Cris C Ledón-Rettig’s research while affiliated with Indiana University Bloomington and other places

Stressful experiences in early life can have phenotypic effects that persist into, or manifest during, adulthood. In vertebrates, such carryover effects can be driven by stress-induced secretion of glucocorticoid hormones, such as corticosterone, which can lead to developmental reprogramming of hypothalamic-pituitary-adrenal/interrenal axis activity and behavior. Nutritional stress in the form of early life nutrient restriction is well known to modify later life behaviors and stress activity through corticosterone-related mechanisms. However, it is not known whether corticosterone is also mechanistically involved in carryover effects induced by a different form of nutritional variation: the use of alternate or entirely novel types of dietary resources. The plains spadefoot (Spea bombifrons) presents an excellent system for testing this question, since larvae of this species have evolved to use two alternate diet types: an ancestral detritus-based diet and a more novel diet of live shrimp. While previous work has shown that feeding on the novel shrimp diet influences juvenile (i.e., post-metamorphic) behavior and corticosterone levels, it is unclear whether these diet-induced carryover effects are mediated by diet-induced corticosterone, itself. To test for the mechanistic role of corticosterone in diet-induced carryover effects, we experimentally treated S. bombifrons larvae with exogenous corticosterone and measured subsequent effects on juvenile behavior and corticosterone levels. We found that while shrimp-fed larvae had elevated corticosterone levels, treatment of larvae with corticosterone itself had effects on juvenile behavior that partially resembled those carryover effects induced by the shrimp diet, such as altered food seeking and higher locomotor activity. However, unlike carryover effects caused by the shrimp diet, larval corticosterone exposure did not affect juvenile corticosterone levels. Overall, our study shows that corticosterone-related mechanisms are likely involved in carryover effects induced by a novel diet, yet such diet-induced carryover effects are not driven by corticosterone alone.

Novel behaviours can spur evolutionary change and sometimes even precede morphological innovation, but the evolutionary and developmental contexts for their origins can be elusive. One proposed mechanism to generate behavioural innovation is a shift in the developmental timing of gene-expression patterns underlying an ancestral behaviour, or molecular heterochrony. Alternatively, novel suites of gene expression, which could provide new contexts for signalling pathways with conserved behavioural functions, could promote novel behavioural variation. To determine the relative contributions of these alternatives to behavioural innovation, I used a species of spadefoot toad, Spea bombifrons . Based on environmental cues, Spea larvae develop as either of two morphs: ‘omnivores' that, like their ancestors, feed on detritus, or ‘carnivores' that are predaceous and cannibalistic. Because all anuran larvae undergo a natural transition to obligate carnivory during metamorphosis, it has been proposed that the novel, predaceous behaviour in Spea larvae represents the accelerated activation of gene networks influencing post-metamorphic behaviours. Based on comparisons of brain transcriptional profiles, my results reject widespread heterochrony as a mechanism promoting the expression of predaceous larval behaviour. They instead suggest that the evolution of this trait relied on novel patterns of gene expression that include components of pathways with conserved behavioural functions.

The large size and rapid development of amphibian embryos has facilitated ground-breaking discoveries in developmental biology. Here, we describe the embryogenesis of the Budgett's frog (Lepidobatrachus laevis), an unusual species with eggs that are over twice the diameter of laboratory Xenopus, and embryos that can tolerate higher temperatures to develop into a tadpole four times more rapidly. In addition to detailing their early development, we demonstrate that, like Xenopus, these embryos are amenable to explant culture assays and can express exogenous transcripts in a tissue-specific manner. Moreover, the steep developmental trajectory and large scale of Lepidobatrachus make it exceptionally well-suited for morphogenesis research. For example, the developing organs of the Budgett's frog are massive compared to those of most model species, and are composed of larger individual cells, thereby affording increased subcellular resolution of early vertebrate organogenesis. Furthermore, we found that complete limb regeneration, which typically requires months to achieve in most vertebrate models, occurs in a matter of days in the Budgett's tadpole, which substantially accelerates the pace of experimentation. Thus, the unusual combination of the greater size and speed of the Budgett's frog model provides inimitable advantages for developmental studies-and a novel inroad to address the mechanisms of spatiotemporal scaling during evolution. Copyright © 2015 Elsevier Inc. All rights reserved.

