Alasemenia , the earliest ovule with three wings and without cupule

The ovules or seeds (fertilized ovules) with wings are widespread and especially important for wind dispersal. However, the earliest ovules in the Famennian of the Late Devonian are rarely known about the dispersal syndrome and usually surrounded by a cupule. From Xinhang, Anhui, China, we report a new taxon of Famennian ovules, Alasemenia tria gen. et sp. nov. Each ovule possesses three integumentary wings evidently extending outwards, folding inwards along abaxial side and enclosing most part of nucellus. The ovule is borne terminally on smooth dichotomous branches and lacks a cupule. Alasemenia suggests that the integuments of the earliest ovules without a cupule evolved functions in wind dispersal and probable photosynthetic nutrition. It indicates that the seed wing originated earlier than other wind dispersal mechanisms such as seed plume and pappus, and that three-or four-winged seeds were followed by seeds with less wings. Mathematical analysis shows that three-winged seeds are more adapted to wind dispersal than seeds with one, two or four wings under the same condition.

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.

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).

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.
Each ovule possesses a layer of integument with three radially arranged and winglike integumentary lobes (Fig. 1a,d,e,2d,e,o,arrows,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 1.2-2.3mm at the maximum width and free for 8.3-14.8mm 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 dé gagement (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,.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.

Comparison of winged ovules and record of acupulate ovules in Devonian
In Devonian ovules, besides Alasemenia, both Guazia (Wang et al., 2022) and Warsteinia (Rowe, 1997) possess winged integumentary lobes.As in Alasemenia, the lobes 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.In contrast to Alasemenia, Warsteinia has four integumentary lobes and their free portions are short, flat and straight.

Functions of Devonian acupulate ovules and evolution of winged ovules
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.Little is known about the dispersal syndrome of Famennian ovules, because the wings as a derived character are rarely documented.Guazia, Warsteinia, and now Alasemenia indicate that the anemochory originated in Famennian.Their integumentary wings illustrate diversity in number (three or four per ovule), length, folding or flattening, and being straight or curving distally.Alasemenia confirms that, like Guazia, the integuments of acupulate ovules developed a new function in wind dispersal.
In early seed plants, the fertile branches terminated by ovulate cupules 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).Of 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.
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(Long, , 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).
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 inwards curving wings, Alasemenia with long and outwards extending wings would efficiently reduce the rate of descent and be more capably moved by wind.

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(Augspurger et al., , 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  ter is: where  is the weight of samaras, AW is the surface area of the wing, /  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(Rowe, , 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 10 3 -10 4 , 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,  is the density of air,  is the windward face,  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   and  represents the number of wings revolving on its own axis, we define a function () to represent the area of windward when the angle between airflow and wings is .We introduce relative efficiency   for comparison.Here we list 5 ideal basic situations.The summary results are shown in Fig. 5.
1.  = 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 2  , which can be written as: We define a function () to represent the accumulated area of windward in a cycle.By definition, 2.  = 2.In this situation, we discuss the condition when  ∈ [0, ].
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. 5.The relative efficiency (Er) of these seeds in five ideal basic situations are 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 relative efficiency for wind dispersal is 100%.In descending through autorotation, one-to four-winged seeds present different relative efficiencies for wind dispersal.
In summary, the mathematical analysis of winged seeds indicates that the relative wind dispersal efficiency of three-winged seeds is obviously better than that of singleand two-winged seeds, and is close to that of four-winged seeds (Fig. 5).In addition, the maximum windward area of each wing of Alasemenia is greater than that of Guazia and Warsteinia with four wings.Significantly, three-winged seeds have the most stable area of windward, which also ensures the motion stability in wind dispersal.All these factors suggest that Alasemenia is well adapted for anemochory.photographs were made with a digital camera and microscope.-12b, 10a, 9b).f, g, Part and counterpart.h-k, Sections of seed in f and g (at four lines, in ascending orders) (Slide PKUBC19798-8b, 6b, 4a, 4b).l, m, Part and counterpart.n-r, Sections of seed in l and m (at five lines, in ascending orders), showing three wings departing centrifugally (Slide PKUBC17835-5a, 7b, 8b, 9a, 10a).s, v, A, One seed sectioned.t, u, Sections of seed in s (at two lines, in ascending orders) (Slide PKUBC18716-8b, 7a).w-z, Sections of seed in v (at four lines, in ascending orders) (Slide PKUBC20774-7a, 6b, 3a, 3b).B-E, Sections of seed in A (at four lines, in ascending orders), showing three wings departing centrifugally (Slide PKUB17904-5b, 4a, 4b, 3b).Scale bars, 2 mm (a, b, f, g, l, m, s, v, A), 1 mm (c-e, h-k, n-r, t, u, w-z, B-E).Fig. 5.The mathematical analysis of wind dispersal ability of ovules with 1-4 wings.The maximum windward area of each wing is   and  represents the number of wings per ovule. is the distance from the tip of wing to the axis of ovules.() represents the area of windward when the angle between airflow and wings is , and () represents the accumulated area of windward in a cycle.  (%) means relative efficiency for wind dispersal.Red lines and expressions show the situation of  = 1.