Annals of Botany 123: 451–460, 2019 doi: 10.1093/aob/mcy170, available online at www.academic.oup.com/aob

Cretaceous asterid evolution: of Eydeia jerseyensis sp. nov. () from the upper of eastern

Brian A. Atkinson1,2,*, Camila Martínez3 and William L. Crepet3

1Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, KS 66044, USA, 2Biodiversity Institute and Museum of Natural History, University of Kansas, Lawrence, KS 66044, USA and 3L. H. Bailey Hortorium, Biology Downloaded from https://academic.oup.com/aob/article/123/3/451/5096126 by guest on 28 September 2021 Section, School of Integrative Plant Science, Cornell University, Ithaca, NY 14853, USA *For correspondence. E-mail [email protected]

Received: 21 March 2018 Returned for revision: 5 May 2018 Editorial decision: 13 August 2018 Accepted: 10 September 2018 Published electronically 13 September 2018

• Background and aims The (>80 000 extant ) appear in the record with considerable diversity near the Turonian– boundary (~90 Ma; Late ) and are strongly represented in the earliest diverging lineage, Cornales. These early asterid representatives have so far been reported from western North America and eastern Asia. In this study, we characterize a new cornalean taxon based on charcoalified fruits from the upper Turonian of eastern North America, a separate landmass from western North America at the time, and identify early palaeobiogeographical patterns of Cornales during the Cretaceous. • Methods were studied and imaged using scanning electron microscopy and micro-computed tomogra- phy (micro-CT) scanning. To assess the systematic affinities of the fossils, phylogenetic analyses were conducted using maximum parsimony. • Key results The charcoalified fruits are represented by tri-locular woody endocarps with dorsal apically open- ing germination valves. Three septa intersect to form a robust central axis. Endocarp ground tissue consists of two zones: an outer endocarp composed of isodiametric sclereids and an inner endocarp containing circum-locular fibres. Central vasculature is absent; however, there are several small vascular bundles scattered within the septa. Phylogenetic analysis places the new taxon within the extinct Eydeia. • Discussion Thick-walled endocarps with apically opening germination valves, no central vascular bundle and one per locule are indicative of the order Cornales. Comparative analysis suggests that the fossils represent a new species, Eydeia jerseyensis sp. nov. This new taxon is the first evidence of Cornales in eastern North America during the Cretaceous and provides insights into the palaeobiogeography and initial diversification of the order.

Key words: Asterids, Cornales, core , Cretaceous, fossils, fruits, , palaeobiogeography.

INTRODUCTION charcoalified , an abundance of ericalean taxa have been characterized from the uppermost Turonian of eastern Exceptionally well-preserved fossils recently recovered from North America (Nixon and Crepet, 1993; Crepet et al., 2013; Upper Cretaceous deposits (~100–66 Ma) have provided mean- Martínez et al., 2016). For much of the , North ingful advancements in our understanding of the initial diversifi- America was divided by the Western Interior Seaway, sepa- cation of major core eudicot clades, the asterids and rosids (e.g. rating two distinct landmasses, (western half) and Friis et al., 2011, 2016; Atkinson, 2016, 2018; Martínez et al., (eastern half). Abundant palaeontological data sug- 2016; Atkinson et al., 2018). The earliest known core eudicots gest that northern Laramidia was connected with eastern Asia are rosid flowers and infructescences from the middle Cretaceous during the Late Cretaceous (discussed in Farke et al., 2014). (~100 Ma) of North America (Basinger and Dilcher, 1984; Friis However, despite their strong representation at the Turonian– et al., 2016; Manchester et al., 2018). Asterids appear relatively Coniacian boundary, Cornales have not yet been recovered late in the fossil record, near the Turonian–Coniacian boundary from Appalachia and have not yet been recovered from (~90–89 Ma) (Takahashi et al., 2002; Martínez-Millán, 2010; Laramidia or Asia (see Atkinson et al., 2018 for a discussion Friis et al., 2011; Manchester et al., 2015; Atkinson et al., 2018), on early asterids). It appears that each order initially diversified indicating that the initial phase of core eudicot evolution was in separate geographical regions, suggesting early endemism. dominated by rosid taxa; however, this pattern could be due to In this study, we characterize a new asterid taxon based on reporting and sampling biases. 106 charcoalified fruits from the upper Turonian Old Crossman Turonian–Coniacian asterids are represented by the two Clay Pit locality. The morphology and anatomy of these fruits successive earliest-diverging lineages, Cornales and Ericales, are indicative of the order Cornales. Phylogenetic analyses respectively. A diversity of cornalean fruits are known from and their unique combination of characters indicates that they the lowermost Coniacian of Asia and western North America represent a new species, Eydeia jerseyensis sp. nov. Atkinson, (Takahashi et al., 2002; Atkinson et al., 2018). Based on Martínez et Crepet. This report corresponds to the first record

