Genetic accommodation via modified endocrine signalling explains phenotypic divergence among spadefoot toad species

Abstract

Phenotypic differences among species may evolve through genetic accommodation, but mechanisms accounting for this process are poorly understood. Here we compare hormonal variation underlying differences in the timing of metamorphosis among three spadefoot toads with different larval periods and responsiveness to pond drying. We find that, in response to pond drying, Pelobates cultripes and Spea multiplicata accelerate metamorphosis, increase standard metabolic rate (SMR), and elevate whole-body content of thyroid hormone (the primary morphogen controlling metamorphosis) and corticosterone (a stress hormone acting synergistically with thyroid hormone to accelerate metamorphosis). In contrast, Scaphiopus couchii has the shortest larval period, highest whole-body thyroid hormone and corticosterone content, and highest SMR, and these trait values are least affected by pond drying among the three species. Our findings support that the atypically rapid and canalized development of S. couchii evolved by genetic accommodation of endocrine pathways controlling metamorphosis, showing how phenotypic plasticity within species may evolve into trait variation among species.

Developmental Bias and Evolution: A Regulatory Network Perspective

“…This suggests that evolution has capitalized on the effects of physical stress whose functionality was ensured by channeling cellular and genetic regulatory networks in morphogenesis. Environmentally induced bias has also been suggested as a contributor to the evolution of carotenoid coloration in birds (Badyaev et al 2017), pigmentation in water fleas (Scoville and Pfrender 2010), morphology and physiology in carnivorous toads (Gomez-Mestre and Buchholz 2006;Kulkarni et al 2017), morphological and behavioral traits in Onthophagus dung beetles (Casasa and Moczek 2018), and sexual size dimorphism in the house finch (Badyaev 2005).…”

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

“…As it turns out, four of our identified genes served these functions (JUN, TENT5A, MED13, and MAP3K4; Devary, Gottlieb, Lau, & Karin, 1991; Grueter et al., 2012; Kuchta et al., 2016; Takekawa, Posas, & Saito, 1997). Notably, MED13 has been implicated in helping modulate thyroid hormone‐dependent transcription (Grueter et al., 2012), and thyroid hormone, in turn, has been implicated in mediating carnivore development specifically (Pfennig, 1992b) and tadpole development generally (Denver, 1998; Kulkarni & Buchholz, 2012; Kulkarni, Denver, Gomez‐Mestre, & Buchholz, 2017). Moreover, MED13 also plays a role in limiting lipid accumulation (Pospisilik et al., 2010), a key metabolic difference between spadefoot tadpole morphs (de la Serna Buzón, 2019).…”

Plasticity‐led evolution: A survey of developmental mechanisms and empirical tests

“…Some studies have noted that changes in thresholds of responsiveness to external cues are important (e.g., Kulkarni, Denver, Gomez-Mestre, & Buchholz, 2017;Sikkink et al, 2014;Suzuki & Nijhout, 2006), and others have noted concomitant changes in gene expression (e.g., Levis et al, 2017;Schrader, Helanterä, & Oettler, 2017;Scoville & Pfrender, 2010). Addressing this issue may help unravel the details of genetic assimilation and how environmental induction switches to constitutive production.…”

“…Addressing this issue may help unravel the details of genetic assimilation and how environmental induction switches to constitutive production. Some studies have noted that changes in thresholds of responsiveness to external cues are important (e.g., Kulkarni, Denver, Gomez-Mestre, & Buchholz, 2017;Sikkink et al, 2014;Suzuki & Nijhout, 2006), and others have noted concomitant changes in gene expression (e.g., Levis et al, 2017;Schrader, Helanterä, & Oettler, 2017;Scoville & Pfrender, 2010). However, additional investigations that place developmental processes such as hormonal regulation, epigenetic change, and gene expression in the context of gene regulatory networks (Pfennig & Ehrenreich, 2014) could elucidate the developmental changes that facilitate the transition from environmental induction to canalization (Debat & David, 2001;Debat et al, 2009).…”