Introduction

Since plants colonized the land, wind dispersal (anemochory) became common with the seed wing representing a key dispersal strategy through geological history (Taylor et al., 2009; Ma, 2009; Stephen and Christian, 2019). Winged seeds evolved numerous times in many lineages of extinct and extant seed plants (spermatophytes) (Schenk, 2013; Stevenson et al., 2015). Lacking wings as integumentary outgrowths, the earliest ovules in the Famennian (372-359 million years ago [Ma], Late Devonian) rarely played a role in wind dispersal (Rowe, 1997). Furthermore, nearly all Famennian ovules are cupulate, i.e., borne in a protecting and pollinating cupule (Prestianni et al., 2013; Meyer-Berthaud et al., 2018).

Warsteinia was a Famennian ovule with four integumentary wings, but its attachment and cupule remain unknown (Rowe, 1997). Guazia was a Famennian ovule with four wings and it is terminally borne and acupulate (devoid of cupule) (Wang et al., 2022). This paper documents a new Famennian seed plant with ovule, Alasemenia tria gen. et sp. nov. It occurs in Jianchuan mine of China, where Xinhang fossil forest was discovered to comprise in situ lycopsid trees of Guangdedendron (Wang et al., 2019). The terminally borne ovules are three-winged and clearly acupulate, thus implying additional or novel functions of integument. Based on current fossil evidence and mathematical analysis, we discuss the evolution of winged seeds and compare the wind dispersal of seeds with different number of wings.

Results

Locality and stratigraphy

All fossils came from Upper Devonian Wutong Formation at Jianchuan mine in Xinhang town, Guangde City, Anhui Province, China. Details on locality are available in previous works (Wang et al., 2019; Xu et al., 2022). At this fossil locality, Wutong Formation consists of Guanshan Member with quartzose sandstone and a little mudstone, and the overlying Leigutai Member with inter-beds of quartzose sandstone, siltstone and mudstone. Spore analysis indicates that the Leigutai Member here is late Famennian in age (Gao et al., 2023). Progymnosperm Archaeopteris and lycopsid Leptophloeum occur in Leigutai and/or Guanshan members, and they were distributed worldwide in the Late Devonian (Taylor et al., 2009). Fernlike plant Xinhangia (Yang and Wang, 2022) and lycopsid Sublepidodendron (Xu et al., 2022) were found at the basal part of Leigutai Member. In situ lycopsid trees of Guangdedendron with stigmarian rooting system appear in multiple horizons of Leigutai Member and they formed the Xinhang forest (Wang et al., 2019; Gao et al., 2022). From many horizons of siltstone and mudstone of Wutong Formation (Leigutai Member) at Jianchuan mine, numerous ovules of Alasemenia were collected.

Systematic palaeontology

Division Spermatophyta

Order and family incertae sedis

Alasemenia tria gen. et sp. nov.

Etymology

The generic name from the Latin “ala” and “semen”, meaning wing and seed, respectively; the specific epithet from the Latin “tri” (three), referring to wing number of a seed.

Holotype designated here

PKUB21721a, b (part and counterpart housed in Department of Geology, Peking University, Beijing) (Fig. 1a, m, n).

Fig. 1.

Locality and horizon

Xinhang, Guangde, Anhui, China; Leigutai Member of Wutong Formation, Upper Devonian.

Diagnosis

Dichotomous branches bearing terminal and acupulate ovules. Three broad wing-like integumentary lobes radially and symmetrically attached to each nucellus, distally tapered and proximally reduced. Integumentary lobes evidently extending outwards, with their free parts ca. 40% of ovule length. Individual integumentary lobes folding inwards along abaxial side. Nucellus largely adnate to integument.

