the above figure dramatically illustrates, the Jurassic gap is pronounced, and has been demonstrated by a wide variety of researchers for basically every order within the angiosperm clade (Magallón et al., 2015). What’s more, the Jurassic gap has persisted even as molecular dating techniques have improved. For example, Li, et. al. (2019) used gene sequences from 2881 chloroplast genomes belonging to species from 85% of extant flowering-plant families, time-calibrated using 62 fossils, to date the origin of angiosperms to the late Triassic (>200 Ma). Li, et. al. were able to corroborate much of the conventional phylogeny of the angiosperm clade, which many take to be a positive indicator of the reliability of their methods. Beyond the headline late Triassic date, Li et. al’s work suggests that major radiations occurred in the Late Jurassic and Early Cretaceous (approximately 165 to 100Ma), again much earlier than the fossil record suggests. This is important given the presumed central role of angiosperms in the KTR. If many angiosperms were present much earlier, another explanation would be needed for the rapid rise to dominance of the angiosperm clade during the KTR.
While it is very unlikely that the first angiosperm fossil actually represents the first angiosperm on earth, many who play close attention to this gap remain skeptical of explanations that take the main issues to be the notorious incompleteness of the fossil record. Consider pollen, which is an extremely important type of fossil evidence in discussions of angiosperm origins. Unlike botanical megafossils (leaves or flowers), pollen fossils are both well distributed and well preserved in the fossil record. Within the lower Cretaceous, angiosperm megafossils only appear near the Barremian-Aptian boundary (ca. 125 Ma) in two or three locations (Coiro et al. 2019). By contrast, there is an extensive pre-Aptian age pollen record of angiosperms distributed all over the world (Coiro et al. 2019).
The idea that there was an explosive radiation of angiosperms is also supported by the appearance of tricolpate pollen (see the figure, below) in the early Cretaceous followed by an explosive increase in variety of fossils in the middle and late Cretaceous (Coiro et al. 2019). Researchers Mario Coiro, James Doyle, and Jason Hilton have conducted an extensive review of the known fossil record in 2019 and argue that there are two pieces of evidence supporting this hypothesis. First, there are many sites with good pollen fossil preservation before the Cretaceous, and researchers have looked extensively for angiosperm fossils at these sites. So far they have failed to turn up any angiosperm pollen at any of these sites (Coiro et al. 2019). Second, and more important, when we do see definitive angiosperm pollen in the record, and the diversification of that pollen, these events occur in a precise order. Groups within the angiosperm clade appear in the same sequence in different location around the globe, and this order in which they appear is the same order predicted by molecular analyses of the phylogenetic relationship among these groups (Coiro et al. 2019).
Monosculcate pollen with a single germinal furrow, and tricolpate pollen with three germinal furrows. Image credit: Coiro et al. (2019)
As one might expect given the attention Darwin paid to the issue of Angiosperm origins, combined with the contemporary ecological dominance of angiosperms, the search for angiosperm fossils has been extensive. Tricolpate pollen is taken by some to be the first definitive record of angiosperms in the fossil record and appears in the late Barremian (ca. 125 Ma). Approximately 72% of living angiosperms are members of the eudicot clade, which molecular evidence strongly suggests is monophyletic. Tricolpate pollen is usually taken as evidence of the existence of this clade, which later went on to evolve derived forms of pollen structure (Coiro et al., 2019). Still, other angiosperms have a simpler monosulcate pollen. In fact, the simpler monosulcate pollen structure is believed to be the ancestral form of the more complex tricolpate pollen (Coiro et al. 2019, Barba-Montoya et al. 2018). Despite claims of the discovery of pre-Cretaceous angiosperm fossils, a careful analysis of the specimens suggests that these interpretations result from “misunderstandings of the basic plant morphology” (Coiro et al. 2019, 95).
Absence of evidence is not usually considered evidence of absence, so some might suggest that the absence of pre-Cretaceous angiosperms should not be taken as evidence of the absence of such taxa. However, in this case it would be curious if angiosperms were missing from the extensive pollen fossil record (which records the presence of many close relatives of angiosperms) if angiosperm were, in fact, present. The point here is that there is an extensive fossil record and basic agreement about the timing and order of that record. While there have been claims of the discovery of a pre-Cretaceous fossils there have been no definitive attributions despite over 150 years of careful searching.
There's more. Not only do tricolpate pollen follow monosulcate pollen in the fossil record, but the further diversification of tricolpate pollens into derived pollen types is consistent with the evolutionary transformations proposed by early paleobotanists and confirmed by molecular analyses (Coiro et al. 2019). This “stratigraphic succession” is seen repeatedly at different sites all over the globe and for various groups within the angiosperm clade. As Coiro et al. argue, “Congruence between inferred pollen evolution and stratigraphy is expected only if there was a relatively short lag between evolution of successively more derived types and their appearances in the fossil record” (90). If this were not the case, we would have to explain why plants were waiting around for millions of years before appearing in the fossil record in a precise order. The increased improbability of such coincident preservation failures causes some researchers to argue that the fossil record has more-or-less accurately preserved the origins of angiosperms.
Montsechia vidalii, an early flowering plant from the Cretaceous (ca. 125 Ma)
This view of angiosperm origins has been termed the “short-fuse” hypothesis because the suggestion is that angiosperms diversified fairly quickly after their initial appearance. This view seems to suggest that it is our molecular clock estimates that are wrong rather than the fossil record. Perhaps given the complexities of molecular clock models and their sensitivity to calibration practices, there is reason to doubt the results of these analyses.
