Xin Wang

State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology and Center for Excellence in Life and Paleoenvironment, Chinese Academy of Sciences, Nanjing 210008, China

1. Introduction

Angiosperms are the most important group of plants in the current earth ecosystem. However, little is known about the origin of angiosperms, which has been a headache for many botanists. The core question in the origin of angiosperms is the homology of carpels. Formerly, Arber EAN and Parkin J(1907) speculated that the carpels in angiosperms were derived from the former megasporophylls bearing ovules along their margins. Consequently, conduplicate carpels bearing ovules on their adaxial (ventral) margins (as in Magnoliaceae) were taken as the most ancestral among angiosperms (Canright JE, 1960; Cronquist A, 1988). This hypothesis remained unsupported by fossil evidence untilArchaeanthuswas published by Dilcher DL and Crane PR(1984). Such support was later reinforced by the so-called“First Flower”Archaefructus(Sun G et al., 1998, 2002),which was also assumed to have “conduplicate” carpels.However, more careful research indicate thatArchaefructushas no “conduplicate” carpels (namely, its ovules are inserted along the dorsal margin of the fruits) (Ji Q et al., 2004; Wang X and Zheng XT, 2012), casting doubt over the validity of Arber and Parkin’s hypothesis. This doubt grows greater as the APG’s basalmost angiosperm,Amborella, has ascidiate rather than conduplicate carpels (Buzgo M et al., 2004). The situation prompts the author to double-check the ovule insertion inArchaeanthus. The outcome is crucial in botany,as it is hinged with the ultimate fate of the hypothesis of Arber and Parkin that has been influencing almost all leading systematic botanists for more than a century. To ascertain the ovule insertion inArchaeanthus, the author re-examined the type materials ofArchaeanthus, and compared the author’s observation with the previous one.

2. Methods

Specimens were photographed with a Sony ILCE-1 digital camera. Details of the specimens were observed and photographed under a Nikon SMZ-10 stereomicroscope equipped with a Canon EOS Rebel XSi digital camera. All photographs were saved in JPEG format and organized for publication using Photoshop 7.0.

3. Results

The observation focuses on only one character ofArchaeanthus, namely, the ovule/seed insertion in the fruits.Therefore other aspects ofArchaeanthuswill not be discussed since Dilcher DL and Crane PR (1984) have documented them well. To clearly demonstrate the ovule insertion of the fossil, one infructescence ofArchaeanthusis shown in Figs.1a, b, with the apex pointing to the top. Enlarging from the infructescence in Fig. 1a, one of the fruits is shown in Fig. 1c.The adaxial margin of the fruit is oriented to the upper, and the abaxial margin to the lower. There are several seeds/ovules in this fruit (Figs. 1c, g). Two seeds/ovules are clearly inserted along the abaxial margin and isolated from the adaxial margin (Figs. 1c, d) while three distal seeds/ovules in the same fruit are inserted along both the adaxial and abaxial margins, respectively (Figs. 1g, 2). In the meantime,ovules/seeds in another fruit of the same infructescence are inserted along the adaxial margin (Figs. 1b, e). Each fruit has a stern stalk (Figs. 1f, 2).

Fig. 1. Infructescence, fruits, and in situ seeds/ovules of Archaeanthus linnenbergeri. a-an infructescence. IU15703-2300′. Bar = 5 mm. b-the counterpart of the infructescence is shown in Fig. 1a. IU15703-2300′. Bar = 5 mm. c-detailed view of the fruit arrowed in Fig. 1a. Note the in situ seeds/ovules (arrows) and their spatial relationship relative to the adaxial (AD) and abaxial (AB) margins of the fruit. Bar = 1 mm. d-detailed view of the two seeds/ovules (within the left rectangle in Fig. 1c). Note the organic attachment of seeds/ovules (bottom arrows) to the abaxial margin (AB) of the fruit and the gap (between the two top arrows) between the seeds/ovules and adaxial margin. Bar = 0.5 mm.e-adaxial insertion of a row of seeds/ovules inside the fruit marked by the arrow in Fig. 1b. Note the adaxial margin (AD) of the fruit and the smooth outlines of the in situ seeds/ovules. Bar = 1 mm. f-a stern fruit stalk. IU15703-2318′. Bar = 5 mm. g-detailed view of the three seeds/ovules (within the right rectangle in Fig. 1c). Note one of the seeds/ovules (1) close to the abaxial margin (AB) and the other two (2, 3) attached to the adaxial margin (AD) in the same fruit. Bar = 0.5 mm.

Fig. 2. Sketch of an Archaeanthus linnenbergeri fruit showing the seed (SE)/ovule(OV) insertion along both ventral/adaxial (AD) and dorsal/abaxial (AB) margins of the fruit.

4. Discussions

The above observation is apparently at odds with the interpretation of Dilcher DL and Crane PR (1984), in which the ovules/seeds were interpreted as inserted uniformly along the “adaxial suture” (page 351, 363, 364, 371). Can this discrepancy be due to observing different specimens ofArchaeanthuslinnenbergeri? Such a possibility can be ruled out completely, as the author’s (Figs. 1c, d) and previous observation (Fig. 24 of Dilcher DL and Crane PR, 1984) were performed on exactly the same specimen (IU15703-2300 ′).Examining Fig. 24 [one of the only two figures showing seed/ovule attachment in Dilcher DL and Crane PR (1984)],one can easily find that the seeds/ovules are indeed inserted along the “abaxial” margin of the fruit and anotherin situseed(marked as h in their figure) appears to be inserted to the abaxial (rather than adaxial) margin of the fruit. The whole fruit/carpel and seeds/ovules within appear intact and there is no evidence of displacing or twisting during the fossilization.Instead, there is evidence of a stern fruit stalk (Fig. 1f; Fig. 20 of Dilcher DL and Crane PR, 1984), which appears not to allow fruit twisting inArchaeanthus. The author prefers to believe that preservation ofArchaeanthusis faithful and believable. Otherwise, if it were taken as an artifact, all interpretations about seed/ovule attachment in Dilcher DL and Crane PR (1984) as well as in the present paper would become groundless and therefore spurious.

