Abstract
Organisms withstand normal ranges of environmental fluctuations by producing a set of phenotypes genetically programmed as a reaction norm; however, extreme conditions can expose a misregulation of phenotypes called a hidden reaction norm. Although an environment consists of multiple factors, how combinations of these factors influence a reaction norm is not well understood. To elucidate the combinatorial effects of environmental factors, we studied the leaf shape plasticity of the carnivorous pitcher plant Cephalotus follicularis. Clonally propagated plants were subjected to 12-week-long growth experiments in different conditions controlled by growth chambers. Here, we show that the dimorphic response of forming a photosynthetic flat leaf or an insect-trapping pitcher leaf is regulated by two covarying environmental cues: temperature and photoperiod. Even within the normal ranges of temperature and photoperiod, unusual combinations of the two induced the production of malformed leaves that were rarely observed under the environmentally typical combinations. We identified such cases in combinations of a summer temperature with a short-to-neutral day length, whose average frequency in the natural Cephalotus habitats corresponded to a once-in-a-lifetime event for this perennial species. Our results suggest that even if individual cues are within the range of natural fluctuations, a hidden reaction norm can be exposed under their discordant combinations. We anticipate that climate change may challenge organismal responses through not only extreme cues but also through uncommon combinations of benign cues.
Highlights
Phenotypic plasticity allows a single genotype to produce a set of phenotypes called a ‘reaction norm’ [1] in response to external cues
We focused on phenotypic plasticity in the carnivorous pitcher plant Cephalotus follicularis, which is endemic to the south-western corner of Western Australia [11]
We showed that naturally rare combinations of multiple environmental cues expose a hidden reaction norm, which is otherwise masked
Summary
Phenotypic plasticity allows a single genotype to produce a set of phenotypes called a ‘reaction norm’ [1] in response to external cues. Under conditions typical of a habitat, highly autocorrelated environmental cues often change concurrently [10], as observed in the seasonal covariation of temperature and photoperiod This fact highlighted a potential role for environmental covariation in regulating phenotypic plasticity and allowed us to develop a testable prediction that a discordance of covarying cues can expose hidden reaction norms. To test this hypothesis, we focused on phenotypic plasticity in the carnivorous pitcher plant Cephalotus follicularis, which is endemic to the south-western corner of Western Australia [11]. We show that an unusual combination of temperature and photoperiod unmasks a hidden reaction norm, even though neither environmental cue is extreme
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