The emergence of core eudicots: new floral evidence from the earliest Late Cretaceous

Abstract

Eudicots, the most diverse of the three major clades of living angiosperms, are first recognized in the latest Barremian-earliest Aptian. All Early Cretaceous forms appear to be related to species-poor lineages that diverged before the rise of core eudicots, which today comprise more than 70% of angiosperm species. Here, we report the discovery of a well-preserved flower, Caliciflora mauldinensis, from the earliest Late Cretaceous, with unequivocal core eudicot features, including five sepals, five petals and two whorls of stamens borne on the rim of a floral cup containing three free carpels. Pollen is tricolporate. Carpels mature into follicular fruitlets. This character combination suggests a phylogenetic position among rosids, but more specific assignment is precluded by complex patterns of character evolution among the very large number of potentially relevant extant taxa. The whorled floral organization is consistent with ideas that this stable pattern evolved early and was a prerequisite for more integrated patterns of floral architecture that evolved later. However, limited floral synorganization in Caliciflora and all earlier eudicot flowers recognized so far, calls into question hypotheses that substantial diversification of core eudicots had already occurred by the end of the Early Cretaceous.

Keywords: SRXTM; asterid; fossil flower; rosids; synchrotron X-ray microtomography; tricolporate pollen.

Figure 1.

SEM images of flower bud of Caliciflora mauldinensis gen. et sp. nov. from the Late Cretaceous (earliest Cenomanian) Mauldin Mountain locality, MD, USA; holotype (PP53985; sample Mauldin Mountain 116). (a–c) Lateral (a) and apical (b,c) views of stalked flower bud showing subtending bract (br), two prophylls (pp), revolute-valvate sepals (s) and petals (p). (d) Detail of petal surface showing dense indumentum of interlocking stellate hairs. (e) Detail of sepal surface showing a stellate hair.

Figure 2.

SRXTM volume renderings of flower bud of Caliciflora mauldinensis gen. et sp. nov. from the Late Cretaceous (earliest Cenomanian) Mauldin Mountain locality, MD, USA; holotype (PP53985; sample Mauldin Mountain 116). (a) Volume rendering of apical view of entire floral bud showing subtending bract (br), prophylls (pp) and five revolute-valvate sepals (s). (b–g) Transverse views of flower bud at different levels from apex (b) to middle of floral cup (g) showing subtending bract (br), two prophylls (pp), five revolute-valvate sepals (s), five petals (p), three antesepalous stamens (arrowheads), five antepetalous stamens (asterisks) and three carpels; note three closely appressed stigmas (c) and the free ventral margins of carpels below the stigmatic region (f,g) (a, not cut; b, section at level of orthoslice xy0766; c, section at level of orthoslice xy1756; d, section at level of orthoslice xy1916; e, section at level of orthoslice xy2044; f, section at level of orthoslice xy2233; g, section at level of orthoslice xy2427). (h,i) Longitudinal views of flower bud in median section showing floral cup surrounding the carpels and with antesepalous stamens (arrowheads) and antepetalous stamens (asterisks) on the rim of the floral cup (h, section at level of orthoslice xz1112; i, section at level of orthoslice yz0983).

Figure 3.

SRXTM reconstructions (orthoslices) of flower bud of Caliciflora mauldinensis gen. et sp. nov. flower from the Late Cretaceous (earliest Cenomanian) Mauldin Mountain locality, MD, USA; holotype (PP53985; sample Mauldin Mountain 116). (a) Detail of perianth in transverse section below the apex of the flower bud showing the thicker sepals with a layer of thin-walled hypodermal cells (asterisks), thin lamina of a folded petal with an almost glabrous inner surface and a dense indumentum on the outer surface; note the especially clear stellate hair (arrowhead) on the keel of the outer surface of the petal (orthoslice xy1200). (b) Detail of perianth in transverse section close to the apex of the floral bud showing folded petal with dense indumentum on the outer surface and scattered hairs on the inner surface (arrowhead) (orthoslice xy1050). (c) Longitudinal sections of sepals (s) and petals (p) showing dense indumentum; note sepals with dense, infilled cells towards the outside, and a layer of thin-walled hypodermal cells (asterisks) (orthoslice xz1485). (d) Detail of perianth and androecium in transverse section close to the rim of the floral cup showing sepals (s) with dense indumentum of stellate hairs on the outer surface and sepal margins (arrowhead), narrow base of petal (p, arrow) and an antepetalous anther (an, arrow) (orthoslice xy1900). (e) Detail of sepal (s) showing glabrous inner surface and dense indumentum of stellate hairs on the outer surface and sepal margins; note thin-walled cells on the inner surface of the sepal (asterisk) (orthoslice xy1950).

Figure 4.

SEM (a–c, e–g, i–l) and SRXTM (d, h) images of carpels, ovules/seeds, stamens and pollen of Caliciflora mauldinensis gen. et sp. nov. from the Late Cretaceous (earliest Cenomanian) Mauldin Mountain locality, MD, USA. (a) Anthetic specimen in apical view showing five sepals, remnants of a keeled petal (arrow), six stamens and three carpels (PP34773, sample Mauldin Mountain 116). (b,c) Fragment of post-anthetic specimen in apical view (b) showing remains of three carpels (ca) and three elongated, anatropous, reticulate ovules/seeds (arrowhead) in the most complete carpel; note also remains of the slightly bulging margins of the two other carpels (arrows) (PP54159; sample Mauldin Mountain 117). (d) Surface rendering of adaxial surface of petal from specimen in figures 1–3 showing the gradual expansion of the thin petal lamina from the base and the distinct groove, which corresponds to the keel on the abaxial surface (PP53985; sample Mauldin Mountain 116). (e,f) Fragment of post-anthetic specimen showing the dense indumentum of stellate hairs on the surface of the sepals (e) and scattered on the papillate surface of the carpel (f) (PP54160; sample Mauldin Mountain 022). (g) Detail of the apical portion of an anther from anthetic flower in (a) showing numerous pollen grains in situ (PP34773, sample Mauldin Mountain 116). (h) Volume rendering of the floral bud cut at level of orthoslice xy1905 to show stamens with filament attached to dorsal side of the anthers (arrow heads) (PP53985; sample Mauldin Mountain 116). (i–l) Pollen grains are psilate to weakly regulate with three long colpi that reach almost to the pole; a narrow raised area (bridge) is seen at the middle of the colpi (arrows): note tiny, spherical orbicules (arrowheads) with a central depression adhering to the inner surface of the thecae and pollen grains (PP54161; sample Mauldin Mountain 022).

Figure 5.

Floral diagrams of Caliciflora mauldinensis gen. et sp. nov. from the Late Cretaceous (earliest Cenomanian) Mauldin Mountain locality, MD, USA (a) and the Rose Creek Flower [10] from the latest Early Cretaceous or earliest Late Cretaceous (latest Albian–earliest Cenomanian) Rose Creek locality, NE, USA (b).