Unfortunately, molecular clock researchers are confident that this is not the case. While molecular clock experts readily admit that their estimates are not precise, and can only provide ranges of high probability for the emergence of angiosperms, many are confident that they can reject a post-Jurassic emergence for angiosperms (e.g. Barba-Montoya et al. 2018, Li et al. 2019). These researchers instead suspect the “long-fuse” hypothesis is correct— they believe that crown group angiosperms evolved in the Jurassic or earlier, leaving little or poorly understood fossil evidence during this interval. For example, Barba-Montoya et al. used cutting edge Bayesian approaches to try to account for uncertainties surrounding both calibration-point date estimates and evolutionary rates across groups. While they confirm the general Cretaceous Terrestrial Revolution assertion of a rapid Cretaceous diversification of angiosperms, their results “only reinforced” the “enduring controversies between paleontological and molecular biological approaches to establishing evolutionary timescales” (831).
* * *
Max Planck is often (slightly mis-) quoted as saying that science progresses “one funeral at a time.”* This is usually taken to be a criticism of stubborn senior scientists, who would rather persist in error than change their minds. However, in the wake of the pluralist turn in the philosophy of science, diversity of opinion has come to be understood as a key to healthy science. In fact, epistemic peer disagreement is often seen as a driver of successful scientific research. In recent years various philosophers have analyzed this situation; and yet it is still challenging to understand what to make of the dispute over angiosperm origins.
[* What Planck actually said was: “A new scientific truth does not triumph by convincing its opponents and making them see the light, but rather because its opponents eventually die and a new generation grows up familiar with it” (Planck 1949, 33).]
Basically, it seems that researchers are at an impasse, and that no evidence is forthcoming that will settle the debate in a way that satisfies all parties. Not only are there no “smoking guns” (Cleland 2002), but it also seems implausible to expect that one will materialize or be “manufactured” (Currie 2018). Both streams of available evidence are highly incomplete, and most of our ways for dealing with their incompleteness increase their interdependence (reducing their value as independent lines of evidence). As Derek Turner argues, historical science often finds itself in a situation of “local underdetermination” (Turner 2005), and the present debate seems like a good example of this. One might think of the debate over angiosperm origins, then, as an example of fruitless disagreement, where decades of research and innovation have brought no resolution to the debate, and it seems likely that (barring significant technological innovation) no “tie-breaking” evidence is coming over the horizon.
However, just as Turner’s suggestion that we would never know the color of dinosaurs didn’t survive the test of time, we should not rush to a pessimistic conclusion about the future of the present debate (Turner 2016). We should also consider that the concept of “fruitfulness” is a broad one, not limited to progress on the focal question (settling the timing of angiosperm origins/diversification). For example, if we examine the three ways De Cruz and De Smedt (2013) argue that peer disagreements are advantageous (generating new evidence, leading to the re-evaluation of existing evidence and assumptions, and serving as an antidote to confirmation bias), it is clear that the angiosperm disagreement has fulfilled all three. So maybe it has been a fruitful debate, in some sense, even if it shows no signs of impending resolution.
Reconstruction of flowers that bloomed 113 million years ago in Brazil. Credit: Mark P. Witton
Yet I am hesitant to declare a victory for optimists in the angiosperm origin debate, either. It is not merely the fact that researchers are at an impasse that generates pessimism. The way they are engaged in the debate also makes it seem less than robustly productive. If we look closely at some of the exchanges that I have discussed, we find many examples of researchers talking past one another. For example, Coiro, Doyle, and Hilton assert that “Most molecular studies have not addressed these conflicts directly, but recently Barba-Montoya et al. (2018) argued that they reflect deep flaws in interpretation of the fossil record” (84). However, a close inspection of Barba-Montoya et al. reveals that they do not argue for the falseness of the fossil record. Instead, they conclude that “In large part, the discrepancy between these approaches is an artefact of false precision on both sides” (831). In this case, and others like it, researchers disagree, but not in a way that reflects a deep and thoughtful engagement (of the sort that we might expect to pay epistemic dividends).
We can detect a similar superficiality in the frequent references to Darwin’s remarks in the literature. Even in the contemporary literature, many papers on the origin of angiosperms open with a reference to Darwin’s “abominable mystery” (e.g. Coiro et al. 2019; van der Kooi and Ollerton 2020; Sauquet, et al. 2022; Silvestro et al. 2021). Yet our contemporary mystery is not analogous to Darwin’s. Darwin’s mystery concerned the apparently rapid diversification of angiosperms, which was problematic in light of his strong preference for evolutionary gradualism (Friedman 2009). While Darwin did acknowledge the possibility of rapid emergence and diversification of angiosperms, he additionally speculated that there might be, to quote Friedman’s analysis, a “long, gradual, and undiscovered pre-Cretaceous history of flowering plants on a lost island or continent” (5). Many, if not most, of the authors who invoke Darwin’s name today take for granted that there was a rapid diversification of angiosperms in the Cretaceous. The abominable mysteries these modern authors refer to are varied, but are rarely the same mystery Darwin had in mind.
Not all disagreements are created equal. Some foster productivity and novel scientific discoveries, while others leave us comparatively dissatisfied. Simplistic optimism about the benefits of genuine epistemic peer disagreement is a bad idea, as is simplistic pessimism. Looking carefully at productive disagreements has yielded important insights about epistemic goods that come in unexpected forms (e.g. methodological refinements, the utilization of different streams of evidence, etc.). Yet too little attention has been paid to cases where disagreements fail to yield these benefits. The angiosperm debate has something important to tell us about the nature of disagreement in science. After all, if angiosperms cannot teach us about when something will bear fruit, what can?
References
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