© The Author(s) 2018. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For permissions, please e-mail: [email protected]. 452 Atkinson et al. — Cretaceous Cornales evolution of Cornales in Appalachia during the Cretaceous, and expands Facility, Corvallis, OR, USA). Micro-computed tomography their known geographical distribution at the time of their earli- (micro-CT) scanning was also used to view internal structure of est appearance in the fossil record. The early diversity and dis- the holotype (CUPC 1601) and was conducted at Cornell tribution of the cornalean fossil record supports the hypothesis University on the Zeiss Versa 520, at 60 kV/5 W, using the ×4 that the asterids were diversifying alongside the rosids prior to objective and an LE3 filter. The data were reconstructed from the Coniacian (Atkinson et al., 2018). 1601 fluoroscopy exposures of 1 s. The voxel size was 3.71 µm. The program used to visualize the CT scan results was OsiriX 64 bit DICOM Viewer. Images were processed using Photoshop MATERIALS AND METHODS CS 5.0 (Adobe, San Jose, CA, USA). Palaeobiogeographical maps (Fig. 5) were obtained from Scotese (2001) and One hundred and six charcoalified fruits were recovered from Plateau Geosystems (2014). the Old Crossman Clay Pit locality, south of the Raritan River Downloaded from https://academic.oup.com/aob/article/123/3/451/5096126 by guest on 28 September 2021 in Sayreville, Middlesex County, NJ, USA (40°28’ N, 74°19′ W; Fig. 1). Geologically, this locality belongs to the South Phylogenetic analyses Amboy Fire Clay Member of the Raritan Formation (Fig. 1). The Raritan Formation is composed of four members, of which the With the addition of the taxon described in this study, the mor- upper one corresponds to the South Amboy Fire Clay Member phological data matrix generated by Atkinson (2018) using 59 (Christopher, 1979; Sirkin, 1991). This member consists of mas- taxa (25 fossil and 34 extant) and 77 characters was utilized as sive unconsolidated to laminated, dark grey clay, and contains the basis of the phylogenetic analyses using maximum parsimony lignitized plant fragments, charcoalified flowers, stems, and is available through MorphoBank (O’Leary and Kaufman, fragments, fruits, and small pieces of that may have inclu- 2012; Project P3236). Seven characters were deactivated to sions of plant or insect material (Sugarman et al., 2005; Grimaldi improve phylogenetic resolution (Atkinson, 2018). The matrix and Nascimbene, 2010). The unconsolidated clay-silt beds gener- was analysed with and without a constraint topology. For the con- ally occur in channels, and are commonly adjacent to cross-bed- straint topology six nodes, grouping modern clades known from ded, fine to medium quartz sands with thin carbonaceous layers molecular phylogenies (Xiang et al., 2011), were constrained: (Sugarman et al., 2005). One of the more prevalent hypotheses (1) + Alangiaceae; (2) –Mastixiaceae– to explain the three-dimensional preservation at the cellular level Davidiaceae; (4) ; (5) ; and (6) the of these charcoalified fossils is that wildfires converted plant Ericales outgroup. None of the fossil taxa was constrained for the remains to carbonized replicas that were buried in the forest analysis. The phylogeny was estimated based on maximum par- litter (Grimaldi and Nascimbene, 2010; Friis et al., 2011). simony criteria using TNT (Goloboff, 1998) through Winclada The paucity of marine invertebrates in rocks from the version 1.99 (Nixon, 2015). In the TNT analyses, ten sets of 500 Cretaceous Atlantic Coastal Plain has prevented precise cor- iterations and 10 % perturbation of characters were used for the relations of the lithological units with zonations based on ratchet analysis (Nixon, 1999), and default values were used for marine organisms; therefore, age determinations have been drift, sectorial search and fusion. A strict consensus and a based primarily on palynology (Christopher, 1982). The bootstrap analysis were implemented to assess the coherence and Complexiopollenites exigua–Santalacites minor palynologi- support of the phylogenetic inference. The bootstrap was esti- cal zone has been consistently recognized in the South Amboy mated using 100 replications in Winclada using Nona (Goloboff, Fire Clay (Doyle and Robbins, 1977; Christopher, 1979). The 1998). Visualization of character distribution was also performed age of this zone has been mostly considered middle to late with Winclada version 1.99 (Nixon, 2015). Turonian (Doyle and Robbins, 1977; Christopher, 1979, 1982; Sirkin, 1991). In this study we chose latest Turonian as a more conservative date for the fossils. The Raritan Formation prob- RESULTS ably represents a fluvial/deltaic depositional environment (Christopher, 1979) possibly similar to present-day coastal Systematics swamp forests of the Gulf coasts of the US, with coniferous stands and swamp-dwelling angiosperms (Sugarman et al., Order: Cornales sensu Xiang et al. (2011). 2005; Grimaldi and Nascimbene, 2010). Specifically, the South Genus: Eydeia Stockey, Nishida et Atkinson (2016). Amboy Clay Member may have represented the filling of old Species: Eydeia jerseyensis sp. nov. Atkinson, Martínez-A. et meanders that would correspond with a phase of marine regres- Crepet. sion (Christopher, 1979). Specific diagnosis: Endocarps ovoid, with acuminate apex. Bulk samples from the Old Crossman Clay pit were washed Germination valves short and elongate with one to three ridges. and sieved several times and treated with hydrofluoric acid. Exterior periphery of septa forming longitudinally elongate Subsequently the fossils were sorted and identified using a Zeiss ribs. Outer endocarp consisting of sclereids. Inner endocarp SV-11 stereomicroscope. To obtain anatomical data, several present, composed of circum-locular fibres. Three dorsal vas- specimens were dissected using a razor blade. Dissected speci- cular bundles per germination valve. mens were studied and imaged using scanning electron micros- Holotype: CUPC-1601. copy (SEM). The fruits were mounted on a stub using fingernail Paratypes: CUPC-1602 to 1707. polish and were coated with 9 nm of Au-Pd on a Cressington Repository: Cornell University Paleobotanical Collection, L.H. 108 sputter-coater. SEM images were obtained using a Quanta Bailey Hortorium, Plant Biology Section, School of Integrative 600 FEG SEM (Oregon State University Electron Microscopy Plant Science, Cornell University, Ithaca, NY. Atkinson et al. — Cretaceous Cornales evolution 453

