Neontological and paleontological congruence in the evolution of Podocarpaceae (coniferales) reproductive morphology

Abstract

IntroductionPodocarpaceae are a diverse, primarily tropical conifer family that commonly produce large leaves and highly reduced, fleshy seed cones bearing large seeds. These features may result from relatively recent adaptation to closed-canopy angiosperm forests and bird-mediated seed dispersal, although determining precisely when shifts in leaf and seed cone morphology occurred is difficult due to a sparse fossil record and relatively few surviving deep lineages.MethodsWe compare the fossil record of Podocarpaceae with results from ancestral state reconstruction methods and correlated character models using neontological data and a previously published molecular time-tree.ResultsAncestral state reconstructions suggest that small leaves, small seeds, and multi-seeded cones are ancestral in crown Podocarpaceae, with reduced cones bearing few seeds appearing in the Early Cretaceous and the correlated evolution of large leaves and large seeds occurring from the Late Cretaceous onwards. The exact timing of these shifts based on neontological data alone are poorly constrained, however, and estimates of leaf and seed size are imprecise.DiscussionThe fossil record is largely congruent with results based on the molecular time-tree, but provide important constraints on the range of leaf and seed sizes that were present in Cretaceous Podocarpaceae and the time by which changes in cone morphology and seed size likely occurred. We suggest in particular that reduced seed cones appeared in the Early Cretaceous and are linked to the contemporaneous diversification of small bodied avialans (birds), with shifts to larger seed sizes occurring after the Cretaceous in association with the spread of closed-canopy angiosperm forests.

Detailed Seed Cone Morpho-Anatomy Provides New Insights into Seed Cone Origin and Evolution of Podocarpaceae; Podocarpoid and Dacrydioid Clades

“…The number of prosuspensor cells varies widely in the Podocarpaceae (Table 2), and it ranges from seven to twenty-three in the Podocarpoid clade and from five to fourteen in the Dacrydioid clade. The number is lower in other reported Podocarps (3)(4)(5)(6), and there is variable reporting of the number of binucleate cells and elongating cells present. The reproductive cycle varies from one to two years.…”

“…The Podocarpoid clade species have relatively large seed cones (Supplementary Figure S4). Furthermore, Leslie et al [50] reported that seed sizes are generally larger in animal dispersed species [5]. The number of seeds per cone varies in the Podocarpoid clade from one to two, which have, for example, been reported in Podocarpus [51].…”

“…Podocarps are unique among conifers in their ability to successfully compete with angiosperms, especially in tropical forests [1]. Podocarps achieved this capacity by evolving some functionally significant traits, e.g., flattened broad leaves, fleshy seed cones and large seed sizes [2][3][4][5]. Podocarps have an amazing diversity of fleshy seed cones and have evolved several complex functional structures in different genera [6][7][8][9][10].…”

Quantifying the complexity of plant reproductive structures reveals a history of morphological and functional integration

“…For example, the Jurassic to Early Cretaceous increase in conformable edges among many conifer clades coincides with a shift towards thicker and more heavily armored seed cones [22,65], a pattern that mirrors microevolutionary changes in extant conifer populations experiencing high predation pressure from birds and mammals [66,67]. At the same time, fleshy seedcovering organs and compact fruit-like cones that likely functioned in vertebrate seed dispersal become notable features of other conifer clades [68,69], members of the Gnetales [70] and extinct gymnosperms like Caytonia, whose cupules have been recorded in coprolites [71]. Stronger ecological interactions with vertebrates, particularly as small-bodied birds and mammals radiated from the Jurassic onwards [69,72,73], may have favoured the evolution of more compact reproductive structures better adapted to either protect seeds or function as small edible diaspores [74,75].…”

“…At the same time, fleshy seedcovering organs and compact fruit-like cones that likely functioned in vertebrate seed dispersal become notable features of other conifer clades [68,69], members of the Gnetales [70] and extinct gymnosperms like Caytonia, whose cupules have been recorded in coprolites [71]. Stronger ecological interactions with vertebrates, particularly as small-bodied birds and mammals radiated from the Jurassic onwards [69,72,73], may have favoured the evolution of more compact reproductive structures better adapted to either protect seeds or function as small edible diaspores [74,75]. These morphologies appear to be largely derived from existing morphological elements, however, rather than new suites of organs, resulting in a diverse range of morphological strategies for covering seeds (e.g.…”