Transcriptomic bases of a polyphenism

Abstract

Polyphenism—in which multiple distinct phenotypes are produced from a single genotype owing to differing environmental conditions—is commonplace, but its molecular bases are poorly understood. Here, we examine the transcriptomic bases of a polyphenism in Mexican spadefoot toads (Spea multiplicata). Depending on their environment, their tadpoles develop into either a default “omnivore” morph or a novel “carnivore” morph. We compared patterns of gene expression among sibships that exhibited high versus low production of carnivores when reared in conditions that induce the carnivore morph versus those that do not. We found that production of the novel carnivore morph actually involved changes in fewer genes than did the maintenance of the default omnivore morph in the inducing environment. However, only body samples showed this pattern; head samples showed the opposite pattern. We also found that changes to lipid metabolism (especially cholesterol biosynthesis) and peroxisome contents and function might be crucial for establishing and maintaining differences between the morphs. Thus, our findings suggest that carnivore phenotype might have originally evolved following the breakdown of robustness mechanisms that maintain the default omnivore phenotype, and that the carnivore morph is developmentally regulated by lipid metabolism and peroxisomal form, function, and/or signaling. This study also serves as a springboard for further exploration into the nature and causes of plasticity in an emerging model system.

Disentangling the developmental origins of a novel phenotype: enhancement versus reversal of environmentally induced gene expression

“…Our study thereby provides a window into the developmental origins of a novel phenotype and the early stages of PLE. This study also complements recent work on this system [34–36] regarding how gene expression changes undergird phenotypic plasticity and the evolution of the distinctive carnivore phenotype.…”

“…[63,64]). Moreover, recent studies have shown that plasticity in spadefoots may often entail regulating oxidative stress [34,65]. Thus, phenotypic accommodation to a new environment in the brain may involve energetic changes that can affect cognition.…”

“…Specifically, cholesterol is a necessary precursor for producing steroid hormones, two of which have been implicated in spadefoot tadpole morphological development (thyroxine, [29]; corticosterone, [66]). Moreover, carnivore-omnivore plasticity is related to changes in developmental rates [29], and recent work has found that cholesterol and steroid biosynthesis are not only important for trophic plasticity [34], but also plasticity in developmental rate in response to pond drying in spadefoots [67]. Together with the present results, this suggests that the cue environment may trigger the process of upregulating the synthesis of cholesterol and presumably hormones derived from it (likely through a dietary shift), and that those individuals exceeding some threshold level develop into carnivores.…”

“…We measured gene expression in liver and brain tissue because our treatments differed in resource environment (affecting the liver) and social environment (affecting the brain). Moreover, previous work suggested that these two tissues are foci of numerous, environmentally induced changes in gene expression [34].

Figure 2Diagrammatic representation of our ( a ) experimental design and ( b ) predictions.

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Linking Molecular Mechanisms and Evolutionary Consequences of Resource Polyphenism

“…Thus, the loss of cues or insufficient levels or duration of cues can result in “intermediate” and mosaic phenotypes. However, a recent study suggests that cholesterol biosynthesis and peroxisome activity might be important regulators of the morph transition because of their system-wide effects on metabolism and hormone production, suggesting a role for a top-down, “master regulator” model (Levis et al, 2021 ). In addition, whether the component traits of the carnivore morph are activated sequentially—thus making the architecture actually more akin to that of ganged switches—and are responding to the same internal (e.g., hormonal) signals, as opposed to environmental cues, requires further study.…”