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W2967492605 abstract "The question of whether any angiosperms existed before the Cretaceous period is of key importance for understanding seed-plant evolution. Most authorities suggest that the earliest unequivocal microfossil and macrofossil records of flowering plants date from the Early Cretaceous (reviewed by Herendeen et al., 2017; Coiro et al., 2019). However, recent indirect evidence from molecular dating analyses suggests that angiosperms began to diversify into living clades (the crown group) before this time, during the Jurassic, Triassic or even Permian (Foster et al., 2017; Salomo et al., 2017; Barba-Montoya et al., 2018). The latest detailed molecular study dated the origin of the crown angiosperms to the Late Triassic (Li et al., 2019). It is therefore unsurprising that the range of claims for pre-Cretaceous, especially Jurassic, angiosperm fossils has accelerated in recent years. Several Jurassic fossils from China have been described and attributed to angiosperms, including Euanthus, Juraherba, Nanjinganthus, Solaranthus, Yuhania and Xingxueanthus (Wang et al., 2007; Wang, 2010, 2018; Wang & Wang, 2010; Zheng & Wang, 2010; Han et al., 2016; Liu & Wang, 2016, 2017; Fu et al., 2018). The taxonomic attribution of these potentially pivotal fossils has been widely discussed and often directly criticized (Herendeen et al., 2017; Coiro et al., 2019). Here, we comment on one such discovery in particular – the recently described compression fossil Nanjinganthus from the Early Jurassic of China (Fu et al., 2018), which has attracted considerable attention in the literature (Taylor & Li, 2018; Coiro et al., 2019; Rümpler & Theißen, 2019). We present new arguments that support a non-angiosperm interpretation of this fossil, thus further contradicting the original interpretation. Nanjinganthus resembles another Jurassic fossil from China, Euanthus, described in an earlier paper (Liu & Wang, 2016). Both fossils were described by the original authors as pentamerous flowers (sometimes tetramerous in Nanjinganthus) with a double perianth, a unilocular ovary that is inferior (Nanjinganthus) or semi-inferior (Euanthus), and a long style that is branched (Nanjinganthus) or unbranched (Euanthus) (Liu & Wang, 2016; Fu et al., 2018). Herendeen et al. (2017) disagreed with a floral interpretation for Euanthus and plausibly interpreted the fossil as a fragmentary ovuliferous conifer cone. Noting the similarity of the ‘sepals’ and ‘petals’ of Liu & Wang's (2016) fossil to the lowermost and successive ovuliferous scales of a conifer cone, respectively, they proposed that the naked axis of a fragmentary cone corresponds in shape and size to the structure interpreted by Liu & Wang (2016) as a style. According to Herendeen et al. (2017), the structures interpreted by Liu & Wang (2016) as receptacle, ovary and ovule correspond with the minute non-ovuliferous scales and the detachment scar of a partially decomposed cone. Collections of the newer fossil, Nanjinganthus, are relatively abundant (264 specimens comprising 198 ‘flowers’: Fu et al., 2018). Despite earlier criticism of Euanthus, Fu et al. (2018) interpreted similar structures of Nanjinganthus as sepals and petals and described the perianth as either pentamerous or tetramerous. As highlighted by Fu et al. (2018, p. 16), ‘the radial arrangement of two whorls of foliar parts (sepals and petals) in Nanjinganthus is very similar to those of flowers in extant angiosperms.’ Furthermore, the authors noted that the fossil demonstrates a certain resemblance to species of Pentapetalae, or core eudicots. These ideas were further developed by Taylor & Li (2018), who described the perianth of Nanjinganthus as whorled; more precisely, as consisting of a whorl of sepals plus a whorl of petals. According to the diagram provided by Taylor & Li (2018), the petals regularly alternate with the sepals. They listed the supposed floral characters of Nanjinganthus and compared them with various reconstructions of the ancestral angiosperm flower, notably those of Endress & Doyle (2009) and Sauquet et al. (2017). They then calculated and compared the proportions of the ancestral angiosperm character states proposed by various authors that can be found in the fossil. This approach to identification, and the apparently angiospermous nature of Nanjinganthus, were highlighted in a commentary by Rümpler & Theißen (2019). By contrast, Coiro et al. (2019) did not accept the evidence for placement of Nanjinganthus within angiosperms and instead suggested