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. 2020 Aug 29;127(3):305–315. doi: 10.1093/aob/mcaa154

Fossil evidence from South America for the diversification of Cunoniaceae by the earliest Palaeocene

Nathan A Jud 1,✉, Maria A Gandolfo 2
PMCID: PMC7872129  PMID: 32860407

Abstract

Background and Aims

Cunoniaceae are woody plants with a distribution that suggests a complex history of Gondwanan vicariance, long-distance dispersal, diversification and extinction. Only four out of ~27 genera in Cunoniaceae are native to South America today, but the discovery of extinct species from Argentine Patagonia is providing new information about the history of this family in South America.

Methods

We describe fossil flowers collected from early Danian (early Palaeocene, ~64 Mya) deposits of the Salamanca Formation. We compare them with similar flowers from extant and extinct species using published literature and herbarium specimens. We used simultaneous analysis of morphology and available chloroplast DNA sequences (trnL–F, rbcL, matK, trnH–psbA) to determine the probable relationship of these fossils to living Cunoniaceae and the co-occurring fossil species Lacinipetalum spectabilum.

Key Results

Cunoniantha bicarpellata gen. et sp. nov. is the second species of Cunoniaceae to be recognized among the flowers preserved in the Salamanca Formation. Cunoniantha flowers are pentamerous and complete, the anthers contain in situ pollen, and the gynoecium is bicarpellate and syncarpous with two free styles. Phylogenetic analysis indicates that Cunoniantha belongs to crown-group Cunoniaceae among the core Cunoniaceae clade, although it does not have obvious affinity with any tribe. Lacinipetalum spectabilum, also from the Salamanca Formation, belongs to the Cunoniaceae crown group as well, but close to tribe Schizomerieae.

Conclusions

Our findings highlight the importance of West Gondwana in the evolution of Cunoniaceae during the early Palaeogene. The co-occurrence of C. bicarpellata and L. spectabilum, belonging to different clades within Cunoniaceae, indicates that the diversification of crown-group Cunoniaceae was under way by 64 Mya.

Keywords: Gondwana, fossil flowers, Argentina, palaeobotany, Danian, parsimony

INTRODUCTION

The distribution of Cunoniaceae throughout tropical and southern temperate forests suggests a deep Gondwanan legacy (Raven and Axelrod, 1974; Carpenter and Buchanan, 1993; Bradford et al., 2004). The family includes 28 extant genera and six tribes, but six of the genera are not assigned to a tribe (Fig. 1). Several species groups have intercontinental distributions, such as Cunonia L., Eucryphia Cav., Geissoieae, Schizomerieae and Weinmannia L. (Bradford and Barnes, 2001; Sweeney et al., 2004; Hopkins et al., 2013), but disentangling the relative importance of vicariance, long-distance dispersal, extinction and diversification in explaining these disjunctions depends on direct evidence of ancient distributions from the fossil record (Pole, 1994, 2001; Barnes et al., 2001; Sanmartín and Ronquist, 2004; Wilf and Escapa, 2015).

Fig. 1.

Fig. 1.

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Summary of phylogenetic relationships among Cunoniaceae based on previous work (Bradford and Barnes, 2001; Sweeney et al., 2004; Hopkins et al., 2013).

The rich fossil record of Cunoniaceae in Australia provides evidence of at least 11 genera during the Cenozoic, but limited Cretaceous outcrops obscure the earlier history of the family on the continent (Barnes et al., 2001). Elsewhere, fossil occurrences of the family are comparatively rare; therefore, new discoveries have the potential to provide valuable information about the evolution and biogeographic history of Cunoniaceae (e.g. Gandolfo and Hermsen, 2017). In South America and the Antarctic Peninsula (Fig. 2), fossil woods (Petriella, 1972; Archangelsky, 1973; Baldoni and Askin, 1993; Raigemborn et al., 2009) and pollen (Archangelsky, 1973; Romero and Archangelsky, 1986; Troncoso, 1991; Zamaloa, 2000) ascribed to Cunoniaceae have been known for decades, but their possible relationships to extant tribes have not been evaluated through phylogenetic analyses.

Fig. 2.

Fig. 2.