40°28´50˝ 40°27´50˝ 74°17´30˝ Downloaded from https://academic.oup.com/aob/article/123/3/451/5096126 by guest on 28 September 2021 74°20´00˝ 40 km 0 03 02 01 Sugarman et al. , 2005 ). Clay ( Sugarman Woodbridge Fire Clay; Kmo, Old bridge sand; Krw, Amboy Kms, South the Old Crossman Clay Pit (red arrow). . The map on the left shows the The map on the left shows . from http://www.state.nj.us/dep/njgs/pricelst/gmseries.htm geology of the area. Modified from maps downloaded Location of the Old Crossman Clay Pit and surface 1. Fig. rocks, rocks are Palaeozoic Map 1:24 000; 2005). In grey Geological Survey Jersey (New Jersey geology of New The centre map illustrates the surface within the USA. Jersey location of New rectangle in the centre map and location of the zoomed area of grey The map on the right shows are rocks. and metamorphic igneous rocks; in green are yellow 454 Atkinson et al. — Cretaceous Cornales evolution

Type locality: Old Crossman Clay Pit, Sayreville, New Jersey (USA; 40°28′ N, 74°19′ W). Age: Uppermost Turonian (~90 Ma).

Description Each fossil fruit consists of a three-dimensionally preserved charcoalified woody endocarp. Endocarps are ovoid in shape, 1.0–3.0 mm long and 0.5–1.0 mm wide, with an acuminate apex that most likely represents the base of the style (Figs 2A and 3A, B; Supplementary Data Video S1). Endocarps have Downloaded from https://academic.oup.com/aob/article/123/3/451/5096126 by guest on 28 September 2021 apically opening dorsal germination valves that are associated with each locule (Figs 2A and 3G). The lengths of the valves can vary on an individual fruit, in which some are roughly restricted to the apical half of the endocarps while others are more elongated (Fig. 2A). There are one to three ridges per valve, which are more conspicuous towards the apical half of the endocarp (Figs 2C and 3C). Each endocarp was found to have three germination valves indicating the presence of three locules as also seen in several dissected and CT-scanned fruits (Fig. 3C). The locules are ellipsoid to sub-triangular in cross- section. There are three septa that separate each germination valve (and locule) and extend outwards slightly beyond the valves to form longitudinally elongate ribs (Fig. 2C). The septa A B intersect to form a robust central axis (Fig. 3C, D, F). Ground tissue of the valves, septa and central axis is composed of two zones, the inner and outer endocarp. The outer endocarp consists of isodiametric sclereids (Fig. 3D–H). The inner endo- carp is composed of circum-locular fibres, two or three cell lay- ers thick (Fig. 3E). A distinct locule lining was not observed. Vascular tissues of the endocarps are located in the dorsal and ventral areas. Dorsal vasculature is represented by three bundles that run longitudinally along the surface, opposite to the ridges (Fig. 2A). A central vascular strand is absent within the endocarps (Fig 3D); however, several small vascular bun- dles consisting of about six tracheary elements can be found scattered within the septa (Fig. 3F–H). There is one apically attached seed per locule (Fig. 3B, C; Supplementary Data Video S1). The fill much of the space within the locules (Fig. 3B). Due to the preservation, it is C difficult to decipher the histology of the seeds. Fig. 2. Eydeia jerseyensis sp. nov. (A) Exterior view of endocarp with three dorsal vascular bundles (arrowheads) showing apical half of locule cavity, indi- cating that the missing valve was short. Note acuminate apex. CUPC-1602. Phylogenetic analysis Scale bar = 1.0 mm. (B) Exterior view of endocarp showing more of the locule cavity than in (A), suggesting