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

Abstract

Novel forms of phenotypic plasticity may evolve by lineage‐specific changes or by co‐opting mechanisms from more general forms of plasticity. Here, we evaluated whether a novel resource polyphenism in New World spadefoot toads (genus Spea) evolved by co‐opting mechanisms from an ancestral form of plasticity common in anurans—accelerating larval development rate in response to pond drying. We compared overlap in differentially expressed genes between alternative trophic morphs constituting the polyphenism in Spea versus those found between tadpoles of Old World spadefoot toads (genus Pelobates) when experiencing different pond‐drying regimes. Specifically, we (1) generated a de novo transcriptome and conducted differential gene expression analysis in Spea multiplicata, (2) utilized existing gene expression data and a recently published transcriptome for Pelobates cultripes when exposed to different drying regimes, and (3) identified unique and overlapping differentially expressed transcripts. We found thousands of differentially expressed genes between S. multiplicata morphs that were involved in major developmental reorganization, but the vast majority of these were not differentially expressed in P. cultripes. Thus, S. multiplicata's novel polyphenism appears to have arisen primarily through lineage‐specific changes in gene expression and not by co‐opting existing patterns of gene expression involved in pond‐drying plasticity. Therefore, although ancestral stress responses might jump‐start evolutionary innovation, substantial lineage‐specific modification might be needed to refine these responses into more complex forms of plasticity.

Genetic Variants Underlying Plasticity in Natural Populations of Spadefoot Toads: Environmental Assessment versus Phenotypic Response

“…These findings indicate that the morph production and environmental assessment phenotypes are both polygenic complex traits. Our results correspond with other genetic and genomic findings within this system [30], including the large number of differentially expressed genes found between carnivores and omnivores across different time points and tissues [72,86,87]. Our findings also accord with the large number of phenotypic traits that differ between the alternative morphs [51,54]-the number of coordinated traits involved in producing carnivores and omnivores suggests that many genes are likely involved in these differences.…”

“…We found many candidate genes and transcripts in windows around the putative QTLs. Here, we focus on two candidate genes because of their positions relative to the QTLs, putative functions, and previous identification as differentially expressed genes between carnivores and omnivores [72]. First, the QTL for morph production in Horseshoe on chromosome 2 at position 9,988,823 was located near the end of an intron of the gene PAXBP1, which was previously found to be differentially expressed between carnivores and omnivores [72].…”

“…We utilized 'flo' [70] to generate a chain file as input for 'liftOver' [71] to transfer the annotations to coordinates within the new assembly. Additionally, we aligned the recently generated whole tadpole transcriptome [72] to the pseudogenome assembly using 'GMAP' version 2019-05-12 [73].…”

“…The sequence of each identified gene was compared to human, Xenopus tropicalis, and Nanorana parkeri genes using the top hit from 'blastn'. We additionally compared all the nearby transcripts to those identified as differentially expressed between carnivores and omnivores in a previous study [72] to see whether any differentially expressed genes were in proximity to the putative QTLs.…”

“…We also identified 186 transcripts within these 200 Kb windows, ranging from three transcripts (with one isoform each) to 39 transcripts (with 52 corresponding isoforms; Supplementary Data S2). Of these, one transcript (with a single isoform) in the morph production contrast and three transcripts with five total isoforms in the environmental assessment contrast in the window around each QTL were previously identified as differentially expressed genes between carnivores and omnivores [72].…”