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Map of southern South America and the Antarctic Peninsula showing the occurrences of macrofossils identified to Cunoniaceae. (1) Williams Point Beds (Upper Cretaceous), Williams Point, Antarctica (Poole et al., 2000). (2) Salamanca Formation (Palaeocene), Chubut Province, Argentina (Jud et al., 2018a; this study). (3) Peñas Coloradas Formation (Palaeocene), Chubut Province, Argentina (Raigemborn et al., 2009). (4) Cerro Bororó Formation (Palaeocene), Chubut Province, Argentina (Petriella, 1972). (5) Fossil Hill Formation (Eocene), King George (25 de Mayo) Island, Antarctica (Zhang and Wang, 1994). (6) Sobral Formation (Palaeocene), Seymour (Marambio) Island, Antarctica (Poole et al., 2003). (7) Lopez de Bertodano Formation (Palaeocene), Seymour Island, Antarctica (Poole et al., 2003). (8) La Meseta Formation (Eocene), Seymour Island, Antarctica (Poole et al., 2003). (9) Fildes Formation (Eocene) King George Island, Antarctica (Poole et al., 2001, Francis and Poole, 2002). (10) Huitrera Formation (Eocene), Chubut Province, Argentina (Hermsen et al., 2010; Gandolfo and Hermsen, 2017). (11) Ligorio Márquez Formation (Eocene), Chile (Terada et al., 2006). (12) Ligorio Márquez Formation (Eocene), Chile (Carpenter et al., 2018) (13) ‘Forest Bed’ (Miocene), West Point Island, Falkland (Malvinas) Islands (Poole and Cantrill, 2007). (14) Seymour Island (Cretaceous), Antarctica (Pujana et al., 2018).

Here, we build on an earlier study (Jud et al., 2018a) by describing a second extinct species of Cunoniaceae from fossil flowers collected from the Salamanca Formation (earliest Palaeocene, ~64 Mya) in Patagonia, Argentina. The fossils have a combination of character states that indicates a close relationship with the syncarpous members of Cunoniaceae. We use phylogenetic analyses to explore the relationships of this new species and of Lacinipetalum spectabilum (Jud et al., 2018a) to other living and extinct members of the family. Finally, we discuss the implications of the co-occurrence of these two species at an early Palaeocene site in Patagonia for understanding the diversification of Cunoniaceae.

MATERIALS AND METHODS

Geological setting

The Salamanca Formation crops out in the San Jorge Basin in Patagonia, Argentina. It consists primarily of estuarine and shallow marine deposits and yields abundant plant micro- and megafossils (Berry, 1937; Romero, 1968; Petriella, 1972; Iglesias et al., 2007; Brea et al., 2008; Zucol et al., 2008; Futey et al., 2012; Jud et al., 2017, 2018a, b; Ruiz et al., 2017; Andruchow-Colombo et al., 2019; Hermsen et al., 2019). The Salamanca Formation overlies the Cretaceous Chubut Group and underlies the Palaeocene–Eocene Río Chico Group (Clyde et al., 2014; Comer et al., 2015). The fossils described here were collected from the Palacio de los Loros-2 (PL-2) locality in the lower part of the formation in south-eastern Chubut Province (Iglesias et al., 2007). The age of the PL-2 locality is constrained to geomagnetic polarity chron C28n. Comer et al. (2015) dated this chron to 64.67–63.49 Ma (early Danian) on the 2012 Geomagnetic Polarity Timescale, but the age of the lower boundary was revised to 64.535 ± 0.040 Ma by Clyde et al. (2016). This site yields an allochthonous assemblage of leaves, fruits and flowers, but so far Cunoniaceae have not been identified among the dicot leaves (Iglesias et al., 2007). The fossils are preserved in a grey clay shale that is interpreted as a swale between point-bar ridges of a tidally influenced fluvial channel that meandered across the coastal flats (Comer et al., 2015).

All necessary permits were obtained for this study, which complied with all relevant regulations. Coordinates for the locality are on file at the Museo Paleontológico Egidio Feruglio (MEF), Trelew, Chubut, Argentina.

Fossil preparation

The fossils were collected over the course of four field seasons (2005, 2009, 2011 and 2012) and are curated at the Palaeobotanical Collection of the Museo Paleontológico Egidio Feruglio (MPEF-Pb), Trelew, Chubut, Argentina. We captured images of macroscopic features with a Canon EOS 7D DSLR camera and microscopic details were photographed with a Nikon DS Fi1 camera mounted on a Nikon SMZ1000 stereoscope at the MEF. We used epifluorescence microscopy to examine the anthers for preserved pollen grains. We captured images of fossil and modern pollen grains with a Jeol NeoScope JCM-5000 scanning electron microscope at the Paleontological Research Institute (PRI), Ithaca, NY, USA. We processed the images using whole-image manipulations only with Adobe Photoshop CC 2017 (San Jose, CA, USA).

Molecular data

We began by obtaining the trnL–F and rbcL sequence data used by Bradford and Barnes (2001) from GenBank. We modified the dataset to include additional trnL–F and rbcL sequence data from GenBank. We also modified the dataset to reflect changes to the taxonomy since the work of Bradford and Barnes (2001), including the synonymy of Acsmithia Hoogland with Spiraeanthemum A.Gray (Pillon et al., 2009), the segregation of Karrabina Rozefelds & H.C.Hopkins from Geissois Labill. (Hopkins et al., 2013) and the rediscovery of Hooglandia ignambiensis (McPherson and Lowry, 2004). We used one exemplar species for each section of Weinmannia (Bradford, 2002). Next, we searched for additional informative sequences available on GenBank using the BLAST search tool and obtained matK and the trnH–psbA intergenic spacer region sequences for nine and seven species, respectively (Table 1).