that the valve was relatively elongate. CUPC- For the constrained analysis, 12 most-parsimonious 1603. Scale bar = 1.0 mm. (C) Apical view of endocarp showing the apically were found in the phylogenetic analysis with a consistency opening valve and three ridges on the adjacent valve (arrowheads). CUPC- index (CI) of 94 and a retention index (RI) of 98. The strict 1604. Scale bar = 0.5 mm. consensus collapsed 13 nodes and had a length of 2282 steps (Fig. 4A). The unconstrained analysis recovered 216 most-par- simonious trees with CI = 36 and RI = 70. The strict consen- A comparison between the phylogenetic analyses revealed sus collapsed 18 nodes (Fig. 4) and had a length of 214 steps differences in two family nodes: Cornaceae and Nyssaceae. (Fig. 4B). The bootstrap analysis provided strong support for Cornaceae is recovered as polyphyletic because most of the non-collapsed nodes of the strict consensus tree. oblonga is sister to Alangiaceae. Taxa within Nyssaceae The analysis places the fossil E. jerseyensis in a polytomy with are found in a polytomy with Davidiaceae. All the other the fossils Eydeia vancouverensis and the ‘Drumheller Fruit 1’ constrained nodes were also found in the unconstrained within the fossil grade leading the Nyssaceae, Mastixiaceae and analysis, suggesting that the fruit morphology of Cornales Davidiaceae (NMD stem ) in core Cornales. These three is useful to assess the phylogenetic position of fossil fruits extinct taxa share acuminate apices. within this group. Atkinson et al. — Cretaceous Cornales evolution 455 Downloaded from https://academic.oup.com/aob/article/123/3/451/5096126 by guest on 28 September 2021

C

ABD

G

EF H

Fig. 3. (A) Image still of micro-CT scan showing general morphology of endocarp. Note acuminate apex. CUPC-1601. Scale bar = 0.5 mm. (B) Image still of micro-CT scan endocarp in longitudinal section. Note apically attached seed (arrow). Note acuminate apex. CUPC-1601. Scale bar = 0.5 mm. (C) Image still of micro-CT scan showing cross-section of tri-locular endocarp. Note septal ribs (arrows) and single seed in upper left locule. CUPC-1601. Scale bar = 0.25 mm. (D) SEM of cross-section of endocarp showing central axis containing sclereids and no central vascular strand. CUPC-1605. Scale bar = 200 µm. (E) SEM of cross-section of dorsal area of endocarp showing isodiametric sclereids (outer endocarp) and layer of circum-locular fibres (inner endocarp). CUPC-1606. Scale bar = 50 µm. (F) SEM of cross-section of septum showing isodiametric sclereids with scattered small vascular bundles (arrowheads). Note separated germination valve at bottom left. CUPC-1607. Scale bar = 100 µm. (G) SEM of vascular bundle with septum in cross-section. CUPC-1607. Scale bar = 20 µm. (H) SEM of vascular bundles within septum in cross-section. CUPC-1607. Scale bar = 20 µm. 456 Atkinson et al. — Cretaceous Cornales evolution

AB Fouquieria columnaris Fouquieria columnaris Hydrocera triflora Ericales outgroups 82 Hydrocera triflora Ericales outgroups Marcgravia nepenthoides Marcgravia nepenthoides dispersa Loasaceae 100 99 Loasa sclareifolia Loasaceae Loasa sclareifolia Mentzelia dispersa americana 79 80 Deutzia corymbosa Hydrangeaceae 73 Deutzia corymbosa Hydrangeaceae heteromalla 74 Hydrangea heteromalla Philadelphus purpurascens 69 Philadelphus purpurascens Hydrostachys spp. Hydrostachyaceae Hydrostachys spp. Hydrostachyaceae Grubbia rosmarinifolia Grubbia rosmarinifolia Grubbiaceae 76 Grubbiaceae Amersinia obtrullata* 81 Amersinia obtrullata* Hironia fusiformis* Hironia fusiformis* 97 Curtisia dentata 92 Curtisia dentata Curtisiceae Curtisiceae

