Identification of candidate loci for adaptive phenotypic plasticity in natural populations of spadefoot toads

Abstract

Phenotypic plasticity allows organisms to alter their phenotype in direct response to changes in the environment. Despite growing recognition of plasticity's role in ecology and evolution, few studies have probed plasticity's molecular bases—especially using natural populations. We investigated the genetic basis of phenotypic plasticity in natural populations of spadefoot toads (Spea multiplicata). Spea tadpoles normally develop into an “omnivore” morph that is favored in long‐lasting, low‐density ponds. However, if tadpoles consume freshwater shrimp or other tadpoles, they can alternatively develop (via plasticity) into a “carnivore” morph that is favored in ephemeral, high‐density ponds. By combining natural variation in pond ecology and morph production with population genetic approaches, we identified candidate loci associated with each morph (carnivores vs. omnivores) and loci associated with adaptive phenotypic plasticity (adaptive vs. maladaptive morph choice). Our candidate morph loci mapped to two genes, whereas our candidate plasticity loci mapped to 14 genes. In both cases, the identified genes tended to have functions related to their putative role in spadefoot tadpole biology. Our results thereby form the basis for future studies into the molecular mechanisms that mediate plasticity in spadefoots. More generally, these results illustrate how diverse loci might mediate adaptive plasticity.

Cross‐species transcriptomics uncovers genes underlying genetic accommodation of developmental plasticity in spadefoot toads

“…The role of developmental plasticity in evolution has gained prominence in recent years, but how plasticity itself evolves at the molecular level is only recently being elucidated (Casasa et al, 2020; Levis et al, 2020; Sikkink et al, 2019; Sommer, 2020). By studying two species of spadefoot toad with differing degrees of plasticity in response to pond drying, we identified orthologues and functional gene pathways whose environmental sensitivity in expression (i.e., their transcriptomic reaction norms) have diverged.…”

Linking Molecular Mechanisms and Evolutionary Consequences of Resource Polyphenism

“…Among examples of RP, such a switch structure might be responsible for development into the carnivore morph of spadefoot toad tadpoles ( Figure 1B ). Evidence for this possibility comes from observations that carnivores, which are initially induced by competition for and consumption of freshwater shrimp and other tadpoles, can revert into omnivores if environmental conditions change, such as a dramatic reduction in the availability of prey (Pomeroy, 1981 ; Pfennig, 1992a , b ), as might happen following a second rain event at a pond (Levis et al, 2020 ). Often, these reverted individuals exhibit a mosaic of carnivore and omnivore features such as the short gut that is characteristic of carnivores and the jaw musculature of omnivores.…”

“…Image in (A) is courtesy of John J. Gilbert and reproduced from Gilbert ( 2017 ) with permission from John Wiley and Sons (© 2016 Cambridge Philosophical Society). Image in (B) is courtesy of David W. Pfennig and modified from Levis et al ( 2020 ). Images in (C) are by Erik J. Ragsdale and from Bui et al ( 2018 ).…”

State of the Amphibia 2020: A review of five years of amphibian research and existing resources

“…Research on many other amphibian genera has made notable historical contributions to biology: e.g., Plethodon cinereus in behavioral ecology and development (Dent 1942;Heatwole 1962;Kleeberger and Werner 1982;Wyman and Hawksley-Lescault 1987;Kerney 2011;Kerney et al 2012); Engystomops in sexual selection (Ryan et al, 1990); Rana in cloning (Briggs and King, 1952); Rana and (Lefcort et al, 1998;Hopkins et al, 2000;Bridges, 2000;Pollet and Bendell-Young, 2000) Acris (Fleming et al, 1982;Clark et al, 1998;Reeder et al, 1998) in community ecology and toxicology. New tools have since promoted the emergence of more model systems from classically "non-model" species and systems, such as dendrobatid poison frogs for the neurobiology of parental care (Roland and O'Connell, 2015;O'Connell, 2020) and the molecular evolution of chemical defense (Saporito et al, 2012;Tarvin et al, 2017;Caty et al, 2019;Alvarez-Buylla et al, 2022), toxic salamanders and resistant garter snakes for co-evolution (Geffeney et al, 2005;Bucciarelli et al, 2022), Spea for phenotypic plasticity and life-history evolution (Levis et al, 2015(Levis et al, , 2020, and Nanorana parkeri for adaptation to high elevation (Sun et al, 2015(Sun et al, , 2018Wang et al, 2018). As we will highlight here, the growing availability of amphibian genomes and other molecular resources poises amphibian researchers to further develop other amphibians as new "model" species.…”