Table 1.

GenBank accession numbers for each sequence used in the phylogenetic analyses

Term tRNA-Leu (trnL) trnL c–d trnL–F intergenic spacer trnL e–F rbcL matK trnH–psbA
Ackama rosifolia AF299162 AF299215 KT626660 NA NA
Acrophyllum australe AF299168 AF299221 AF291926 NA NA
Anodopetalum biglandulosum AF299175 AF299228 AF291932 NA NA
Bauera rubioides AF299183 AF299236 L11174.2 NA NA
Bauera sessiliflora AF299184 AF299237 NA NA NA
Brunellia colombiana AF299181 AF299234 AF291937 NA NA
Brunellia oliveri AF299182 AF299235 AF291938 NA NA
Caldcluvia paniculata AF299163 AF299216 AF291922 NA NA
Callicoma serratifolia AF299170 AF299223 AF291928 KM894952 NA
Ceratopetalum apetalum NA NA KM895900 KM894747 KM895248
Ceratopetalum gummiferum AF299176 AF299229 L01895 NA NA
Codia discolor AF299171 AF299224 AF291929 NA NA
Cunonia atrorubens AF299154 AF299207 AF291918 NA NA
Cunonia capensis AF299156 AF299209 NA JX517913 NA
Davidsonia jerseyana AF299185 AF299238 AF206759 AY935930 NA
Davidsonia johnsonii AF299186 AF299239 KM895905 NA KM895252
Eucryphia cordifolia AF299173 AF299226 AF291931 KF224980 NA
Eucryphia moorei AF299174 AF299227 NA NA NA
Geissois superba AF299166 AF299219 NA NA NA
Gillbeea adenopetala AF299169 AF299222 AF291927 NA NA
Hooglandia ignambiensis AY549639 AY549640 AY549641 NA NA
Karrabina benthamiana AF299165 AF299218 AF291924 NA KM895230
Lamanonia ternata JX236029 JX236029 JX236032 MG833493 KF421056
Opocunonia nymanii NA NA MH826693 NA MH826497
Pancheria engleriana AF299158 AF299211 AF291919 NA NA
Platylophus trifoliatus AF299177 AF299230 AF291933 JX517817 NA
Pseudoweinmannia lachnocarpa AF299167 AF299220 AF291925 NA NA
Pullea glabra AF299172 AF299225 AF291930 NA NA
Schizomeria ovata AF299178 AF299231 KM895629 KM894933 KM895087
Schizomeria serrata JX236028 JX236028 JX236031 NA NA
Spiraeanthemum samoense AF299180 AF299233 AF291936 NA NA
Spiraeanthemum ellipticum EU867222 EU867222 AF291935 NA NA
Spiraeopsis celebica AF299164 AF299217 AF291923 NA NA
Vesselowskya rubifolia AF299160 AF299213 AF291920 NA NA
Weinmannia bangii AF299145 AF299198 AF291915 NA NA
Weinmannia fraxinea AF299149 AF299202 NA AM889750 GQ248402
Weinmannia madagascarensis AF299152 AF299205 AF291916 NA NA
Weinmannia minutiflora AF299150 AF299203 NA NA NA
Weinmannia raiateensis AF291917 NA GQ248402
Lacinipetalum spectabilum NA NA NA NA NA
Cunoniantha bicarpellata NA NA NA NA NA
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We used Brunelliaceae (represented by Brunellia colombiana Cuatrec. and B. oliveri Britton) as the outgroup. Cunoniaceae form a clade with Brunelliaceae, Cephalotaceae and Elaeocarpaceae (Moody and Hufford, 2000; Bradford and Barnes, 2001; Sun et al., 2016; Valencia et al., 2020), but the sister taxon of Cunoniaceae is unclear. We did not use Cephalotaceae because they are morphologically specialized herbaceous pitcher plants and we did not use Elaeocarpaceae because the alignment of the trnL–F sequences with Cunoniaceae was ambiguous.

We aligned each locus independently using MUSCLE v. 3.8.31 in Aliview v. 1.18 (Larsson, 2014). The final concatenated matrix of sequence data (Supplementary Data NEXUS file) consists of the trnL intron (36 species, positions 1–618), the trnL–F intergenic spacer (36 species, positions 619–1167), rbcL (31 species, positions 1168–2638), matK (9 species, positions 2639–4151) and trnH–psbA (7 species, positions 4152–4752).