Curtisia quadrilocularis* Curtisia quadrilocularis* Downloaded from https://academic.oup.com/aob/article/123/3/451/5096126 by guest on 28 September 2021 javanicum Cornus oblonga Alangium villosum 84 70 Alangium javanicum Alangium vermontanum* Alangiaceae 77 Alangium villosum Alangium chinense Alangiaceae 91 Alangium vermontanum* Alangium eydei* 83 Alangium chinense Cornus oblonga 76 Alangium eydei* 74 95 Cornus controversa Cornus controversa Cornus sanguenea Cornus sanguenea 81 Cornus canadensis Cornus kousa Cornaceae Cornus piggae* Cornus eydeana 70 71 Cornus florida Cornus multilocularis* 86 Cornus canadensis Cornus volkensii Cornus kousa Cornus mas 71 Cornus eydeana 83 Cornus officinalis Cornus multilocularis* Cornus piggae* Cornus volkensii Edencarpa grandis* Edencarpa grandis* Sheltercarpa vancouverensis* 70 Sheltercarpa vancouverensis* Eydeia hokkaidoensis* 70 Eydeia hokkaidoensis* Drumheller fruit 1* Stem NMD Drumheller fruit 1* Eydeia jerseyensis* 69 Eydeia jerseyensis* group Stem NMD Eydeia vancouverensis* 69 Eydeia vancouverensis* Obamacarpa edenensis* Obamacarpa edenensis* group Drumheller fruit 2* 85 Drumheller fruit 2* Suciacarpa starrii* 95 Suciacarpa starrii* Suciacarpa xiangae* 69 Suciacarpa xiangae* Nyssa grayensis* Camptotheca acuminata Nyssa aquatica Nyssa talamancana 72 Nyssa grayensis* Nyssa javanica Nyssaceae Nyssa ogoche Nyssa spatulata* Nyssa sylvatica Camptotheca acuminata Nyssa talamancana Nyssa aquatica 75 83 Davidia antiqua*

Nyssa ogoche n

Davidia involucrata n Davidia antiqua* 79 Nyssa javanica Davidia involucrata Davidiaceae

Cr ow Nyssa spatulata* eydei* Cr ow

NMD group Beckettia samuelis* Diplopanax stachyanthus Langtonia bisulcata* NMD group Langtonia bisulcata* 76 philippinensis Retinomastixia schultei* Mastixioidiocarpum oregonense* Beckettia samuelis* Retinomastixia schultei* Mastixia philippinensis 85 Diplopanax eydei* Mastixioidiocarpum oregonense* Mastixiaceae Diplopanax stachyanthus

Fig. 4. Phylogenetic analyses. The fossil Eydeia jerseyensis sp. nov. is shown in bold font within the NMD crown group. *Fossil taxa. (A) Constrained analysis. Strict consensus tree of 12 most parsimonious trees for Cornales based on fruit morphological characters. The stars above the branches show those nodes that were constrained in the analysis. (B) Unconstrained analysis. Strict consensus of 216 most parsimonious trees. The numbers above the node branches are bootstrap values.

DISCUSSION Fruit 1’ (Atkinson, 2018). This clade is united by the pres- ence of ridged germination valves, and several small vascular Eydeia jerseyensis sp. nov. is characterized by relatively thick- walled woody endocarps with apically opening dorsal germi- bundles within the septa. The presence of an acuminate apex nation valves, a single apically attached seed per locule, rows unites E. vancouverensis, Drumheller Fruit 1 and E. jerseyensis of vascular bundles within the septa, and no central vascular (Supplementary Data Fig. S1). However, it is worth noting that strand. This combination of characters is indicative of the order subsets of this character mosaic are present in other cornaleans Cornales (Eyde, 1963, 1967, 1988; Atkinson, 2016; Atkinson (Supplementary Data Fig. S1). et al. 2017). The phylogenetic analysis in this study is con- The Drumheller fruits were recovered from the cordant with that of Atkinson (2018) and places E. jerseyensis of Alberta, Canada and Eydeia jerseyensis differs from these within an Eydeia clade consisting of E. hokkaidoensis Stockey, Canadian fossils by having more than one ridge per valve. Nishida et Atkinson, E. vancouverensis Atkinson, Stockey et Furthermore, the Drumheller fruits can have up to five locules Rothwell, and an undescribed fossil cornalean, ‘Drumheller per fruit while E. jerseyensis consistently has three (Table 1). Atkinson et al. — Cretaceous Cornales evolution 457

