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Eocene lantern fruits from Gondwanan Patagonia and the early origins of Solanaceae

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Science  06 Jan 2017:
Vol. 355, Issue 6320, pp. 71-75
DOI: 10.1126/science.aag2737

Shedding light on fossil lantern fruit

The Solanaceae (or nightshades) are one of the best-studied plant families, yet their evolutionary origins have thus far been relatively obscure. Corroborative fossil evidence of molecular phylogenetic divergence dates has been lacking. Wilf et al. present 52-million-year-old fossils of lantern fruits from Argentina, which they ascribe to the modern genus Physalis. These fossil finds suggest a much earlier origin of the lantern fruit lineage and indicate that the Solanaceae may have diversified before the final breakup of the Gondwanan supercontinent.

Science, this issue p. 71

Abstract

The nightshade family Solanaceae holds exceptional economic and cultural importance. The early diversification of Solanaceae is thought to have occurred in South America during its separation from Gondwana, but the family’s sparse fossil record provides few insights. We report 52.2-million-year-old lantern fruits from terminal-Gondwanan Patagonia, featuring highly inflated, five-lobed calyces, as a newly identified species of the derived, diverse New World genus Physalis (e.g., groundcherries and tomatillos). The fossils are considerably older than corresponding molecular divergence dates and demonstrate an ancient history for the inflated calyx syndrome. The derived position of these early Eocene fossils shows that Solanaceae were well diversified long before final Gondwanan breakup.

The Solanaceae, an angiosperm family of ~2500 species and 100 genera, include some of the world’s most economically valuable and historically important crops such as potatoes, tobacco, tomatoes, eggplants, and peppers (1). The family is a source of pharmaceutical compounds and model organisms (e.g., tobacco, tomato, and petunia) and is known for its diverse reproductive structures (25). One well-studied feature found in several Solanaceae genera is the inflated calyx syndrome (ICS), in which complex signaling pathways cause the calyx to expand after fertilization and surround the fruit (6, 7), as in tomatillos and other lantern fruits.

Despite increasing interest in the timing and biogeography of Solanaceae evolution (8), the family’s poor fossil record provides little information. There are no valid previous records of fossil flowers, fruits, or leaves of Solanaceae (9). Several Eocene-Pliocene isolated seeds are known, but except for some Oligocene and younger specimens assigned to the large Solanoideae clade, they cannot be placed in derived groups (10). Molecular divergence estimates for the crown group of the family range from ~35 to 51 million years ago (Ma) (11) and, most recently, ~30 Ma, based on intensive taxon sampling and critical use of the available fossils for temporal calibrations (10). Recent estimates of the Solanaceae divergence from Convolvulaceae vary from ~49 to 67 Ma (10, 12, 13). The Solanaceae are thought to have evolved and diversified on late- or post-Gondwanan South America (11, 14), which is the family’s center of diversity today (1). Nevertheless, Miocene wood from Argentina (15) has been the only physical evidence of its South American history.

We present here two compressed fossil lantern fruits (Fig. 1) with angled, five-lobed, inflated calyces from terminal-Gondwanan South America that preserve diagnostic features of the derived, diverse (>120 species) New World Solanaceae genus Physalis. One fossil (Fig. 1, A to C) is elongate and preserves a slender pedicel, one meridional primary vein per lobe, and four of the five lobe tips; the coalified remains of the berry fill the width of the calyx, revealed by the cleavage plane cutting just under part of the calyx surface. The second specimen (Fig. 1, G and H) is more rounded, is basally well invaginated, and preserves five lobes; it has lost the pedicel and the berry. As in living Physalis fruits, there are no corolla elements in these specimens; what appear superficially to be corolla components near the bases are instead compressed calycine vein remnants that project into the matrix behind the pedicel, similar to the preservation of some flattened herbarium specimens (Fig. 1I). The two fossils have an identical venation pattern, and comparable variation in aspect ratio and calyx closure is found in several Physalis species (e.g., P. angustifolia) (Fig. 1, D and I). Therefore, we consider the two fossil specimens to belong to the same newly identified species.

Fig. 1 Physalis infinemundi sp. nov. and selected herbarium specimens of Physalis calyces.

(A to C) P. infinemundi holotype, MPEF-Pb 6434a,b. (A) MPEF-Pb 6434a, preserving pedicel attachment, venation compressed into the matrix behind the pedicel, four of the presumed five lobe tips, and the coalified berry revealed by cleavage through the calyx. (B) MPEF-Pb 6434b, preserving a slender pedicel segment. (C) MPEF-Pb 6434a, showing the secondary vein narrowly bifurcating at the arrow, before the lobe sinus visible in (A). (D and E) P. angustifolia, BH 000079053, showing general features and preservation similar to the fossil holotype and secondary vein bifurcation at the arrow (berry dried and shrunken). (F) P. glutinosa, MICH 1295968, showing exposure of the (dried and shrunken) berry via calyx breakage as in (A) and (B). Scale bar, 1 cm. (G and H) P. infinemundi paratype, MPEF-Pb 6435a (G) and 6435b (H), showing invaginated, angled calyx with all five lobes preserved [arrows in (G)], intersecondary veins, and numerous veins compressed into the matrix behind the base. (I) P. angustifolia, MICH 1514118, showing rounded aspect similar to (G) and (H) versus elongate aspect of the same species in (D); compression of veins behind the pedicel (right-hand specimen) similar to both fossils; and distortion effects of flattening under a stem (left-hand specimen) similar to the compression preservation in (G) and (H).