Morphological data

We examined the matrix of morphological characters used by Bradford and Barnes (2001) and modified several characters. Leaf arrangement is treated as unordered to remove any assumption about how this character evolves. Marginal tooth vascularization was replaced with secondary vein framework following Ellis et al. (2009). The stipule characters are modified from present/absent and lateral/interpetiolar/axillary to a single character where the various stipule types are considered alternative states along with the absence of stipules (Rutishauser and Dickison, 1989; Dickison and Rutishauser, 1990). We replaced the character of petal morphology (entire/incised) with a more complex set of four states to reflect the diversity of venation, shape, and type of incision across the family: ovate to obovate and single veined/large multiveined–obovate/flabellate incised/retuse. We used these new character states because we doubt the homology between the pattern of petal incision in Schizomerieae (Barnes and Rozefelds, 2000; Rozefelds and Barnes, 2002; Hopkins, 2018) and the retuse glandular petals of Gillbeea F.Muell. (Endress and Matthews, 2006). We also added new characters. These include winged rachis (absent/present), diffuse axial parenchyma in the wood (absent/present), irregular discontinuous bands of axial parenchyma in the wood (absent/present), regular bands of axial parenchyma in the wood (absent/present), number of parts per perianth whorl, number of stamens, anther attachment, number of carpels, texture of the ovary, type of stigma and accrescent calyx. We circumscribed character states with the aims of limiting polymorphic terminals and identifying clear discontinuities in interspecific variation. We coded the character states using descriptions and illustrations available in the literature and with herbarium specimens at the L. H. Bailey Hortorium Herbarium (BH), Cornell University, Ithaca, NY, USA (Supplementary Data Table S1). Missing data associated with the fossil taxa are unknown because the flowers have not yet been matched to co-occurring fossilized leaves, wood or fruits. All characters are treated as unordered. The final dataset comprises 41 taxa and 58 morphological characters. The character descriptions and morphological matrix are available online at the Morphobank website (www.morphobank.com; project P2600, matrix 26123).

Search strategy: parsimony analysis

We concatenated the molecular and morphological matrices using the ‘new matrix merge’ function in Winclada v. 1.99 spawned through ASADO version 1.99 (Nixon, 2008). The resulting matrix includes 41 taxa and 4810 total characters. Of these, 340 characters are parsimony-informative. We omitted all non-informative characters to optimize calculation of branch support values. To minimize a priori assumptions about character evolution and character importance, all characters were equally weighted and unpolarized. We conducted a tree search using NONA version 2.0 (Goloboff, 1999) spawned through ASADO version 1.99 (Nixon, 2008) using the following parameters: ‘hold 1000; mult*100; hold/100’, using the unconstrained ‘mult*max*’ search strategy. Bootstrap support values and jackknife values for branches were estimated by employing 1000 replicates, ten search pseudoreplicates and ten starting trees per pseudoreplicate. We then mapped the support values onto those branches also present in the strict consensus of the the most parsimonious trees.

RESULTS

Systematics

Order

Oxalidales Heintze.

Family

Cunoniaceae R.Br.

Genus

Cunoniantha Jud & Gandolfo gen. nov.

Type species

Cunoniantha bicarpellata Jud & Gandolfo sp. nov. (Figs 3 and 4A, B).

Fig. 3.

Fig. 3.

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Longitudinal views of 35TCunoniantha bicarpellata Jud & Gandolfo gen. et sp. nov.35T specimens from PL-2 locality, Salamanca Formation. (A) Flower with pedicel, remains of petals (black arrowhead), filaments (white arrow), and a superior syncarpous ovary with two diverging styles (white arrowheads). MPEF-Pb 8523a. (B) Flower showing five anthers (arrows). MPEF-Pb 8545. (C) Flower attached to a partial possible thyrsoid/cymiform inflorescence. Note the abscission zone where the terminal flower is attached (at arrow) and the scars where other flowers or bracts were attached (at arrowheads). MPEF-Pb 8533. (D) Flower showing the pedicel, calyx (black arrows), petals (black arrowheads), filaments (white arrow) and a superior ovary. MPEF-Pb 8530b. (E) Counterpart of (D) showing pedicel, calyx (black arrow), petals (black arrowheads), filaments (white arrow) and a superior ovary with two parallel styles (white arrowhead). MPEF-Pb 8530a. (F) Close-up of (E) showing the pubescent ovary (black arrow). Scale bars: A–E = 3.0 mm; F = 1.0 mm.

Fig. 4.

Fig. 4.