The septa and central axes of the Drumheller fruits contain It is worth noting that palaeontological evidence indicates that elongate sclereids that are lacking in the E. jerseyensis fruits Laramidia had a northern connection with Asia (discussed in (R. Serbet, University of Kansas, USA, pers. comm.). Farke et al., 2014). The diversity and disjunct geographical dis- Eydeia hokkaidoensis was described based on five perminer- tribution (EA and WNA versus ENA) of cornaleans at their ear- alized fruits from the of Hokkaido, Japan (Stockey liest appearance clearly indicates that the divergence and initial et al., 2016). While the endocarps of E. hokkaidoensis have diversification of the order occurred well before the end of the rounded apices and one ridge per valve, those of E. jerseyen- Turonian (Atkinson et al., 2018). sis have acuminate apices and two ridges per valve (Table 1). Lithostratigraphic, isotopic and palaeontological data indi- Furthermore, E. hokkaidoensis has up to five locules per fruit cate that for a geologically brief amount of time (~0.5–1.3 m.y.) in contrast to the consistently tri-locular fruits of E. jerseyensis. at the – boundary (~100 Ma) the Western In addition, E. jerseyensis endocarps contain an inner endocarp Interior Seaway experienced a regressive event that disrupted layer that is absent in E. hokkaidoensis and there is only one the connection between the and the Arctic Ocean Downloaded from https://academic.oup.com/aob/article/123/3/451/5096126 by guest on 28 September 2021 dorsal vascular bundle per valve in the fruits of E. hokkaid- (Dolson et al., 1991; Gröcke et al., 2006; Koch and Brenner, oensis (Stockey et al., 2016), while there are three bundles per 2009; also see Slattery et al., 2015). This event resulted in an valve in those of E. jerseyensis. alluvial plain (near present-day Nebraska, Colorado, Kansas, Eydeia vancouverensis was characterized based on sev- northern , Oklahoma Panhandle and northern eral dozen endocarps from the uppermost Coniacian Comox Texas) that may have occasionally been inundated with brack- Formation (Nanaimo Group) of Vancouver Island (Atkinson ish waters (Dolson et al., 1991; Oboh-Ikuenobe et al., 2008). et al., 2018). Endocarps of E. vancouverensis contain up to five This alluvial plain can be thought of as a southerly land bridge locules while those of E. jerseyensis only have three. The two or corridor connecting WNA and ENA (Fig. 5B) that would species differ in histology as well; E. vancouverensis endo- have allowed faunal and floral exchange between the two halves carps contain elongate sclereids that are intertwined with iso- of the continent. Although cornalean fruits may have simply diametric sclereids that are lacking in E. jerseyensis endocarps. floated across the Western Interior Seaway, the corridor would Moreover, fruits of E. jerseyensis have an inner endocarp layer have made movement between the two landmasses easier. By of circum-locular fibres, which is lacking in E. vancouverensis the middle Cenomanian, a transgression event reconnected the (Table 1). Gulf of Mexico with the Arctic Ocean, and as a consequence Based on the differences enumerated above and the phyloge- separated Laramidia (and Asia) from Appalachia (see Slattery netic position of this fossil taxon, it is clear that it represents a et al., 2015 for a review on the history of the seaway; Fig. 5C). new species, Eydeia jerseyensis Atkinson, Martínez et Crepet. This lack of connectivity would have hindered any extensive Thus, in addition to expanding the known diversity of extinct biotic exchange between the two landmasses (Fig. 5). Overall, Cretaceous cornaleans, this report provides new insights into this palaeobiogeographical hypothesis needs to be tested by the initial diversification of the order (see below). collecting fossil from Albian–early Cenomanian depos- its of the corridor/alluvial plain to evaluate whether there are any representatives of Cornales that were present at this time. Due to the palaeobiogeographical distribution of Cornales Diversification and biogeography of Cretaceous asterids at the TCB, we hypothesize that the divergence of the order Cornales appear in the fossil record near the Turonian– may have been as early as the Albian–Cenomanian (~100 Ma) Coniacian boundary (TCB), with five species assigned to four boundary, a time when Cornales could easily migrate between different genera distributed in eastern Asia (EA), western North Laramidia and Appalachia. Moreover, palaeobotanical analyses America (WNA) and eastern North America (ENA): Hironoia and molecular divergence time estimates are concordant in sug- Takahashi, Crane et Manchester (EA), Obamacarpa Atkinson, gesting that the divergence and initial diversification of Cornales Stockey et Rothwell (WNA), Edencarpa Atkinson, Stockey et occurred ~100–96 Ma (Xiang et al., 2011; Atkinson, 2018). Rothwell, (WNA) and Eydeia (WNA and ENA) (Takahashi Cornales may have reached Appalachia from Europe (or vice et al., 2002; Atkinson et al., 2018). The taxon described in this versa), but so far no fossils of this clade have been recovered study, E. jerseyensis, is the first cornalean described near the from the TCB (or earlier) of Europe. An alternative hypothesis TCB within ENA. During the Late Cretaceous much of North to explain this distribution would be long-distance dispersal America was covered by the Western Interior Seaway, a con- between Laramidia and Appalachia. Cornalean fruits are small siderable geographical barrier that divided the western half enough to travel long distances and many extant cornaleans (Laramidia) from the eastern half (Appalachia) of the continent. fruits are known to disperse via water, e.g. Nyssa (Eyde, 1963)