its interpretation as a male or female conifer cone. There is obscure morphology in the crucial part of the fossil that was described by Fu et al. (2018) as an inferior ovary enclosing one to three ovules, the ambiguity reflecting poor preservation and irregularity in the number and appearance of the supposed ovules. We agree with Coiro et al. that, in the absence of unequivocal microsporangia and ovules, it is at best premature to interpret Nanjinganthus as a member of the angiosperm clade. In contrast with Euanthus, material of Nanjinganthus offers an opportunity for more detailed morphological analyses. Several figures in Fu et al. (2018) show compressions of ‘flowers’ viewed from below. These fossils are particularly useful for identification of the pattern of phyllotaxis of the organs that were originally interpreted as sepals and petals. We discuss the most informative images provided by Fu et al. (2018), focusing on the question of whether organ arrangement in Nanjinganthus can be interpreted as whorled or spiral, which represent the two fundamental categories of phyllotaxis. We contend that this aspect of organ patterning represents a feature of this controversial fossil that merits careful analysis. Ten ‘perianth’ organs are clearly discernible in Fu et al.'s (2018) Fig. 2C (our Fig. 1a). The authors interpreted five of these organs as sepals and five as petals. The five ‘sepals’ differ in size and can be arranged from the smallest to the largest along a putative spiral. The spiral can then be continued into the inner organs (described as ‘petals’). The last ‘sepal’ (organ 5 in our numbering) and the first ‘petal’ (organ 6 in our numbering) are remarkably similar to each other in shape, size and texture. Most importantly, organ 6 lies on almost the same radius as organ 1. None of the subsequent ‘petals’ (i.e. organs 7–10) lie exactly between the two adjacent ‘sepals’, as would be expected in a whorled system (e.g. Endress, 2006), but rather are shifted towards one of them. Note that organs 7–10 (in contrast with organ 6) appear to be slightly displaced during fossilization, but their attachment positions are located even closer to the radii of the ‘sepals’. For example, organ 10 (a ‘petal’) is clearly inserted in front of organ 5 but its tip is displaced towards organ 2 (a ‘sepal’). These organs 5 and 10, however, do not lie on the same radius, as organ 10 has a much narrower base. Table 1(a) summarizes the inferred angles between successive organs in the putative spiral of phyllotaxis. These angles show considerable variation. Comparable levels of angle variation (c. ± 20°) have been recorded in quantitative studies of floral phyllotaxis in spiral flowers of some species of Laurales, though most other species possessed more uniform angles (Staedler et al., 2007; Staedler & Endress, 2009). The average divergence angle in the fossil ‘flower’ (Fig. 1a) is 141.6°, a figure that lies midway between the Fibonacci spiral angle (137.5°) and the divergence angle in a 2/5 spiral (144.0°). However, if the angles between organs 1–5 are not taken into account and only the angles between organs 5–10 are considered, the revised average divergence angle in the fossil ‘flower’ (Fig. 1a) is 137.8°, which deviates by only 0.3° from the Fibonacci angle. These results closely approach those of Staedler et al. (2007) and Staedler & Endress (2009), where the observed deviations from the Fibonacci angle were strong among the outermost floral organs but then rapidly decreased toward the apex. These comparisons by no means imply that Nanjinganthus is a spiral flower related to the magnoliids studied by Staedler et al. (2007) and Staedler & Endress (2009). Instead, we believe that the similarity is related to general aspects of divergence angle variation in systems characterized by spiral phyllotaxis. Table 1(b) shows the angles between the organs of the same fossil (Fig. 1a) inserted on the adjacent radii; that is, between the adjacent organs interpreted by Fu et al. (2018) as sepals and petals. According to the whorled model (with five sepals and five petals), the angle separating adjacent organs (i.e. a petal and a sepal) should consistently approximate 36°. However, our measurements reveal strong deviations from this ideal angle (Table 1b). The ‘flower’ shown in Fu et al.'s (2018) Fig. 2D (our Fig. 1b) shows an architecture that was interpreted by the authors as four ‘sepals’ and four ‘petals’. Our organ numbering makes the arrangement of these organs comparable with that shown in our Fig. 1(a) (though the putative spiral is