We discovered these fossils at Laguna del Hunco in Chubut, Patagonia, Argentina, an early Eocene caldera-lake, fossil rainforest locality that represents the terminal phase of Gondwana and the global warmth of the early Eocene climatic optimum (16, 17). The assemblage is dominated by Gondwanic taxa with fossil and extant Australasian affinities (1719). There are few reliable previous records from the site of characteristically New World taxa, suggesting minimal linkage of late-Gondwanan and extant South American floras due to cooling and regional extinctions since the late Eocene (19). The minimum age of the fossils is 52.22 ± 0.22 Ma, based on three 40Ar-39Ar dates from closely associated tuffs and two paleomagnetic reversals from the local stratigraphic section (16, 20).

Inflated, five-angled calyces and other features of fruiting Physalis help make it one of the most recognizable angiosperm genera, although calyx expansion, by itself, is plesiomorphic within the family (7, 21, 22). However, several more detailed characters of Solanaceae fruiting calyces are noted for their systematic value (21, 2325). To assess the phylogenetic position of the fossils, we scored a 16-character morphological matrix (table S1) for the fossils and for 109 Solanaceae species from 39 genera that have available genetic data (10, 20) and mostly have inflated or accrescent fruiting calyces (data table S1). We used these morphological data first for a standard taxonomic treatment, then combined them with the species’ DNA sequences (10) to construct a matrix for total evidence analyses using maximum parsimony (MP) (Fig. 2) and maximum likelihood (ML) (fig. S1) (20). We also mapped the morphological characters individually on the strict consensus MP tree (figs. S2 to S17). Limitations of the phylogenetic analysis included the specialized set of morphological characters appropriate for the fossil fruits (without complementary data preserved from other organs) and the proportionally small (~10%) and phylogenetically nonrandom selection of the species in (10) that had suitable calyx features for comparison (20).

Fig. 2 Phylogenetic relationships of Physalis infinemundi sp. nov. and selected Solanaceae species.

Strict consensus of 2835 most parsimonious trees of 3510 steps (CI = 0.438, RI = 0.726), based on a total evidence analysis using morphology and five gene partitions (ITS, waxy, matK, ndhF, and trnL-F; 7070 total characters). Decay indices are included above each branch (20) (higher indices represent stronger support). Labeled major clades follow (10). See the text and supplementary materials (20) for details and fig. S1 for the maximum likelihood tree.

Systematic paleontology: Solanaceae Jussieu 1789. Physalis Linnaeus 1753. Physalis infinemundi Wilf sp. nov. Etymology: Latin, in fine mundi, “at the end of the world,” reflecting provenance from the last stages of the Gondwanan supercontinent and from Patagonia, popularly known as “the end of the world.” Type material: repository Museo Paleontológico Egidio Feruglio, Trelew, Argentina (MPEF-Pb); holotypus hic designatus MPEF-Pb 6434a,b (Fig. 1, A to C) (lowercase letters indicate part and counterpart), from Laguna del Hunco, Huitrera Formation, early Eocene, Chubut Province, Argentina, quarry LH13 (16), collected 7 December 2002 (fig. S18); paratype MPEF-Pb 6435a,b (Fig. 1, G and H), Laguna del Hunco quarry LH04 (16), 21 November 2006. Description: based on two dispersed, apparently mature, compressed fruiting calyces; only the holotype preserves berry and pedicel remains. Pedicel preserved length 18.8 mm, width 1 mm at inflection point of insertion. Calyx basally invaginated, highly inflated to completely surround the berry, five-lobed, angled, partly open at apex, length by width 25.2 mm by 13.2 mm (1.9:1) on holotype, 21.6 mm by 17.6 mm (ratio 1.2:1) on paratype. Calyx lobes equally sized, sinuses angular and incised one-quarter to half the total calyx length, tips acute triangular. Venation with one robust primary meridional vein per lobe, terminating at lobe apex and alternating with secondary veins. Secondary veins arising near the base, visually distinct from the primaries and other vein orders, and bifurcating close to the lobe sinuses (Fig. 1C). Intersecondary veins arising near the base, visually distinct from secondaries and tertiaries, dichotomizing into the random, irregular reticulum of tertiary through at least quinternary veins that fill most of the vein field. Some basal veins compressed into partial detachment from the calyx body, the remnants visible against the matrix. Berry round, flattened and coalified from fossilization, filling the full width of the calyx and appearing by surface relief to extend apically almost to the lobe sinuses; seeds not preserved.