Table 1. Comparisons of Eydeia and similar species

Taxon Age Acuminate apex Number of locules Valve length Maximum number Inner endocarp of ridges/valve

Eydeia jerseyensis Late Turonian Present 3 Short-elongate 3 Present Eydeia vancouverensis Early Coniacian Present 3 or 4 Elongate 2 Absent Eydeia hokkaidoensis Santonian Absent 4 or 5 Elongate 1 Absent Drumheller fruit Campanian Present 1–5 Elongate 2 Absent

Data are from Stockey et al. (2016) and Atkinson et al. (2018). 458 Atkinson et al. — Cretaceous Cornales evolution Downloaded from https://academic.oup.com/aob/article/123/3/451/5096126 by guest on 28 September 2021

A

B C

Fig. 5. Late Cretaceous palaeogeographical maps. Fossil cornalean endocarps mark approximate location of known occurrences. (A) Global map near 90 Ma showing distribution of reported Cornales at their earliest appearance in the fossil record (from Scotese, 2001). (B) Hypothetical distribution and migration of Cornales in North America during the Cenomanian (~100 Ma), potentially explaining distributions seen in (A) and (C). © 2014 Colorado Plateau Geosystems Inc. Note that the Western Interior Seaway is not at its full extent, which provides a corridor between the two landmasses. (C) Broad-scale distribution of Cornales in Laramidia and Appalachia with the Western Interior Seaway at its full extent separating the two landmasses. © 2014 Colorado Plateau Geosystems Inc. Distributions based on Takahashi et al. (2002), Atkinson et al. (2018) and this study. Atkinson et al. — Cretaceous Cornales evolution 459 and Cornus (Eyde, 1988). Older deposits from both landmasses Atkinson BA. 2018. The critical role of fossils in inferring deep-node phyloge- as well as Europe are needed to test this hypothesis and deci- netic relationships and macroevolutionary patterns in Cornales. American Journal of Botany 105: 1–11. pher the direction of early cornalean migration during the Atkinson BA, Stockey RA, Rothwell GW. 2017. The early phylogenetic Cretaceous. diversification of Cornales: permineralized cornalean fruits from the Ericales is sister to the remaining asterids (Angiosperm Campanian (Upper Cretaceous) of western North America. International Phylogeny Group, 2016) and, like Cornales, appears in the Journal of Plant Sciences 178: 556–666. fossil record near the TCB. The oldest reported fossils of this Atkinson BA, Stockey RA, Rothwell GW. 2018. Tracking the initial diversi- fication of asterids: anatomically preserved cornalean fruits from the early order are a diversity of flowers from the Old Crossman Clay Pit Coniacian (Late Cretaceous) of western North America. International locality (Nixon and Crepet, 1993; Martínez-Millán et al., 2009; Journal of Plant Sciences 179: 21–35. Crepet et al., 2013; Martínez et al., 2016). However, there have Basinger JF, Dilcher DL. 1984. Ancient bisexual flowers. Science 224: been no formal descriptions of Ericales from deposits of the 511–513.

