Physalis infinemundi Wilf

Peter Wilf, Mónica R. Carvalho, María A. Gandolfo & N. Rubén Cúneo, 2017, Eocene lantern fruits from Gondwanan Patagonia and the early origins of Solanaceae, Science 355 (6320), pp. 71-75 : 1-4

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. S 18); 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 2 5.2 mm by 1 3.2 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. 1 C). 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. S 5, S 11, and S 13) ( 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, 23 – 25). 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. S 2 to S 17). All these observations highlight the close relationship of the fossils with core Physalis .

Both the MP and ML results ( Fig. 2 and fig. S 1) 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.

Figures

Fig. 1. Physalis infinemundi sp. nov. and selected herbarium specimens of Physalis calyces. (A to C) P. infinemundi holotype, MPEF-Pb 6434 a, b. (A) MPEF-Pb 6434 a, 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 6434 b, preserving a slen- der pedicel segment. (C) MPEF-Pb 6434 a, showing the secondary vein narrowly bifurcating at the arrow, before the lobe sinus visible in (A). (D and E) P. angustifolia, BH 0 0 0 0 79053, 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 6435 a (G) and 6435 b (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 1 5 1 4 1 1 8, showing rounded aspect similar to (G) and (H) versus elongate aspect of the same species in (D); compression of veins behind the pedicel (righthand 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).

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. S 1 for the maximum likelihood tree.