anticlockwise in Fig. 1a and clockwise in Fig. 1b). There is no obvious organ occupying position 8, though there is a piece of tissue that could represent its remnant (Fig. 1b). Note that there is a ‘petal’ (6) situated precisely on the radius of the smallest ‘sepal’ (1), exactly as in the other compression fossil discussed earlier. ‘Petal’ 5 has a broad base and represents a form that is transitional in size and shape between ‘sepal’ 4 and ‘petal’ 6. ‘Petals’ 7 and 9 are by no means inserted between two sepals; instead, they appear to be arranged in front of ‘sepals’ 2 and 4, though not on the same radii as the ‘sepals’. The relative arrangement of organs 2 + 7 and 4 + 9 is extremely similar in the two ‘flowers’ under discussion (Fig. 1a,b), with the difference that the two fossils mirror each other due to the opposite directions (chiralities) of their respective phyllotactic spirals. The ‘flower’ shown in Fig. 4D of Fu et al. (2018) is labeled by the authors as having three ‘sepals’ and five ‘petals’. It is less well-preserved than the two compressions discussed earlier, and it is entirely possible that some of the outermost organs have been lost. Nevertheless, the arrangement of one of the ‘petals’ exactly on the radius of a ‘sepal’ is unequivocal. There are petals located in front of two other well-recognizable ‘sepals’, both displaced from the sepal radii in the same way as organs 7–9 in our Fig. 1(a). A ‘petal’ lying on a ‘sepal’ radius is also clearly visible in Fig. 6L of Fu et al. (2018). Fu et al.'s (2018) Fig. 2G shows a structure that they interpreted as a ‘flower bud’ in lateral view with five ‘perianth organs’ visible: two large ‘sepals’, a small ‘sepal’ and three ‘petals’. Again, one of the ‘petals’ lies on the same radius as the small ‘sepal’. To summarize, our observations show that the organs interpreted by Fu et al. (2018) as sepals and petals do not form two isomerous and alternating whorls in the same way as the sepals and petals of core eudicots (Pentapetalae). None of the images provided by Fu et al. (2018) support the diagrammatic reconstruction by Taylor & Li (2018) that shows five petals alternating with five sepals. One could speculate in extremis that the observed phyllotaxis found in Nanjinganthus represents five petals each occurring on a sepal radius. Admittedly, a similar condition has been reported in the peculiar and morphologically isolated basal eudicot family Sabiaceae (e.g. Ronse De Craene et al., 2015), though we note that interpretation of the Sabiaceae perianth as spiral or whorled remains unresolved (cf Sauquet et al., 2018; Sokoloff et al., 2018). In this context, we highlight two important concerns. First, in Nanjinganthus, apparently only one ‘petal’ is inserted exactly on a ‘sepal’ radius. In our view, it is far more plausible to consider ‘perianth’ organ arrangement as spiral in Nanjinganthus. Second, as already highlighted by Coiro et al. (2019, Supplementary Information), the morphological differences between the ‘sepals’ and ‘petals’ are less well-defined than was proposed in the original description (they are certainly not as well-defined as in Sabiaceae). Indeed, the strong morphological similarity between organ 5 (the last ‘sepal’) and organ 6 (the first ‘petal’) clearly suggests a gradual transition in organ morphology along the spiral of phyllotaxis. After having re-interpreted the phyllotaxis of Nanjinganthus, we venture a brief remark on ‘pentamery’ in Euanthus. Euanthus was described on the basis of a single compression specimen, the holotype, which is preserved as part and counterpart (Liu & Wang, 2016). It was interpreted as a pentamerous ‘flower’ with a double perianth, but only two ‘sepals’ and three ‘petals’ are visible. The notion of pentamery was inferred from the pentagonal shape of the receptacle. The authors reported an angle of about 110º between adjacent sides of the pentagonal receptacle (Liu & Wang, 2016), which is close to the angle of 108º between the sides of a regular pentagon. In our view, only two corners of the ‘pentagon’ are clearly visible in the illustrations provided by Liu & Wang (2016; especially their Fig. 4D); one corner does indeed approximate 110º but according to our measurements the other approximates 127º. The outline of the ‘pentagon’ provided in Fig. 7G of Liu & Wang (2016) is far from regular. Therefore, evidence for pentamery of Euanthus is unconvincing. Although surprisingly not explicitly stated as such in the core literature, pentamery is as much an angiosperm-specific character as tricolpate pollen. Both features occur