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Anther of 35TCunoniantha bicarpellata Jud & Gandolfo, gen et sp. nov. 35Tand scanning electron microscope micrographs of fossil and pollen of modern Cunoniaceae. (A) Close-up of an anther showing the longitudinal dehiscence slits and the absence of a connective extension. MPEF-Pb 8541a. (B) Two pollen grains 35Twith finely reticulate tectum35T (at arrows) preserved within the anthers of 35TCunoniantha bicarpellata. MPEF-Pb 35T97335T. (C) Prolate, tricolpate pollen grain Weinmannia glabra L.f. Note the perforate tectum. BH 000 054 033. (D) Prolate, tricolpate pollen grain Weinmannia glabra. Note the finely reticulate tectum. BH 000 054 033. (E) Oblate, tricolpate pollen grains of Opocunonia nymanii Schultr. See the finely reticulate tectum. BH 000 046 024. Scale bars: A = 0.5 mm, B = 10 µm, C35T–E = 5 µm.

Generic diagnosis

Flowers pedicellate, perfect, hypogynous, actinomorphic, with two perianth whorls of five organs; sepals ovate, inserted at the margin of the floral disc; petals obovate, entire, and equal to or greater than the length of the sepals; androecium of five stamens in one cycle, alternipetalous, anthers dorsifixed, without a connective extension, thecae with longitudinal dehiscence, pollen tricolpate, prolate and reticulate; gynoecium superior, bicarpellate, syncarpous with two free styles; stigmas non-capitate, ovary pubescent.

Specific diagnosis

As for the genus Cunoniantha.

Etymology

The name Cunoniantha refers to the morphology of the flowers typical of the syncarpous Cunoniaceae, and the epithet refers to the bicarpellate gynoecium.

Holotype

35MPEF-Pb 8523a, b.

Repository

Museo Paleontológico Egidio Feruglio Paleobotany Collection (MPEF-Pb), Trelew, Chubut, Argentina.

Type locality

Palacio de Los Loros-2 (PL-2), Chubut, Argentina.

Stratigraphic position and age

Lower Salamanca Formation; Palaeocene, early Danian (Clyde et al., 2014; Comer et al., 2015).

Description

The flowers are perfect, actinomorphic, and borne on a pedicel ~5.8 mm long (5.0–7.9 mm) (Fig. 3). Most flowers were recovered isolated, but one is attached to an axis with sub-opposite lateral scars (Fig. 3C) indicating that the flowers were borne on an inflorescence. Inflorescence type is variable in Cunoniaceae, but this fragment is more consistent with a thyrsoid or cymiform inflorescence structure than a capitate, racemose or paniculiform structure. The perianth is composed of calyx and corolla, each with five parts and whorled phyllotaxis. The sepals are free and ovate, their bases are broadly attached at the rim of the floral cup and their apices are acute and straight. Sepals are 4.5 mm long by 2.0 mm wide (n = 9) (Fig. 3A). The petals are alternisepalous, narrow, 0.8–1.5 mm wide and 3.4–3.8 mm long, slightly obovate, and entire with a single midvein (Fig. 3D, E). Individual specimens have up to five stamens preserved (Fig. 3B); the stamen filaments taper from the base towards the anther and are 2.8–3.9 mm long (Fig. 3B); the anthers are dorsifixed, introrse, and versatile with longitudinal dehiscence along a ventral slit, ~1.1 mm long by 0.9 mm wide (n = 5) (Figs 3A and 4A). They contain prolate, tricolpate pollen grains (18 µm × 12 µm; n = 3) with a reticulate tectum (Fig. 4A, B). The gynoecium is superior, bicarpellate, and syncarpous with two free diverging styles (Fig. 3A, B). The ovary is pubescent (Fig. 3F), 2.4 mm long by 1.7 mm wide (n = 7). The styles are ~2.1 mm long (n = 5) and have indistinct stigmas (Fig. 3A, B, D). At the base of the gynoecium in many specimens there are abundant coalified remains, suggestive of an annular or segmented floral disc (Fig. 3A, B, D). Floral formula: *Ca5 Co5 A5G(2).

Material examined

MPEF-Pb 8522, 8523, 8527, 8529, 8530, 8533, 8534, 8536, 8540, 8541, 8542, 8545, 9731, 9732, 9733.

Phylogenetic analyses

Parsimony analysis yielded 92 equally short trees of 748 steps (Fig. 5). The consistency index is 0.56 and the retention index is 0.69. In all trees, Cunoniantha is nested in the ‘core Cunoniaceae’ clade of Bradford and Barnes (2001), but outside the tribes. Lacinipetalum is sister to extant members of Schizomerieae in all trees. Bootstrap support values are generally low around the position of the fossil species, but this is typical when including taxa with a high proportion of missing data (Fig. 5).

Fig. 5.

Fig. 5.

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Strict consensus of 92 most parsimonious trees based on simultaneous analysis of rbcL, trnL–F, matK and trnH–psbA sequence data and morphology. Note the positions of the fossil taxa within crown-group Cunoniaceae indicated by the daggers (†). Numbers above the branches are bootstrap support values followed by jackknife support values. Clades indicated by grey shading are tribes.