Description

Some ovules are borne terminally on smooth branches that are thrice (Fig. 1a), twice (Fig. 1c) or once (Fig. 1b, f, g, i; Fig. 2a-c) dichotomous at 40-135°. The boundary between ovule and ultimate axis below refers to position where the ovule width just begins to increase (e.g., Fig. 1a, arrow). The branches excluding ovules are up to 76 mm long and 0.4-0.9 mm wide. Most ovules terminate ultimate axis (Fig. 1j, 2d-f) or are detached (Fig. 1d, e, h, k, 2g-o). The ovules are 25.0-33.0 mm long and 3.5-5.6 mm at the maximum width (excluding the width of outward extension of integumentary wings). Compressions of ovules (Fig. 1-3) and their serial transverse sections (Fig. 4; Fig. S1-5) do not show any cupules.

Fig. 2.

Fig. 3.

Fig. 4.

Each ovule possesses a layer of integument with three radially arranged and wing-like integumentary lobes (Fig. 1a, d, e, 2d, e, o, arrows, 3a-f, 4; Fig. S1-5). They are broad, acropetally tapered and proximally reduced to merge with the ultimate axis (Fig. 1a-c, f, 2a, d-i, n). The integumentary lobes are 1.2-2.3 mm at the maximum width and free for 8.3-14.8 mm distance (32%-45% of the ovule length), and the free lobe parts extend well above the nucellar tip and greatly curve outward. Usually, two lobes of a single ovule are evident and the third one is sometimes exposed through dégagement (Fig. 1a, 2n, arrow 2, o, middle arrow, 3a, e, arrow). Such situation indicates that the lobes of an ovule are present on different bedding planes.

In transverse sections of an ovule, two integumentary lobes extend along the bedding plane, and the third lobe is either originally perpendicular to or compressed to lie somewhat along the bedding plane (Fig. 4c-e, h-k, n-r, t, w-y; Fig. S1-5). The integumentary lobes are narrow, flattened and fused in the lower part of an ovule, and acropetally become wide, thick, separated and far away (Fig. 4c-e; Fig. S1a-k, 2). Because of great outward curving of lobes, it is difficult to observe their distal parts in the sections. When thick, the lobes present a V or U shape. Therefore, they are symmetrically folded along the abaxial side and toward the ovule center.

A few ovules show the outline of a nucellus, which is ca. 10-11.7 mm long and 1.2-1.7 mm at the maximum width (Fig. 1d, 2i, arrows, j, 3f-h). Transverse sections occasionally meet the nucellar tip (Fig. 4d, arrow). With the exception of tip, the nucellus is adnate to the integument and is distally surrounded by the free parts of integumentary lobes. The ovule is reconstructed to show three integumentary wings (Fig. 5a) and nucellar tip (Fig. 5b).

Fig. 5.

Discussion

Late Devonian acupulate ovules and their functions

Except few taxa including Guazia (Wang et al., 2022), Dorinnotheca (Fairon-Demaret, 1996), Cosmosperma (Liu et al., 2017), Elkinsia (Serbet and Rothwell, 1992) and Moresnetia (Fairon-Demaret and Scheckler, 1987), the earliest ovules in the Late Devonian (Famennian) have not been preserved to be connected to the branches. These ovules are usually surrounded by cupules. Now, as in Guazia, the ovules of Alasemenia terminate the dichotomous branches and are transversely sectioned to show the ovular structures. The ovules of these two genera provide rare evidence for acupulate ovules in the earliest seed plants.

Both cupule and integument of an early ovule perform the protective and pollinating functions (Meyer-Berthaud, 2022). The integument of Alasemenia is adnate to most part of the nucellus and its three lobes extend long distance above the nucellar tip and then evidently outwards. Such structure leads to efficient protection of nucellus and adaptation for pollination. In early seed plants, the fertile branches terminated by cupulate ovules consistently lack leaves and thus the cupules probably serve a nutritive function as in photosynthetic organs; this function may be transferred to the integuments of acupulate ovules such as Guazia (Meyer-Berthaud, 2022). Regarding Alasemenia, the nutritive function would also apply to the integuments since the acupulate ovules are terminal on various orders of naked branches and ultimate axes. The surface of integuments is enlarged through the outgrowths of wings and thus promotes the photosynthesis. Little is known about the dispersal function of Famennian ovules, because the integumentary wings as a derived character have been rarely documented. Warsteinia (Rowe, 1997), Guazia (Wang et al., 2022) and now Alasemenia indicate that the anemochory originated in the Famennian. However, the ovule of Warsteinia remains unclear in attachment to branches and possession of a cupule. Alasemenia confirms that, like Guazia, the integuments of acupulate ovules developed a new function in wind dispersal.

