Taxonomy, anatomy and evolution of physical dormancy in seeds

Abstract Physical dormancy (PY) is caused by a water‐impermeable seed or fruit coat. It is known, or highly suspected, to occur in nine orders and 15 families of angiosperms ( sensu Angiosperm Phylogeny Group 1998), 13 of which are core eudicots. The Zingiberales is the only monocot order, and Cannaceae ( Canna ) the only monocot family, in which PY is known to occur. Six of the nine orders, and 12 of the 15 families, in which PY occurs are rosids. Furthermore, six of the families belong to the Malvales. The water‐impermeable palisade layer(s) of cells are located in the seed coats of 13 of the families, and in the fruit coats of Anacardiaceae and Nelumbonaceae. In all 15 families, a specialized structure is associated with the water‐impermeable layer(s). The breaking of PY involves disruption or dislodgment of these structures, which act as environmental ‘signal detectors’ for germination. Representatives of the nine angiosperm orders in which PY occurs had evolved by the late Cretaceous or early Tertiary (Paleogene). Anatomical evidence for PY in fruits of the extinct species Rhus rooseae (Anacardiaceae, middle Eocene) suggests that PY had evolved by 43Ma, and probably much earlier. We have constructed a conceptual model for the evolution of PY, and of PY+ physiological dormancy (PD), within Anacardiaceae. The model begins in pre‐Eocene times with an ancestral species that has large, pachychalazal, non‐dormant (ND), recalcitrant seeds. By the middle Eocene, a derived species with relatively small, partial pachychalazal, orthodox seeds and a water‐impermeable endocarp (thus PY) had evolved, and by the Oligocene, PD had been added to the seed (true seed + endocarp) dormancy mechanism. It is suggested that climatic drying (Eocene), followed by climatic cooling (Eocene–Oligocene transition), were the primary selective agents in the development of PY. An evolutionary connection between PY and recalcitrance is suggested by the relatively high concentration of these two character states in the rosids. Phylogenetic data and fossil evidence seem to support the PY → (PY + PD) evolutionary sequence in Anacardiaceae, which also may have occured in Leguminosae.