The crypsis hypothesis: a stenopic view of the selective factors in the evolution of physical dormancy in seeds

Abstract

Physical dormancy (PY) in seeds/fruits, which is caused by the water-impermeable palisade layer, has long been considered a mechanism for synchronizing germination to a favourable time for seedling survival and establishment. Recently, a new hypothesis (crypsis hypothesis) was proposed as the main selective factor for the evolution of PY. However, there are some misconceptions in this hypothesis. Our objective is to critically evaluate the crypsis hypothesis and to point out that there are multiple adaptive roles of PY. The fundamental argument in the crypsis hypothesis, that PY evolved as an escape mechanism from predators, is not valid according to the evolutionary theory of Darwin. According to Darwin's hypothesis, variations (dormancy in our case) within a population occur randomly, i.e. there is no direct function of a variation at the time of its origin. Different selection pressures operating in the environment increase or decrease the fitness of individuals with the variation. Water-gap anatomy in seeds/fruits and phylogenetic relationships of species with PY suggest that PY has evolved several times in angiosperms. Thus, we argue that not only predatory pressure but also several other environmental pressures (e.g. proper timing of germination, ultra-drying of seeds, dispersal and pathogens) were involved in increasing the fitness of species producing seeds with PY. The significance of PY in the survival of the species under the abovementioned environmental pressures and other misconceptions of the crypsis hypothesis are discussed in detail.

The crypsis hypothesis explained: a reply to Jayasuriya et al. (2015)

“…Furthermore, the sealing of water-impermeable seed coats imposes a cost of increased generation time and, therefore, dormancy-release mechanisms are expected to subsequently evolve in response to local environmental conditions. We also disagree with most other claims by Jayasuriya et al (2015), who failed to appreciate how species with dimorphic seeds -one morph with permeable and the other with impermeable seed coats -benefit from rodent caching behaviour and population dynamics. We welcome this opportunity to clarify and elaborate on key features and the evolution of water-impermeable seed coats according to the crypsis hypothesis.…”

“…The crypsis hypothesis proposes that the primary function of a water-impermeable, hard seed coat is to reduce rodent seed predation by rendering seeds olfactorily cryptic. In an opinion paper, Jayasuriya et al (2015) find the crypsis hypothesis unscientific and 'not consistent with Darwin's theory of evolution by natural selection'. It is unfortunate that Jayasuriya et al (2015) did not appreciate that the crypsis hypothesis offers an alternative explanation for the evolution of waterimpermeable seeds: released seed volatiles are cues used by rodents to locate seeds, and variation in seedcoat permeability leading to differences in seed volatile release represents the variable under selection.…”

“…129-130) This is a deductive fallacy. Jayasuriya et al (2015) assume that rodents will automatically eat located seeds. This is often not the case, because many rodents store seeds for later consumption.…”

“…For at least a century, the literature examining the ecology and ecophysiology of water-impermeable hard seeds has been almost exclusively concerned with their dormancy function, as summarized by, for example, Baskin and Baskin (2014) and Jayasuriya et al (2015). Inspired by the work on how rodents use smell to locate imbibed seeds by Vander Wall and others (e.g.…”

“…Nevertheless, according to the dormancy hypothesis for the evolution of PY, the dormancy function is assumed to be the reason for the evolution of these seeds, as hard seeds evolved from a PD ancestor (Willis et al, 2014). Jayasuriya et al (2015) argue that:…”