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

Many organisms facultatively produce different phenotypes depending on their environment, yet relatively little is known about the genetic bases of such plasticity in natural populations. In this study, we describe the genetic variation underlying an extreme form of plasticity--resource polyphenism--in Mexican spadefoot toad tadpoles, Spea multiplicata. Depending on their environment, these tadpoles develop into one of two drastically different forms: a carnivore morph or an omnivore morph. We collected both morphs from two ponds that differed in which morph had an adaptive advantage and performed genome-wide association studies of phenotype (carnivore vs. omnivore) and adaptive plasticity (adaptive vs. maladaptive environmental assessment). We identified four quantitative trait loci associated with phenotype and nine with adaptive plasticity, two of which exhibited signatures of minor allele dominance and two of which (one phenotype locus and one adaptive plasticity locus) did not occur as minor allele homozygotes. Investigations into the genetics of plastic traits in natural populations promise to provide novel insights into how such complex, adaptive traits arise and evolve.

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

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.

Morphological novelty emerges from pre-existing phenotypic plasticity.

Plasticity-first evolution (PFE) posits that novel features arise when selection refines pre-existing phenotypic plasticity into an adaptive phenotype. However, PFE is controversial because few tests have been conducted in natural populations. Here we present evidence that PFE fostered the origin of an evolutionary novelty that allowed certain amphibians to invade a new niche-a distinctive carnivore morph. We compared morphology, gene expression and growth of three species of spadefoot toad tadpoles when reared on alternative diets: Scaphiopus holbrookii, which (like most frogs) never produce carnivores; Spea multiplicata, which sometimes produce carnivores, but only through diet-induced plasticity; and Spea bombifrons, which often produce carnivores regardless of diet. Consistent with PFE, we found diet-induced plasticity-in morphology and gene expression-in Sc. holbrookii, adaptive refinement of this plasticity in Sp. multiplicata, and further refinement of the carnivore phenotype in Sp. bombifrons. Generally, phenotypic plasticity might play a significant, if underappreciated, role in evolutionary innovation.