Christopher RA. 1979. Normapolles and triporate assemblages from Downloaded from https://academic.oup.com/aob/article/123/3/451/5096126 by guest on 28 September 2021 same age from other regions (e.g. Laramidia). A potential eri- the Raritan and Magothy Formations (Upper Cretaceous) of New Jersey. calean fruit from the uppermost Coniacian Eden Main local- Palynology 3: 73–121. ity of Vancouver Island has been briefly described by Karafit Christopher RA. 1982. The occurrence of the Complexiopollis-Atlantopollis (2008), but this fruit requires further analysis to confirm its zone (Palynomorphs) in the (Upper Cretaceous) of taxonomic affinities. Another possible Ericales taxon has been Texas. Journal of Paleontology 56: 525–541. Crepet WL, Nixon KC, Daghlian CP. 2013. Fossil Ericales from the Upper reported from the uppermost Coniacian Kamikitaba locality of Cretaceous of New Jersey. International Journal of Plant Sciences 174: Honshu, Japan (Takahashi et al., 1999). Recently characterized 572–584. well-preserved Cretaceous fossils, such as E. jerseyensis, are Dolson J, Muller D, Evetts MJ, Stein JA. 1991. Regional paleotopographic contributing much needed information on the initial diversifica- trends and production, muddy sandstone (Lower Cretaceous), central and northern Rocky Mountains. American Association of Petroleum Geologists tion of core eudicots (e.g. Martínez et al., 2016; Friis, et al., Bulletin 75: 409–435. 2016; Atkinson et al., 2018). Doyle JA, Robbins EI. 1977. Angiosperm pollen zonation of the continental Structurally preserved angiosperm fossils recently recovered Cretaceous of the Atlantic coastal plain and its application to deep wells in from Cretaceous deposits are starting to shed much-needed the Salisbury embayment. Palynology 1: 41–78. light onto early macroevolutionary and palaeobiogeographi- Eyde RH. 1963. Morphological and paleobotanical studies of the Nyssaceae, I. A survey of the modern species and their fruits. Journal of the Arnold cal patterns of important and diverse clades. We anticipate Arboretum 44: 1–59. that increased sampling of ancient asterids from Cenomanian– Eyde RH. 1967. The peculiar gynoecial vasculature of Cornaceae and its sys- Turonian deposits from various areas around the world will be tematic significance. Phytomorphology 17: 172–182. essential for testing the above palaeobiogeographical hypoth- Eyde RH. 1988. Comprehending Cornus: puzzles and progress in the system- atics of the dogwoods. Botanical Review 54: 233–351. eses and elucidating the early evolution of the clade as a whole. Farke AA, Maxwell WD, Cifelli RL, Wedel MJ. 2014. A ceratopsian dino- saur from the Lower Cretaceous of western North America, and the bioge- ography of Neoceratopsia. PLoS ONE 9: e112055. SUPPLEMENTARY DATA Friis EM, Crane PR, Pedersen KR. 2011. Early flowers and angiosperm evo- lution. Cambridge, NY: Cambridge University Press. Supplementary data are available online at https://academic. Friis EM, Pedersen KR, Crane PR. 2016. The emergence of core eudicots: oup.com/aob and consist of the following. Fig. S1: strict con- new floral evidence from the earliest Late Cretaceous. Proceedings of the sensus tree of 192 most parsimonious trees for Cornales based Royal Society B: Biological Sciences 283: 20161325. Grimaldi DA, Nascimbene PC. 2010. Raritan (New Jersey) amber. In: Penney on fruit morphological characters. The circles represent char- D, ed. Biodiversity of fossils in amber from the major world deposits. acters present in a clade or in a taxon; the numbers above the Manchester, UK: Siri Scientific Press, 167–191. circles represent the character number and the numbers below Goloboff P. 1998. Nona. Computer program and software. [Published by the the circle represent the character state (Atkinson, 2018). Black author.] Tucuman, . Gröcke DR, Ludvigson GA, Witzke BL, et al. 2006. Recognizing the Albian- circles represent synapomorphies or autoapomorphies, and Cenomanian (OAE1d) sequence boundary using plant carbon isotopes: white circles represent homoplasies. Video S1: micro-CT scan Dakota Formation, Western Interior Basin, USA. Geology 34: 193–196. of fruit (approaching from side) showing overall morphology Karafit SJ. 2008. Permineralized Late Cretaceous plants from the Eden Main and seed attachment. fossil localities, British Columbia, Canada. MSc Thesis, University of Alberta, Canada. Koch JT, Brenner RL. 2009. Evidence for glacioeustatic control of large, rapid sea-level fluctuations during the Albian-Cenomanian: Dakota for- ACKNOWLEDGEMENTS mation, eastern margin of western interior seaway, USA. Cretaceous Research 30: 411–423. We thank Jennifer Svitko for her work on specimen prepara- Manchester SR, Grímsson F, Zetter R. 2015. Assessing the fossil record of tions and micro-CT scanning. This work was partly funded by asterids in the context of our current phylogenetic framework. Annals of National Science Foundation grant DGE 1314109 to B.A.A. the Missouri Botanical Garden 100: 329–363. Manchester SR, Dilcher DL, Judd WS, Corder B, Basinger JF. 2018. Early Eudicot and fruit: Dakotanthus gen. nov. from the Cretaceous Dakota Formation of Kansas and Nebraska, USA. Acta Palaeobotanica LITERATURE CITED 58: 27–40. Martínez C, Choo TYS, Allevato D, et al. 2016. Rariglanda jerseyensis, Angiosperm Phylogeny Group. 2016. An update of the Angiosperm a new ericalean fossil flower from the Late Cretaceous of New Jersey. Phylogeny Group classification for the orders and families of flowering Botany 94: 747–758. plants: APG IV. Botanical Journal of the Linnean Society 181: 1–20. Martínez-Millán M, Crepet WL, Nixon KC. 2009. Pentapetalum trifas- Atkinson BA. 2016. 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