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

Abstract

Increasing evidence suggests that many novel traits might have originated via plasticity-led evolution (PLE). Yet, little is known of the developmental processes that underpin PLE, especially in its early stages. One such process is ‘phenotypic accommodation’, which occurs when, in response to a change in the environment, an organism experiences adjustments across variable parts of its phenotype that improve its fitness. Here, we asked if environmentally induced changes in gene expression are enhanced or reversed during phenotypic accommodation of a novel, complex phenotype in spadefoot toad tadpoles ( Spea multiplicata ). More genes than expected were affected by both the environment and phenotypic accommodation in the liver and brain. However, although phenotypic accommodation primarily reversed environmentally induced changes in gene expression in liver tissue, it enhanced these changes in brain tissue. Thus, depending on the tissue, phenotypic accommodation may either minimize functional disruption via reversal of gene expression patterns or promote novelty via enhancement of existing expression patterns. Our study thereby provides insights into the developmental origins of a novel phenotype and the incipient stages of PLE.

Comparative transcriptomics reveals that a novel form of phenotypic plasticity evolved via lineage‐specific changes in gene expression

“…Subsequently, previously non‐plastic genes may have been recruited as the polyphenism underwent elaboration and refinement (Casasa et al., 2020 ; Foquet et al., 2021 ; Morris et al., 2014 ). Such a process may be especially likely to occur when, as suggested elsewhere (Levis et al., 2021 , 2022 ), the shared responses constitute a core set of genes that promote a tadpole's development into alternative trajectories, and when the lineage‐specific plasticity genes constitute those that maintain, elaborate, and refine the alternative phenotypes (Lafuente & Beldade, 2019 ). Indeed, the evolution of polyphenisms in other taxa involves bringing other developmental processes into a conditionally expressed context (Abouheif & Wray, 2002 ; Bhardwaj et al., 2020 ; Hanna & Abouheif, 2022 ; Projecto‐Garcia et al., 2017 ; Sommer, 2020 ; Suzuki & Nijhout, 2006 ).…”

“…multiplicata involves a mosaic of tissues throughout the body, including the gut, jaw muscles, and brain (see above). Yet, future work would benefit from taking a tissue‐specific look at the development of both forms of plasticity, especially given the evidence from this system (Levis et al., 2022 ) and other systems (Mateus et al., 2014 ; Oostra et al., 2018 ; Suzuki & Nijhout, 2006 ; van der Burg & Reed, 2021 ) that tissues differ in how they respond to internal and external environmental change. Another caveat concerns the limited temporal sampling.…”

“…With such future analyses in mind, the transcriptome assembled here provides a significant resource for Spea . For example, it will facilitate analyses of splicing and regulatory differences between morphs, investigating expression differences related to sexual selection and hybridization (Chen & Pfennig, 2020 ; Pfennig, 2007 ; Seidl et al., 2019 ), and the transcriptional bases of other aspects of Spea biology (Levis et al., 2021 , 2022 ). Additionally, as demonstrated here, the transcriptome will allow for comparative studies of plasticity not only across other spadefoot species, but also more widely among Anura and higher taxa.…”

“…Moreover, the carnivore morph is thought to have arisen when pre‐existing (ancestral within Scaphopodidae) trophic plasticity was refined by selection into an adaptive phenotype as part of a polyphenism (reviewed in Levis & Pfennig, 2019 ). Recent studies have found that this polyphenism entails changes to lipid metabolism, cholesterol and steroid biosynthesis, and peroxisome form and function (Levis et al., 2020 , 2021 , 2022 ). Interestingly, many of these same processes mediate another, much more common form of plasticity in anurans: the ability to facultatively accelerate development in response to pond drying (Figure 1b ).…”

“…Of relevance to our study, another research team recently investigated the transcriptomic bases of this plasticity in Pelobates cultripes , a European spadefoot that is among the closest relatives of Spea (Figure 1c ). Notably, this team found that this plasticity involves changes to lipid metabolism, cholesterol, and steroid biosynthesis (Liedtke et al., 2021 )—all of which were implicated in mediating Spea 's resource polyphenism (Levis et al., 2020 , 2021 , 2022 ).…”