Late Devonian winged ovules and evolution of ovular wings

In the Late Devonian ovules, besides Alasemenia, both Warsteinia (Rowe, 1997) and Guazia (Wang et al., 2022) possess integumentary lobes forming radially arranged wings. Their integumentary wings illustrate diversity in number (three or four per ovule), length, folding or flattening, and being straight or curving distally. As in Alasemenia (Fig. 5a), the integumentary wings of acupulate ovule of Guazia are broad, thin and fold inwards along the abaxial side, but their numbers are four in each ovule and their free portions usually arch centripetally (Fig. 5c; Wang et al., 2022, Figure 5). In contrast to Alasemenia, Warsteinia has four integumentary wings without folding and their free portions are short and straight (Rowe, 1997, TEXT-FIG. 4). Ovules of Alasemenia and Guazia terminating long and narrow branches suggest easy abscission of diaspores (ovules with or without an ultimate axis) and better preparation for dispersal. Compared to Warsteinia with short and straight wings and Guazia with long but distally inwards curving wings, Alasemenia with longer and outwards extending wings would efficiently reduce the rate of descent and be more capably moved by wind. Furthermore, the quantitative analysis in mathematics indicates that three-winged ovules such as Alasemenia are more adapted to wind dispersal than four-winged ovules including Warsteinia and Guazia (see following).

Alasemenia, Guazia and Warsteinia suggest that the evolutionarily novel wings, as integument outgrowths and the most important mechanism for seed dispersal by wind, appeared early in the spermatophytes and had been manifested in younger lineages. Other wind dispersal mechanisms including plumes, pappi and parachutes of seeds appeared later in the Permo-Carboniferous and Mesozoic, respectively (Axsmith et al., 2013). Current evidence indicates that seeds with three or four wings occurred first in the Late Devonian. They were followed by two- or three-winged seeds in the Carboniferous (Long, 1960, 1969), and then by single-winged seeds in the Permian (Stevenson et al., 2015; Prevec et al., 2008). Relating to wind dispersal, the diaspores (seeds/fruits) of living spermatophytes possess multiple mechanisms and variable number of wings (Ma, 2009).

Mathematical analysis of wind dispersal of ovules with 1-4 wings

The rate of diaspore descent in still air is an important indicator of the potential ability of modern samaras dispersal (Augspurger et al., 2016, 2017). In examining samaras, it has been demonstrated that the value of angular velocity is smaller than that of terminal velocity (Green, 1980), and the relationship between the samaras’ wing loading and terminal velocity v_ter is:

where w is the weight of samaras, A_W is the surface area of the wing, w/A_W is defined as the samaras’ wing loading.

As for ovules, we also use terminal velocity as an indicator of dispersal ability. Since the broad integumentary wings well extend outwards, the wing loading of Alasemenia is obviously less than that of Guazia. When the winged seeds fall in the air, the predictable spinning can lead to the reduction of fall rate, and result in the increase of the horizontal dispersal distance. This has been observed in the field experiments or proved in the modelling reconstruction experiments (Green, 1980; Habgood et al., 1998).

However, the tiny asymmetry of ovules will be amplified in the running geometry by centrifugal and aerodynamic loads, result in vibrations and thus significantly reduce the efficiency (Lu et al., 2019). The transverse wave caused by vibrations will arrive the tip of wing and form stationary waves. In the ovules with even number of wings like Guazia (Wang et al., 2022) and Warsteinia (Rowe, 1992, 1997), the center symmetry structure will lead to stronger resonance than the ovules with odd number of wings (like Alasemenia). It means the ovules with odd number of wings are more stable in high rate spinning and spend more falling time in the dispersal process.

