Abstract
The environmental regulation of development can result in the production of distinct phenotypes from the same genotype and provide the means for organisms to cope with environmental heterogeneity. The effect of the environment on developmental outcomes is typically mediated by hormonal signals which convey information about external cues to the developing tissues. While such plasticity is a wide-spread property of development, not all developing tissues are equally plastic. To understand how organisms integrate environmental input into coherent adult phenotypes, we must know how different body parts respond, independently or in concert, to external cues and to the corresponding internal signals. We quantified the effect of temperature and ecdysone hormone manipulations on post-growth tissue patterning in an experimental model of adaptive developmental plasticity, the butterfly Bicyclus anynana. Following a suite of traits evolving by natural or sexual selection, we found that different groups of cells within the same tissue have sensitivities and patterns of response that are surprisingly distinct for the external environmental cue and for the internal hormonal signal. All but those wing traits presumably involved in mate choice responded to developmental temperature and, of those, all but the wing traits not exposed to predators responded to hormone manipulations. On the other hand, while patterns of significant response to temperature contrasted traits on autonomously-developing wings, significant response to hormone manipulations contrasted neighboring groups of cells with distinct color fates. We also showed that the spatial compartmentalization of these responses cannot be explained by the spatial or temporal compartmentalization of the hormone receptor protein. Our results unravel the integration of different aspects of the adult phenotype into developmental and functional units which both reflect and impact evolutionary change. Importantly, our findings underscore the complexity of the interactions between environment and physiology in shaping the development of different body parts.
Highlights
The environmental regulation of development can result in the production of distinct phenotypes from the same genotype and provide the means for organisms to cope with environmental heterogeneity
An important step towards understanding how organisms can adaptively respond to the environment by expressing alternative phenotypes, and organize this response across body parts and traits, is to determine to which degree and by what mechanism body parts are integrated into coordinated modules that correspond to functional, evolutionary and/or developmental units [11,12]. This will include understanding how different body parts respond to external environmental cues, as well as to the internal signals that convey information about those cues to the developing tissues
Our results show that different groups of cells on the developing wing epidermis, which correspond to different aspects of the color pattern on adult female wings, have characteristic sensitivities to changes in temperature during pre-adult development (Figure 3), as well as to changes in ecdysone levels during the pupal stage (Figure 4)
Summary
The environmental regulation of development can result in the production of distinct phenotypes from the same genotype and provide the means for organisms to cope with environmental heterogeneity. An important step towards understanding how organisms can adaptively respond to the environment by expressing alternative phenotypes, and organize this response across body parts and traits, is to determine to which degree and by what mechanism body parts are integrated into coordinated modules that correspond to functional, evolutionary and/or developmental units [11,12]. This will include understanding how different body parts respond to external environmental cues, as well as to the internal signals that convey information about those cues to the developing tissues
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