DISCUSSION

The position of Cunoniantha

Character states that support the placement of Cunoniantha within Cunoniaceae include a pentamerous, actinomorphic perianth with free sepals and petals, dorsifixed versatile anthers with longitudinal dehiscence, reticulate tricolpate pollen <20 μm long in maximum diameter (e.g. Fig. 4C–E), and a superior syncarpous bicarpellate gynoecium with two free styles and non-capitate stigmas (Bradford et al., 2004). Cunoniaceae are morphologically diverse; identification of morphological synapomorphies that apply to flowers across the entire family is challenging. Nonetheless, the combination of character states preserved in Cunoniantha falls within the range of variation for Cunoniaceae. Similar flowers occur in Saxifragaceae (Hideux and Ferguson, 1976; De Craene, 2010); however, Saxifragaceae are characterized by some combination of clawed petals, basifixed anthers and capitate stigmas (Soltis, 2007). These features are not present in Cunoniantha. Saxifragaceae are also less likely to be fossilized because they are herbaceous, and they are relatively recent arrivals to Patagonia (Deng et al., 2015). Matthews et al. (2001) found numerous similarities between Cunoniaceae and Anisophylleaceae, but flowers with bicarpellate gynoecia are exceptional in Anisophylleaceae, whereas this is the typical condition in most Cunoniaceae and in Cunoniantha.

The combination of undissected petals, only five stamens per flower, anthers without a thecal connective protuberance, and a thyrsoid/cymiform inflorescence structure observed in Cunoniantha does not match any extant genus. Nor does it match any of the previously described fossil genera that have been compared with Cunoniaceae (Matthews et al., 2001; Schönenberger et al., 2001; Poinar et al., 2008; Chambers et al., 2010; Poinar and Chambers, 2017, 2019; Jud et al., 2018a). Nonetheless, the results of our phylogenetic analysis indicate that Cunoniantha is nested within the syncarpous Cunoniaceae (Supplementary Data Fig. S1) and among the predominantly bicarpellate lineages (Supplementary Data Fig. S2). Bradford and Barnes (2001) recognized a ‘core Cunoniaceae’ clade that excludes Schizomerieae, Davidsonia and Bauera, but includes Eucryphia and is united by a shared deletion in the trnL–F spacer region (Fig. 1). More recent analyses also resolve this clade using maximum likelihood and Bayesian inference (Sweeney et al., 2004; Hopkins et al., 2013). Our analysis places Cunoniantha among this ‘core Cunoniaceae’ clade (Fig. 5).

The position of Lacinipetalum

Jud et al. (2018a) included the fossil Lacinipetalum spectabilum in a phylogenetic analysis of Schizomerieae with Davidsonia as the outgroup. In that analysis, Lacinipetalum was recovered as sister to Schizomerieae. We included Lacinipetalum in this broader analysis for three reasons. First, we updated some of the characters in this new analysis based on available data from the literature and a broader examination of morphological variation in the family (see Materials and methods section). Second, the absence of petals in Davidsonia means that it does not provide polarization for the characters related to the corolla that are preserved in the Lacinipetalum (Supplementary Data Fig. S3). Third, by using an ingroup consisting only of the fossil and extant Schizomerieae, Jud et al. (2018a) evaluated the most parsimonious position of Lacinipetalum within Schizomerieae, not the hypothesis that Lacinipetalum is more closely related to Schizomerieae than to other tribes. Indeed, this new analysis confirms a close relationship between Lacinipetalum and Schizomerieae (Fig. 5).

Biogeography and diversification of Cunoniaceae

Several extant genera in Cunoniaceae likely had broader distributions during the Palaeogene when the climate was warmer and wetter in Patagonia and when Australia was further south. These include Ceratopetalum Sm. (Holmes and Holmes, 1992; Barnes and Hill, 1999a; Gandolfo and Hermsen, 2017), Callicoma Andrews (Barnes and Hill, 1999b), Codia J.R.Forst & G.Forst (Barnes and Hill, 1999b), Eucryphia (Hill, 1991; Barnes and Jordan, 2000), Spiraeanthemum (Carpenter and Pole, 1995; Barnes et al., 2001) and Weinmannia (Carpenter and Buchanan, 1993; Barnes et al., 2001). The presence of Ceratopetalum, Eucryphia and Spiraeanthemum by the middle Eocene implies either a Cretaceous origin of crown-group Cunoniaceae or rapid diversification during the Palaeogene. Heibl and Renner (2012) presented the results of an analysis calibrated with early Eocene Eucryphia fossils (Barnes and Jordan, 2000) showing a late Eocene or younger divergence for most of the tribes in Cunoniaceae (except Spiraeanthemieae); however, given the Eocene–early Oligocene fossil occurrences discussed above, their ages are likely underestimates.

