A review of the Cenozoic fossil record of the genus Zamia L. (Zamiaceae, Cycadales) with recognition of a new species from the late Eocene of Panama - evolution and biogeographic inferences

Abstract

Cycads today comprise 349 accepted species in ten genera (Calonje et al. 2017). The number of cycad species described during the last decade increased significantly as a result of intense fieldwork by botanists. Recent results of phylogenetic studies of cycads suggested a relatively recent, late Miocene radiation of cycad species along with the Paleogene appearance of most of the major clades (genera excluding Cycas L. and Dioon Lindl.) and have challenged the theory of "living fossil cycads" (Nagalingum et al. 2011, Salas-Leiva et al. 2013, Condamine et al. 2015). These studies estimated the divergence of Microcycas-Zamia to the late Eocene-early Oligocene. Zamia, with 77 currently accepted species (Calonje et al. 2017) is the second largest genus of cycads, and is the most morphologically and ecologically diverse genus in the extant Cycadales (Norstog & Nichols 1997). Furthermore it is the most speciose and broadly distributed cycad genus in the New World. The centre of diversity for the genus appears to be northern South America and Central America, as the highest species diversity occurs in Colombia (21 species) and Panama (17 species). Zamia species inhabit a great variety of habitats including areas near mangrove swamps (Zamia roezlii Linden), dry desert-like areas (Zamia encephalartoides D.W. Stev.), coastal sand dunes (Zamia lucayana Britton), 185 A review of the Cenozoic fossil record of the genus Zamia L. (Zamiaceae, Cycadales) with recognition of a new species from the late Eocene of Panamaevolution and biogeographic inferences Boglárka ErdEi, MichaEl calonjE, austin hEndy & nicolas Espinosa Modern Zamia L. is the second largest genus among cycads, however reliably identified fossil occurrences of the genus have so far been missing. Previously, fossil "Zamia" species were established in large numbers on the basis of macromorphological similarity of foliage fragments to living Zamia species. However, a reinvestigation of specimens assigned formerly to Zamia and the relevant literature provided no clear-cut evidence for their assignment to this genus. We investigated a newly recovered fossil specimen from marine sediments of the Gatuncillo Formation, near Buena Vista, Colon Province, Central Panama. It represents the first unequivocal fossil record of the genus confirmed by epidermal as well as macromorphological characters and it is described as Zamia nelliae Erdei & Calonje sp. nov. Foraminiferal and nannoplankton biostratigraphy of the locality indicates a late Eocene to earliest Oligocene age. Morphometric comparison of epidermal features of Z. nelliae with those of modern Zamia species suggests similarity with those of the Caribbean Zamia clade. The fossil record of Zamia from Panama implies that the genus appeared by the end of the Eocene or earliest Oligocene in the Central American-Caribbean region, however, the origin of the genus is still unresolved. The record of Z. nelliae may challenge former concepts on the evolution of Zamia and raises an "intermediate" hypothesis on its origin in the Cent...

A Time-Calibrated Species Tree Phylogeny of the New World Cycad Genus Zamia L. (Zamiaceae, Cycadales)

“…Little is known about its terrestrial origin, but since parts of the Panama Arc were emergent since at least 30 Ma (O'Dea et al 2016), it is possible that leaflets may have been carried by currents from nearby islands or more distant land. Interestingly, the cuticular micromorphology of the Panamanian fossil more closely resembles that of extant Caribbean clade species than that of Central-meridional clade species (Erdei et al 2018). This may imply that the elongated adaxial cuticular cell shape and stomatal band width and ratio found in Caribbean species are ancestral character states.…”

“…The species tree was calibrated using 95% HPD age estimates obtained from a previously published time divergence analysis of the Cycadales based on six fossil calibrations and the birth-death tree prior (Condamine et al 2015), as well as from a recently discovered Zamia fossil (Erdei et al 2018). Prior distributions for all calibrated nodes were conservatively set to uniform using the minimum and maximum age bounds outlined below.…”

“…The age intervals for the tree root node (74.3-147.7 Ma) and the crown node of Zamia (9-22.1 Ma), as well as the maximum age bound (84.5 Ma) for the stem node of Zamia, were set according to the 95% HPD estimates provided by Condamine et al (2015). The minimum age bound for the stem group of Zamia was constrained to the minimum age estimate (33 Ma) of a fossil cycad leaflet of unknown terrestrial origin recently found preserved in marine sediments of the Gatuncillo Formation in Central Panama, which is as-signable to Zamia based on cuticular micromorphology (Erdei et al 2018). The fossil age is considered to be 35-33 Ma based on nannoplankton and foraminiferal biostratigraphy, and the minimum age estimate (33 Ma) was used to constrain the minimum age bound for the stem group of Zamia.…”

“…Historical biogeography of Zamia. Inferring the historical biogeography of Zamia with any certainty is burdened by an extremely poor fossil record consisting of a single fossil that can be unequivocally assigned to Zamia based on morphological and epidermal characters (Erdei et al 2018). The fossil, estimated to be of late Eocene to earliest Oligocene age , was found in marine sediments in central Panama.…”

Peer Review #2 of "The complete chloroplast genome of Microcycas calocoma (Miq.) A. DC. (Zamiaceae, Cycadales) and evolution in Cycadales (v0.1)"

“…This suggests a possible northward migration of Zamia from South America and that members of Zamiaceae and putative Stangeriaceae were widespread in Patagonia during the Early Cretaceous (Passalia et al, 2010). Other fossil cycad taxa include genera Dioonopsis found in Northeast Japan (Horiuchi and Kimura, 1987) and western North America (Erdei et al, 2012), Encephalartites (Takimoto and Ohana, 2015) in Northeast Japan, Crossozamia in Taiyuan, China (Gao and Thomas, 1989), Antarcticycas in Antarctica (Smoot et al, 1985) and Zamia fossil species discovered in Panama (Erdei et al, 2018). Most of these fossil discoveries were found to be morphologically linked to extant cycads under Zamiaceae, providing plausible explanations to the diverse morphological characters observed in Zamiaceae species compared to the more conserved characters in Cycadaceae.…”