primarily in eudicots – indeed, tricolpate pollen that follows Fischer's rule of development has apparently evolved only once in angiosperms and is exclusively found in eudicots (Furness & Rudall, 2004; but see comments below on Schisandraceae). With respect to phyllotaxis, both spiral and whorled types are found in different groups of gymnosperms, including their reproductive structures. However, whorled types contain relatively few elements per whorl; to our knowledge, whorls with more than four elements occur only in the cotyledonary node of Pinaceae (with merism often higher than 5) and in cones of some Bennettitales such as Weltrichia (Popa, 2019), though in both cases uncertain organ homologies merit further attention. In conifers, cones with whorled bracts are dimerous or trimerous (e.g. Rothwell & Basinger, 1979; Schulz et al., 2003) and vegetative leaf whorls, when present, are dimerous or trimerous. A report of leaf arrangement in whorls of four in Papuacedrus (Cupressaceae; e.g. Hill & Carpenter, 1989) is not convincing as the entire shoot has only four orthostichies, and the so-called whorls should instead be viewed as pairs of closely spaced nodes with decussate phyllotaxis. Leaves are mostly decussate in Gnetales, though whorls of three and even four leaves (and bracts) occur in some species of Ephedra (e.g. Chamberlain, 1935). In the absence of unequivocal dithecal anthers and clearly documented fully enclosed ovules, the reported (but here disputed) presence of a double perianth with 4–5 regularly alternating sepals and petals would have represented one of the most important arguments in favour of an angiosperm identity for Nanjinganthus. Having disproved the claim for pentamery, we agree with additional arguments put forward by Coiro et al. (2019) that Nanjinganthus is most unlikely to have been an angiosperm. In this context, it is reasonable to revisit the suggestion of Taylor & Li (2018) that Nanjinganthus possesses the characteristics of the earliest angiosperms as summarized by Bateman et al. (2006). In doing so, Taylor & Li ignored not only the subtleties of the discussion in Bateman et al. (2006) but also their clear warning of the dangers of exclusively employing ‘top-down’ thinking constrained by extant morphologies. We remain unconvinced by interpretations of several important characters of Nanjinganthus as portrayed by Taylor & Li (2018). Apart from their imaginative interpretation of the perianth, as critiqued earlier, we can find no evidence supporting inferred features such as carpel number more than one, carpel phyllotaxis whorled, carpel size variation absent, extragynoecial compitum absent, or placentation dorsal/laminar. All the characters listed earlier require recognition of carpels and their boundaries. Notably, Fu et al. (2018), in their original publication, emphasized the absence of conventional carpels in Nanjinganthus. Most extant angiosperms with inferior ovaries possess more than one carpel, though in some cases only one is fertile (Kedrov, 1969; Sokoloff, 2015, but see Endress & Lorence, 2004). Therefore, if one accepts the occurrence of an inferior ovary in Nanjinganthus (evidence for which is in our view insufficient), it is tempting to anticipate that the gynoecium will be syncarpous with more than one carpel. Unfortunately, Taylor & Li (2018, p. 2) did not explain which approaches they used to infer boundaries between the carpels and to estimate the occurrence of ‘five fused carpels (which could be four)’. The apparently spiral phyllotaxis of Nanjinganthus could be used for its further taxonomic identification. Conifer genera differ from each other in spiral vs whorled arrangement of the sterile scales surrounding the microsporophylls and spiral vs whorled arrangement of the scales of the female cones, so those with spiral phyllotaxis merit particular attention in future comparisons with Nanjinganthus. Fu et al. (2018) noted similarities of Nanjinganthus with male cones of some conifers, such as Thuja, Sequoia, Taxus and Tsuga (as described by Schulz et al., 2014). Although Fu et al. (2018) ultimately rejected an interpretation of Nanjinganthus as a male cone, Coiro et al. (2019) considered it to be a plausible hypothesis. In our view, the identity of Nanjinganthus should lie among either male or female conifer cones. The morphological similarity between the scales (‘sepals’ and ‘petals’) of Euanthus and Nanjinganthus (e.g. the presence of multiple parallel longitudinal vein-like strips) suggests that the two fossils belong to the same major taxonomic group. We