With the exception of the early Eocene Ceratopetalum (Gandolfo and Hermsen, 2017), most Upper Cretaceous and Palaeogene fossils from Patagonia and Antarctica assigned to Cunoniaceae are not included in any extant genus (Table 2). Nonetheless, fossil pollen from Upper Cretaceous and early Palaeogene sites across South America (Archangelsky, 1973; Romero and Archangelsky, 1986; Troncoso, 1991; Baldoni and Askin, 1993; Zamaloa, 2000; Barreda et al., 2020), Antarctica (Cranwell, 1959; Cantrill and Poole, 2012) and Australia (Kershaw and Sluiter, 1982; Hill and MacPhail, 1983; Christophel et al., 1987; Sluiter, 1991; Macphail, 1997; Alley, 1998; Barnes and Jordan, 2000) indicate that the family was widespread when floristic interchange was still possible without invoking trans-oceanic long distance dispersal. Similarly, fossil woods of Weinmannioxylon Petriella and Eucryphioxylon Poole Mennega & Cantrill are widespread in Upper Cretaceous and Palaeocene deposits in Patagonia (Petriella, 1972; Terada et al., 2006; Raigemborn et al., 2009) and Antarctica (Chapman and Smellie, 1992; Zhang and Wang, 1994; Poole et al., 2000, 2001, 2003; Cantrill and Poole, 2012; Pujana et al., 2018). However, these genera may or may not belong to the crown group. They have suites of plesiomorphic character states for the family including diffuse porosity, scalariform perforation plates, vessel-ray parenchyma pits that are scalariform to opposite, and diffuse axial parenchyma (Ingle and Dadswell, 1956; Dickison, 1980). Fossil leaves similar to Cunoniaceae have also been reported from the Eocene Ligorio Márquez Formation in South America, but these were not identified to genus (Carpenter et al., 2018).

Table 2.

Macrofossils attributed to Cunoniaceae from Antarctica, South America (Australian record summarized by Barnes et al., 2001)

Taxon Organs Age Locality Continent Reference Latitude Longitude
Eucryphiaceoxylon eucryphioides Wood Eocene King George Island (8) Antarctica Poole et al., 2001 −62.17 −59.07
Eucryphiaceoxylon eucryphioides Wood Cretaceous-Eocene? Seymour Island (7) Antarctica Poole et al., 2003 −64.2784 −56.7324
Eucryphiaceoxylon eucryphioides Wood Upper Cretaceous James Ross Island (14) Antarctica Pujana et al., 2018 −63.898 −57.948
Weinmannioxylon ackamoides Wood Palaeocene King George Island (5) Antarctica Zhang and Wang, 1994 −62.33 −58.45
Weinmannioxylon nordenskjoeldii Wood Upper Cretaceous Williams Point (1) Antarctica Poole et al., 2000 −62.475 −60.137
Weinmannioxylon trichospermoides Wood Upper Cretaceous James Ross Island (14) Antarctica Pujana et al., 2018 −63.876 −57.906
Weinmannioxylon sp. Wood Neogene Falkland Island (13) South America Poole and Cantrill, 2007 −51.35 −60.66
cf. Weinmannioxylon Wood Middle Eocene Arroyo Cardenio River (11) South America Terada et al., 2006 −46.763 −71.775
Weinmannioxylon multiperforatum Wood Palaeocene Peñas Coloradas (3) South America Raigemborn et al., 2009 −46.82 −69
Weinmannioxylon multiperforatum Wood Palaeogene Chubut (4) South America Petriella, 1972 −43.65 −67.71
Weinmannioxylon pluriradiatum Wood Palaeogene Chubut (4) South America Petriella, 1972 −43.65 −67.71
Ceratopetalum edgaroromeroi Fruit Eocene Laguna del Hunco (10) South America Gandolfo and Hermsen, 2017 −42.461 −70.037
undetermined Cunoniaceae Leaf Middle Eocene Río Zeballos (12) South America Carpenter et al., 2018 −46.834 −71.856
Cunoniantha bicarpellata Flower Palaeocene PL-2, Chubut (2) South America This study −45.912 −69.214
Lacinipetalum spectabilum Flower Palaeocene LF, Chubut (2) South America Jud et al., 2018a −45.69 −68.611
Lacinipetalum spectabilum Flower Palaeocene PL-2, Chubut (2) South America Jud et al., 2018a −45.912 −69.214
Lacinipetalum spectabilum Flower Palaeocene PL-5, Chubut (2) South America Jud et al., 2018a −45.909 −69.226
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Numbers following each locality correspond to points on the map in Fig. 2.