It is clear that the seeds/ovules are not inserted only along the adaxial suture inArchaeanthus, as claimed by Dilcher DL and Crane PR (1984). Instead, the seeds/ovules inArchaeanthusappear to more likely be inserted either along the abaxial, adaxial, or both margins of the fruits (Figs. 1c-e,g). This information rules out a magnoliaceous affinity forArchaeanthusclaimed by Dilcher DL and Crane PR (1984) as well as Romanov MS and Dilcher DL (2013) since all seeds/ovules in Magnoliaceae are inserted along the adaxial fruit margin (Canright JE, 1960). The presence of an elongated fruit stalk inArchaeanthus(Fig. 1f; Fig. 20 of Dilcher DL and Crane PR, 1984) further alienatesArchaeanthusfrom Magnoliaceae, in which all fruits are sessile and have no obvious stalks. It is noteworthy thatNeofructus, a fossil from the Early Cretaceous Yixian Formation, demonstrates clearly that, at least in some of its fruits, the seeds/ovules are inserted along both the adaxial and abaxial margins of the fruits, which also, interestingly, has elongated fruit stalks (Liu ZJ and Wang X, 2018), suggesting that the carpels inArchaeanthusandNeofructusmight be derived similarly.

It is noteworthy that, like inArchaeanthus(Dilcher DL and Crane PR, 1984), the carpels inArchaefructus liaoningensis(Sun G et al., 1998) used to be similarly misinterpreted as “conduplicate”, implying adaxial seed/ovule insertion in the fruits. This error has been corrected twice (Ji Q et al., 2004; Wang X and Zheng XT, 2012). Although“surprising” to many botanists who grew up with Arber and Parkin’s hypothesis, such corrections are rather expected if recent progress in botany is taken into consideration: A typical carpel in Magnoliaceae actually is a composite organ derived from a former ovule-bearing branch plus a subtending foliar part (Zhang X et al., 2017; Wang X, 2018; Wang X et al., 2020), rather than is a “megasporophyll”, which has been proven non-existing among known seed plants (Wang X and Luo B, 2013; Miao Y et al., 2017). Therefore the hypothesis of Arber EAN and Parkin J (1907) becomes spurious, and all concerned conclusions hinged with this hypothesis in angiosperm systematics in the past century become vulnerable to suspicions. This disillusion actually should have happened earlier since, as early as in 1925, Parkin J admitted that their 1907 speculation had no fossil support. Apparently, the proponents of Arber and Parkin’s speculation were preferentially blind to this confession and warning. Dilcher and Crane’s misinterpretation about seed/ovule insertion inArchaeanthusandArchaefructusmore or less reflect their preference of conformity in botany. Not surprising, several“theoretically correct ” claims of seed/ovule vascular connection in Magnoliaceae (Canright JE, 1960), bitegmic ovules inMonetianthus(Friis EM et al., 2009), free carpels inKajanthus(Mendes MM et al., 2014), and gratuitous and perplexing interpretations of carpel orientations in the Fabaceae (Wang X et al., 2021) were very likely due to similar peer pressure. Consequentially, the lack of a solution for the origin of angiosperms is a rather expected aftermath of Arber and Parkin’s speculation.

5. Conclusion

Archaeanthusis a famous Cretaceous angiosperm from the Albian-Cenomanian of Kansas, the USA documented by Dilcher and Crane in 1984. Its seeds/ovules were interpreted as arranged along the adaxial (ventral) suture of the fruits.This interpretation used to sound plausible, especially under the light of the then-dominating doctrine of angiosperm evolution. However, Dilcher and Crane’s interpretation of seed/ovule insertion was not fully supported even by their own evidence. Considering the early age, importance, and influence ofArchaeanthusin palaeobotany and angiosperm systematics, it is necessary to ascertain the seed/ovule position inArchaeanthus. New observation on the type materials ofArchaeanthusindicates that at least some ovules/seeds inArchaeanthusare attached to the abaxial (dorsal) margin of the fruit. This information undermines the former assumed Magnoliaceous affinity ofArchaeanthusand falsifies its support to the then-dominating speculation of carpel homology and origin of angiosperms. Analysis of the common reason underlying the misinterpretations of early fossil angiosperms (includingArchaeanthus,Archaefructus,and others) indicates that the speculation of Arber and Parkin deviated much from the botanical reality.

CRediT authorship contribution statement

Xin Wang designed the research plan, collected and interpreted the data, wrote and finalized the manuscript.

Declaration of competing interest

The author declares no conflict of interest.

Acknowledgment

The author thanks Dr. Steven Manchester and Dr. Hongshan Wang for the access to the valuable type specimens ofArchaeanthus linnenbergerideposited in the Florida Museum of Natural History. This research was supported by the Strategic Priority Research Program (B) of the Chinese Academy of Sciences (XDB26000000), and the National Natural Science Foundation of China (41688103, 91514302).The author appreciates two anonymous reviewers for their suggestions and help, which have helped to improve this paper.