agree with Coiro et al. (2019) and Herendeen et al. (2017) that the interpretation of stamens and ovules is not convincing in Euanthus whereas the similarity between Euanthus and a fragmentary female cone of Tsuga (Herendeen et al., 2017) is considerable. The phyllotaxis of Euanthus and Nanjinganthus was almost certainly spiral rather than whorled, and followed the Fibonacci pattern, at least in Nanjinganthus. In our view, the importance of the discovery of these fossils (and the confusion perennially surrounding them) is that they highlight the need for comprehensive analysis of the evolution of phyllotaxis in reproductive structures across the seed plants, both living and fossil (see also Sokoloff et al., 2018). A major problem in the search for a consensus between the contradictory molecular divergence dates and the fossil record is the absence of reliable pre-Cretaceous fossils belonging to the crown-group angiosperms (Coiro et al., 2019). Indeed, what is actually inferred from the molecular dating analyses is the age of the crown-group angiosperms. The fossils that potentially belong to the stem-group cannot shed light on this problem. Precise identification of fossils belonging to the crown-group can be made using morphological cladistic analyses (Doyle & Endress, 2010, 2014, 2018). A related approach is a search for fossils possessing certain character states that appeared during the course of crown-group evolution, such as tricolpate pollen (Coiro et al., 2019) and stable pentamery. Stable pentamery involving regular alternation of whorls is almost entirely restricted to the major eudicot clade named Pentapetalae (e.g. Soltis et al., 2003; Ronse De Craene, 2010, 2016; Sauquet et al., 2017). It is also known in another eudicot lineage, Ranunculaceae (Ranunculales), where it is present in Aquilegia and some other Thalictroideae (Tucker & Hodges, 2005; Ren et al., 2011). In general, whorled pentamerous flowers are uncommon in Ranunculaceae (Schöffel, 1932). Among magnoliids, stable pentamery with two alternating perianth whorls is known in Illigera (Hernandiaceae, Laurales), where it occurs in the context of the meristic variation from three to eight in the entire family (Kubitzki, 1993; outer perianth whorls sometimes dimerous, Endress & Lorence, 2004). Another magnoliid showing an interesting parallel with Pentapetalae is Warburgia (Canellaceae, Canellales), where the flowers consistently possess three sepals, 5 + 5 petals, 5 + 5 stamens and 5 carpels. The quincuncial arrangement of the outer-whorl petals and the contort (though questionably stable – not reported for any magnoliid by Endress, 2012) arrangement of the inner-whorl petals in Warburgia (Wilson, 1966) strongly resemble those of sepals and petals of some core eudicots. The only difference from a typical pentamerous flower is the occurrence of three ‘true’ sepals in Warburgia. In the context of Pentapetalae, one would interpret these three phyllomes as an epicalyx, but they are homologous with the sepals of all other Canellaceae, including Canella, where the three sepals and the five petals give an impression of being arranged in a continuous spiral sequence (Wilson, 1966). Pentamery with a two-whorled perianth can be found as an unstable condition in a few monocot groups with exceptionally high overall meristic variation; for example, in some species of Paris (Melanthiaceae, Liliales) and Aspidistra (Asparagaceae, Asparagales). Outside the eudicots, stable occurrence of a whorled perianth with five sepals alternating with five petals (in Illigera) seems to be as rare as records of tricolpate pollen outside the eudicots (in the ‘ANA grade’ family Schisandraceae). The colpi of tricolpate species of Schisandraceae s.l. are offset from the colpi of most eudicots by 60º (Garside's rule; though this will not be visible in dispersed fossil pollen), like the arms of a polar trichotomosulcus, and the three apertural branches are indeed united at the distal pole in some members of the family (Doyle et al., 1990; see also Doyle & Endress, 2000). Curiously, pollen of some other members of Schisandraceae possess three distally fused colpi alternating with three short free colpi (reviewed by Doyle et al., 1990; Saunders, 2000), the latter thus positionally corresponding with the typical eudicot colpi arranged according to Fischer's rule (Furness & Rudall, 2004). Both characters (pollen apertures and phyllotaxis) are free from the inevitable ambiguity of inferring homologies of the flower and its parts. The character ‘pentamery’ can best be defined as ‘the stable