Developmental origins of a novel gut morphology in frogs

Abstract

SUMMARY Phenotypic variation is a prerequisite for evolution by natural selection, yet the processes that give rise to the novel morphologies upon which selection acts are poorly understood. We employed a chemical genetic screen to identify developmental changes capable of generating ecologically relevant morphological variation as observed among extant species. Specifically, we assayed for exogenously applied small molecules capable of transforming the ancestral larval foregut of the herbivorous Xenopus laevis to resemble the derived larval foregut of the carnivorous Lepidobatrachus laevis. Appropriately, the small molecules that demonstrate this capacity modulate conserved morphogenetic pathways involved in gut development, including downregulation of retinoic acid (RA) signaling. Identical manipulation of RA signaling in a species that is more closely related to Lepidobatrachus, Ceratophrys cranwelli, yielded even more similar transformations, corroborating the relevance of RA signaling variation in interspecific morphological change. Finally, we were able to recover the ancestral gut phenotype in Lepidobatrachus by performing a reverse chemical manipulation to upregulate RA signaling, providing strong evidence that modifications to this specific pathway promoted the emergence of a lineage-specific phenotypic novelty. Interestingly, our screen also revealed pathways that have not yet been implicated in early gut morphogenesis, such as thyroid hormone signaling. In general, the chemical genetic screen may be a valuable tool for identifying developmental mechanisms that underlie ecologically and evolutionarily relevant phenotypic variation.

Retinoic Acid and the Development of the Endoderm

“…In addition, there are relatively few markers of early hindgut that could be used to understand early patterning events. Addition of exogenous RA clearly disrupts the morphogenesis of this region with lack of looping and rotation [132,133] and differing levels of RA may even be important in the evolution of novel gut morphologies [134]. However, loss of RA signaling experiments in the hindgut, that can circumvent the earlier requirements for RA in other tissues, are necessary for an in depth understanding of the role of RA in this region.…”

Insulin signalling underlies both plasticity and divergence of a reproductive trait inDrosophila

“…One hypothesis is that common molecular mechanisms underlie both plasticity and interspecific variation in a trait, which would allow plasticity to promote diversification by providing a range of phenotypes whose underlying genetic variation can be subject to selection by genetic accommodation, genetic assimilation or other means [3]. The molecular underpinnings of plasticity within a single species are known for several systems [4][5][6][7], and there is also evidence that plasticity contributes to species differentiation [8]. However, specific examples that functionally demonstrate the molecular basis for both the plasticity and interspecies divergence of the same trait are lacking.…”

Hedgehog signaling enables nutrition-responsive inhibition of an alternative morph in a polyphenic beetle

“…For instance, in many butterfly species, seasonal conditions critically alter selective environments, and seasonal sensitivity in eye spot formation is able to adjust wing phenotypes, thereby maintaining high fitness across fluctuating environments (9). Similarly, environment-dependent induction of carnivory in spadefoot toad tadpoles (10,11) or tooth formation and bacterial predation in nematodes (12), two striking and complex evolutionary novelties, greatly affect the adaptive significance of each innovation, thereby facilitating their adaptive radiations (13). Here, we investigate the functional significance of the Hedgehog (Hh) signaling pathway, a deeply conserved cellular transduction pathway, in the development of beetles horns, a striking evolutionary novelty (14), and specifically, the origins of environment-responsive horn formation, alternative male phenotypes, and body size thresholds, emergent phenotypes that have greatly impacted patterns of morphological radiation among horned beetles (15)(16)(17).…”