Another consideration is the capacity of airflow in horizontal direction. The Reynolds number (Re) is the indicator of patterns in fluid flow situations, and for ovules, the Reynolds numbers are mainly fall in 10³-10⁴, suggesting that the inertia forces are much stronger than viscous forces (Burrows, 1975; Seter and Rosen, 1992). In this situation, the thrust of airflow can be represented as:

where c is the coefficient, ρ is the density of air, S is the windward face, v is the velocity of relative movement.

It means that we can transform the comparison of capacity of airflow into the area of windward. Supposing the maximum windward area of each wing is S_wing and n represents the number of wings revolving on its own axis, we define a function S(θ) to represent the area of windward when the angle between airflow and wings is θ. We introduce relative efficiency E_r for comparison. Here we list the following 5 ideal basic situations and the summary results are shown in Fig. 6.

Fig. 6.

1. n = 2 and the wings keep facing the wind (wings without rotation, as a control group). In this situation, the area of windward is identical to 2S_wing, which can be written as:

We define a function D(θ) to represent the accumulated area of windward in a cycle. By definition,

2. n = 2. In this situation, we discuss the condition when θ ∈ [0, π].

Based on symmetry,

3. n = 1. In this situation,

As can be seen in Fig. 6, the relative efficiency is equal to the situation of n = 2,

4. n = 3 (Alasemenia).

Based on symmetry,

5. n = 4 (Guazia, Warsteinia).

When θ ∈ [π/4, π/2],

Based on symmetry,

Generally, the above one- to four-winged seeds are quantitatively analysed for their wind dispersal capability and the results are shown in Fig. 6. The relative efficiency for wind dispersal (E_r) of these seeds in five ideal basic situations is calculated for comparison. The one- or two-winged seeds are treated as a control group when the wings keep facing the wind and do not rotate. In this case, the value of E_r is 100%. When descending through autorotation, one-to four-winged seeds present different values of E_r. The relative wind dispersal efficiency of three-winged seeds is obviously better than that of single- and two-winged seeds, and is close to that of four-winged seeds (Fig. 6). In addition, three-winged seeds have the most stable area of windward, which also ensures the motion stability in wind dispersal. Significantly, the maximum windward area of each wing of Alasemenia is greater than that of Guazia and Warsteinia with four wings. All these factors suggest that Alasemenia is well adapted for anemochory.

Conclusion

The earliest ovules in the Famennian of Late Devonian, usually preserved to be unconnected with branches, are mostly devoid of integumentary wings and enclosed in cupules; they are thus insufficiently known for integument function and wind dispersal. New ovule Alasemenia in this paper terminates leafless branches, bears three wings and lacks cupules. It represents the second acupulate ovule in the Famennian. Besides protective and pollinating functions, Alasemenia suggests photosynthetically nutritive and anemophilous functions of early ovules. It indicates the diversity of Famennian winged ovules and the evolutionary sequence of ovule wings. Compared to Famennian four-winged ovules of Warsteinia and Guazia, Alasemenia with three distally outwards extending wings shows advantage in anemochory. Mathematical analysis implies that three-winged ovules could be efficiently dispersed by wind.

Methods

All specimens are housed in Department of Geology, Peking University, Beijing, China. Steel needles were used to expose some seeds and fertile axes. Serial dégagement was employed to reveal the morphology and structure of seeds. Seeds were embedded in resin, sectioned and ground to show the integuments and nucelli. All photographs were made with a digital camera and microscope.

Acknowledgements

We thank X. Gao, Z. Z. Deng and L. Liu for help in fieldwork. Q. Y. Jia and D. B. Ni provide assistance in the experiment for seed sections. This work was supported by the National Natural Science Foundation of China (grant no. 42130201).

Author Contributions

D.W., L.L. and M.Q. conceived the research. All authors collected the fossils. D.W. and J.Y. conducted the observations and photography of specimens. Y.Z., P.X. and P.H. made mathematical analysis and prepared some figures. D.W. wrote the manuscript, with discussion and contributions from other authors.

Competing interests

The authors declare no competing interests.