occurrence of regularly alternating pentamerous whorls in reproductive structures’, thus being in theory fully applicable to non-angiosperms. However, in practice, stable pentamery is not recorded in the vegetative or reproductive organs of any Jurassic seed plants or post-Jurassic gymnosperms. Furthermore, the absence of stable pentamery is probably also characteristic of earlier seed-plant groups, especially when leaf/sporophyll arrangement is considered. The striking rarity of species consistently characterized by a two-whorled pentamerous perianth outside the eudicot clade suggests that this condition is far from trivial in terms of regulation of the underlying developmental processes and evolutionary origins (see also Specht & Bartlett, 2009; Ronse De Craene et al., 2015; Sauquet et al., 2017; Sokoloff et al., 2018). The occurrence of various meristic figures higher than four in several groups of non-eudicot angiosperms (and in Bennettitales) indicates the absence of a direct constraint against pentamery. However, whorls with more than four organs typically occur in androecia and/or gynoecia (e.g. Ronse De Craene, 2010; Endress, 2014), and the outermost organs of the perianth of the same flowers often do not form polymerous whorls. For example, the gynoecium of Nymphaeaceae is single-whorled and typically polymerous, whereas the outermost perianth whorl is either trimerous or tetramerous in the same flowers (Endress, 2001). The pentamerous corolla of some Canellaceae occurs together with a trimerous calyx. In their schematic outline of early angiosperm diversification, Herendeen et al. (2017) misleadingly illustrated the basal angiosperm grade using a floral diagram of the nymphaealean fossil flower Monetianthus with a two-whorled pentamerous perianth. Their diagram of Monetianthus (see also Friis et al., 2011) does not fit the original data on organ arrangement in Monetianthus presented by Friis et al. (2009), in which one of the 10 scars of the apparent perianth members is located at a lower level than the other scars and, more importantly, is inserted on almost the same radius as another perianth member. Friis et al. (2009) noted difficulties in describing the floral phyllotaxis of Monetianthus as either spiral or whorled. Doyle & Endress (2014) interpreted the phyllotaxis of Monetianthus as irregular. Given the potential evolutionary importance of this fossil, its exceptional three-dimensional preservation and the availability of X-ray microtomography data, it is important to deduce its precise floral diagram. It is unlikely that the Jurassic fossils Euanthus and Nanjinganthus are interpreted correctly as angiosperm flowers and it is clear that the original publications did not provide convincing evidence for the occurrence of a whorled, pentamerous perianth divisible into distinct sepals and petals. It appears that in reproductive structures outside the eudicots, with very few exceptions, whorls with merism higher than four are developmentally unstable and merism of polymerous whorls is not precisely fixed. Encouragingly, the existence of a model plant (Aquilegia; Kramer, 2009), belonging to one of very few lineages where stable pentamery evolved independently of Pentapetalae (Ronse De Craene et al., 2003), should allow us to make insightful comparisons with the iconic pentamerous model Antirrhinum. The core eudicots somehow ‘managed’ to maintain a developmental programme for precise and stable patterning of as many as five organs per whorl (and sometimes more, mostly borne in even numbers; Ronse De Craene, 2016), whereas non-angiosperm seed-plant groups can only deal with the ‘simpler’ tasks of ensuring stable dimery, trimery and rarely tetramery. This insight highlights an open question for developmental genetics and developmental morphology: how the eudicots have learned to slice a pie into five carefully arranged pieces. The work of DDS, MVR and ESE is supported by FRBR grant no. 18-04-00797. The authors thank James Doyle, Susana Magallón and Louis Ronse De Craene for suggestions that improved the manuscript. DDS and MVR conceived and wrote the initial draft. ESE made measurements. DDS, MVR, ESE, PJR and RMB contributed to writing and revising the manuscript." @default.
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W2967492605 title "Supposed Jurassic angiosperms lack pentamery, an important angiosperm‐specific feature" @default.
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W2967492605 doi "https://doi.org/10.1111/nph.15974" @default.
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