Hedgehog signaling is necessary and sufficient to mediate craniofacial plasticity in teleosts
Autor: | Ira Male, Dina Navon, Benjamin Aaronson, Rolf O. Karlstrom, R. Craig Albertson, Emily R. Tetrault |
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Jazyk: | angličtina |
Rok vydání: | 2020 |
Předmět: |
ecodevo
Fish Proteins Evolution Foraging Plasticity craniofacial phenotypic plasticity flexible stem Cichlid Animals Hedgehog Proteins Craniofacial Hedgehog Phenotypic plasticity Multidisciplinary biology Skull Cichlids Biological Sciences biology.organism_classification Phenotype hedgehog signaling Adaptation Physiological Hedgehog signaling pathway Evolutionary biology Signal Transduction |
Zdroj: | Proceedings of the National Academy of Sciences of the United States of America |
ISSN: | 1091-6490 0027-8424 |
Popis: | Significance Phenotypic plasticity has emerged as an important concept in evolutionary biology. It is thought to contribute to an organism’s ability to adapt to environmental change within a single generation, which may facilitate survival and increase fitness. Furthermore, plasticity has the potential to bias the direction and/or speed of evolution by changing patterns of phenotypic variation and exposing new genetic variation to selection (i.e., flexible stem evolution). Our understanding of this important phenomenon is incomplete owing to limited knowledge of the molecular underpinnings of reaction norm evolution. Using the teleost feeding apparatus as a model, we explore this open question and show that the Hh signaling pathway underlies the ability of this structure to respond plastically to alternate feeding regimes. Phenotypic plasticity, the ability of a single genotype to produce multiple phenotypes under different environmental conditions, is critical for the origins and maintenance of biodiversity; however, the genetic mechanisms underlying plasticity as well as how variation in those mechanisms can drive evolutionary change remain poorly understood. Here, we examine the cichlid feeding apparatus, an icon of both prodigious evolutionary divergence and adaptive phenotypic plasticity. We first provide a tissue-level mechanism for plasticity in craniofacial shape by measuring rates of bone deposition within functionally salient elements of the feeding apparatus in fishes forced to employ alternate foraging modes. We show that levels and patterns of phenotypic plasticity are distinct among closely related cichlid species, underscoring the evolutionary potential of this trait. Next, we demonstrate that hedgehog (Hh) signaling, which has been implicated in the evolutionary divergence of cichlid feeding architecture, is associated with environmentally induced rates of bone deposition. Finally, to demonstrate that Hh levels are the cause of the plastic response and not simply the consequence of producing more bone, we use transgenic zebrafish in which Hh levels could be experimentally manipulated under different foraging conditions. Notably, we find that the ability to modulate bone deposition rates in different environments is dampened when Hh levels are reduced, whereas the sensitivity of bone deposition to different mechanical demands increases with elevated Hh levels. These data advance a mechanistic understanding of phenotypic plasticity in the teleost feeding apparatus and in doing so contribute key insights into the origins of adaptive morphological radiations. |
Databáze: | OpenAIRE |
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