The fossils preserve several features that, together, are diagnostic of the Physalinae clade of Solanaceae (20, 21, 23, 25). These include the highly inflated, lantern-shaped, pedicellate, five-parted, angled, regular calyces covering a large, fleshy berry, along with the combination of (i) invaginated base, (ii) robust primary veins that terminate in the lobe tips (not the lobe sinuses), and (iii) secondary veins that fork before the sinus. Nonphysaline species of Solanaceae with ICS lack some or all of these three features (e.g., those in Deprea, Nicandra, Solanum, Withania, and the Juanulloeae clade) (figs. S5, S11, and S13) (23, 24). Within Physalinae, there are several problematic species of Physalis s.l. and other genera that diverge below the core Physalis clade (Fig. 2) (equivalent to P. subgenus Rydbergis) of relatively homogeneous species (13, 2325). Among these taxa, Alkekengi officinarum calyces are the most similar to the fossils, but they have a much larger size, consistently rounded shape, and nearly closed apex. Otherwise, each of these basal physaline species structurally differs from the fossils and core Physalis (20, 24, 25) (figs. S2 to S17). All these observations highlight the close relationship of the fossils with core Physalis.

Both the MP and ML results (Fig. 2 and fig. S1) support the fossils’ affinity with Physalinae and Physalis. The newly identified species is placed in Physalinae with strong support in both MP and ML analyses and at a basal polytomy of (MP, weak support) or within (ML, strong support) the crown of core Physalis. Both the MP and ML topologies are generally consistent with and reproduced most major clades from (10), with robust support of the critical Physalinae clade. However, each tree recovered the closely related (10) Iochrominae and Deprea as collapsed into a single clade that also included Nicandra, which has Deprea-like calyx morphology but is not closely related to that genus. Nevertheless, the overall agreement of the MP and ML tree topologies with (10) is notable in light of the limitations of the analysis. Notably, no species from outside Physalinae were misplaced among Physalinae, and no Physalinae species were misplaced into other clades. Considering the unknown additional organs of this extinct species, the incomplete knowledge of calyx morphology in extant Solanaceae, and problematic resolution among extant basal species of Physalinae (13, 25), we suggest that the newly identified species can be used, conservatively, to constrain the divergence of Physalinae to a minimum of 52.2 Ma.

Physalis infinemundi sp. nov. represents a derived lineage of Solanaceae in Gondwanan South America at 52.2 Ma, pushing back considerably the evolutionary timing of the family. Compared with recent molecular divergence estimates (10), these fossils are considerably older than the ~30 Ma crown for the entire Solanaceae family as well as the ~11 Ma divergence of Physalinae. A second recent study similarly placed the Physalinae divergence at only ~9 Ma (13).

Our results reinforce the emerging pattern wherein numerous fossil plant taxa from Gondwanan Patagonia and Antarctica are substantially older than their corresponding molecular dates (26, 27), demonstrating Gondwanan history for groups conjectured to have post-Gondwanan origins under entirely different paleogeographic and paleoclimatic scenarios. Likewise, the derived position of the newly identified fossil species shows that the origins and diversification of Solanaceae must have taken place at a much earlier time than previously thought, considerably before final Gondwanan breakup. Other regions of Gondwana are also likely to have played prominent roles in Solanaceae evolution, especially Antarctica, which has produced other important asterid fossils (27). Moreover, the newly identified fossils directly help to resolve temporal inconsistencies between the evolutionary timing of Solanaceae and its herbivores and mutualists (28). The large fossil berry strongly implicates trophic associations with animals, as seen in extant Physalis (29). Today, Physalis inhabits South, Central, and North America, and Mexico is its center of diversity (2). Thus, the fossils establish a rare link to extant New World floras from late-Gondwanan Patagonian assemblages, whose living relatives are mostly concentrated in the Old World tropics and subtropics.

The discovery of 52.2-Ma fossil inflated calyces demonstrates an ancient history for ICS and implies that the Eocene world was already populated with derived solanaceous reproductive structures. The potential adaptive functions of the inflated calyx are scarcely discussed in the literature (30), but the lakeside rainforest paleoenvironment led us to consider flotation dispersal and protective drying for the berry. Simple kitchen-sink and stream experiments on several Physalis species confirmed that intact calyces hold stable air pockets around the berry, enabling flotation for several days in water and preventing wetting of the berry during rains. These insights suggest potential origins of ICS in ancient humid, riparian environments.

Supplementary Materials

www.sciencemag.org/content/355/6320/71/suppl/DC1

Materials and Methods

Figs. S1 to S18

Table S1

Database S1

References (3175)

References and Notes

  1. Materials and methods are available as supplementary materials.
  2. Acknowledgments: This work was supported by NSF grants DEB-1556666 and DEB-1556136, National Geographic Society grant 7337-02, and the David and Lucile Packard Foundation. We thank M. Donovan, I. Escapa, E. Hermsen, K. Johnson, P. Puerta, L. Reiner, A. Reznicek, E. Ruigomez, M. Smith, T. Su, J. Svitko, E. Wilf, the Nahueltripay family, and many others for field and laboratory assistance; S. Knapp and R. Olmstead for helpful discussions; and two anonymous reviewers for very useful comments. The fossil specimens are curated at Museo Paleontológico Egidio Feruglio, Trelew, Argentina. The morphological matrix developed in this paper is tabulated in the supplementary materials.
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