The discovery of Cunoniantha and Lacinipetalum from the early Palaeocene of Argentine Patagonia provides strong evidence that the diversification of crown-group Cunoniaceae was under way by 64 Mya. Although both genera are extinct, our phylogenetic analysis indicates that they belong to two different clades within the syncarpous Cunoniaceae. Together with other occurrences of fossil wood, pollen and Eucryphia leaves discussed above (Table 2), these fossils also indicate that the family was widespread across Gondwana by the Palaeocene, when warm climates permitted floristic exchange between South America and Australia via Antarctica (Hallam, 1995; Sanmartín and Ronquist, 2004; Cantrill and Poole, 2012; Wilf et al., 2013).

Evidence from fossil mammals suggests the land connection between South America and Antarctica was severed during the late Palaeocene or early Eocene (Reguero et al., 2014). Climate deterioration associated with global cooling and eventually deep-water currents through the Drake Passage (Lawver and Gahagan, 2003; Livermore et al., 2007; Eagles and Jokat, 2014) rendered the Antarctic peninsula inhospitable to Cunoniaceae by the mid-Eocene (Anderson et al., 2011). It appears that Cunoniaceae grew on the Falkland (Malvinas) Islands until at least the Miocene, but the age of these fossils is poorly constrained (Poole and Cantrill, 2007). During the late Palaeogene and Neogene, much of Patagonia also became increasingly moisture-limited (Palazzesi et al., 2014; Dunn et al., 2015). Suitable habitat for Cunoniaceae in South America retreated northward with the montane forests of the rising Andes. This dramatic reduction in available habitat area could explain the loss of some Cunoniaceae from South America, whereas Lamanonia, Weinmannia, Eucryphia and Caldcluvia survive.

Conclusions

Cunoniantha bicarpellata exhibits a mosaic of features consistent with Cunoniaceae. Phylogenetic analysis of morphological and molecular characters supports its position within crown-group Cunoniaceae among the syncarpous lineages. This is the second genus of Cunoniaceae from the Salamanca Formation described from fossilized flowers. Based on our phylogenetic analysis, Cunoniantha and Lacinipetalum together provide the oldest evidence of crown-group Cunoniaceae worldwide and show that the diversification was under way by 64 Mya.

SUPPLEMENTARY DATA

Supplementary data are available online at https://academic.oup.com/aob and consist of the following. Table S1: herbarium specimens at the L. H. Bailey Hortorium Herbarium, Cornell University, Ithaca, NY, USA, examined for this study. NEXUS file: character matrix (trnL intron, trnL–F intergenic spacer, rbcL, matK, trnH–psbA). Figure S1: one of the most parsimonious trees showing the distribution of carpel number in Cunoniaceae. Figure S2: one of the most parsimonious trees showing the distribution of apocarpy and syncarpy in Cunoniaceae. Figure S3: one of the most parsimonious trees showing the distribution of petal type in Cunoniaceae.

mcaa154_suppl_Supplementary_Figure_S1
Click here for additional data file. (281.5KB, png)
mcaa154_suppl_Supplementary_Figure_S2
Click here for additional data file. (278.7KB, png)
mcaa154_suppl_Supplementary_Figure_S3
Click here for additional data file. (290.3KB, png)
mcaa154_suppl_Supplementary_Files
Click here for additional data file. (187.5KB, txt)
mcaa154_suppl_Supplementary_Table_S1
Click here for additional data file. (12.1KB, xlsx)

ACKNOWLEDGEMENTS

The authors thank A. Iglesias, P. Wilf, P. Puerta, K. Johnson, M. Caffa, L. Canessa and many others for collecting the fossils. Thanks to the Secretaría de Cultura and Secretaría de Turismo y Areas Protegidas from Chubut Province, A. Balercia, Bochatey family, H. Visser and E. de Galáz for facilitating land access; and the Autoridad de Aplicación de la Ley de Patrimonio Paleontológico Argentino Ley 25,743 (Museo Argentino de Ciencias Naturales Bernardino Rivadavia, MACN) for permits in early stages of this work. The authors also thank E. Ruigomez and L. Reiner for assistance working with collections at 35TMuseo Paleontológico Egidio Feruglio (MEF) and fossil preparation. Thanks to the Paleontological Research Institute, Ithaca, NY, and B. Anderson for access to their scanning electron microscope, and personnel of the L. H. Bailey Hortorium Herbarium (BH), Cornell University. Thanks to K. C. Nixon (Cornell University) and to M. P. Simmons (Colorado State University) for constructive comments on an earlier version of the manuscript and to the reviewers and editor for suggestions that improved the manuscript. The authors declare no competing interests. Locality data and specimens are available in the Palaeobotanical Collection at the MEF, Trelew, Argentina. The matrix of morphological data is available on Morphobank (www.morphobank.org project P2600, matrix 24915).

FUNDING

This work was supported by the National Science Foundation (grant numbers DEB-1556136, DEB-0918932, DEB-1556666, DEB-0919071, DEB-0345750, EAR-1925552, and EAR-1925755) and the Fulbright Foundation (M.A.G.).

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mcaa154_suppl_Supplementary_Table_S1
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