Understanding how populations respond to rapid environmental change is critical both for preserving biodiversity and for human health. An increasing number of studies have shown that genetic variation that has no discernable effect under common ecological conditions can become amplified under stressful or novel conditions, suggesting that environmental change per se can provide the raw materials for adaptation. Indeed, the release of such hidden, or "cryptic," genetic variants has been increasingly viewed as playing a general and important role in allowing populations to respond to rapid environmental change. However, additional studies have suggested that there is a balance between cryptic genetic variants that are potentially adaptive in future environments and genetic variants that are deleterious. In this article, we begin by discussing how population and environmental parameters-such as effective population size and the historical frequency and strength of selection under inducing conditions-influence relative amounts of cryptic genetic variation among populations and the overall phenotypic effects of such variation. The amount and distribution of cryptic genetic variation will, in turn, determine the likelihood that cryptic variants, once expressed, will be adaptive or maladaptive during environmental transitions. We then present specific approaches for measuring these parameters in natural populations. Finally, we discuss one natural system that will be conducive to testing whether populations that vary in these parameters harbor different amounts, or types, of cryptic genetic variation. Generally, teasing apart how population and environmental parameters influence the accumulation of cryptic genetic variation will help us to understand how populations endure and adapt (or fail to adapt) to natural environmental change and anthropogenic disturbance.

Phenotypic variation arises from interactions between environmental and genetic variation, and the emergence of such variation is, in part, mediated by epigenetic mechanisms: factors that modify gene expression but do not change the gene sequence, per se. The role of epigenetic variation and inheritance in natural populations, however, remains poorly understood. The budding field of Ecological Epigenetics seeks to extend our knowledge of epigenetic mechanisms and processes to natural populations, and recent conceptual and technical advances have made progress toward this goal more feasible. In light of these breakthroughs, now is a particularly opportune time to develop a framework that will guide and facilitate exceptional studies in Ecological Epigenetics. Toward this goal, the Ecological Epigenetics symposium brought together researchers with diverse strengths in theory, developmental genetics, ecology, and evolution, and the proceedings from their talks are presented in this issue. By characterizing environmentally dependent epigenetic variation in natural populations, we will enhance our understanding of developmental, ecological, and evolutionary phenomena. In particular, ecological epigenetics has the potential to explain how populations endure (or fail to endure) profound and rapid environmental change. Here, my goal is to introduce some of the common goals and challenges shared by those pursuing this critical field.

Phenotypic variation is a prerequisite for evolution by natural selection, yet the processes that give rise to the novel morphologies upon which selection acts are poorly understood. We employed a chemical genetic screen to identify developmental changes capable of generating ecologically relevant morphological variation as observed among extant species. Specifically, we assayed for exogenously applied small molecules capable of transforming the ancestral larval foregut of the herbivorous Xenopus laevis to resemble the derived larval foregut of the carnivorous Lepidobatrachus laevis. Appropriately, the small molecules that demonstrate this capacity modulate conserved morphogenetic pathways involved in gut development, including downregulation of retinoic acid (RA) signaling. Identical manipulation of RA signaling in a species that is more closely related to Lepidobatrachus, Ceratophrys cranwelli, yielded even more similar transformations, corroborating the relevance of RA signaling variation in interspecific morphological change. Finally, we were able to recover the ancestral gut phenotype in Lepidobatrachus by performing a reverse chemical manipulation to upregulate RA signaling, providing strong evidence that modifications to this specific pathway promoted the emergence of a lineage-specific phenotypic novelty. Interestingly, our screen also revealed pathways that have not yet been implicated in early gut morphogenesis, such as thyroid hormone signaling. In general, the chemical genetic screen may be a valuable tool for identifying developmental mechanisms that underlie ecologically and evolutionarily relevant phenotypic variation.

Animals often facultatively engage in less risky behavior when predators are present. Few studies, however, have investigated whether, or how, such predator-mediated behavior promotes diversification. Here, we ask whether tadpoles of the spadefoot toad Scaphiopus couchii have a diminished ability to utilize a potentially valuable resource--anostracan fairy shrimp--because of behavioral responses to predation risk imposed by carnivorous tadpoles of the genus Spea. Observations of a congener of Sc. couchii that occurs in allopatry with Spea, coupled with an ancestral character state reconstruction, revealed that Sc. couchii's ancestors likely consumed shrimp. By experimentally manipulating the presence of Spea carnivore-morph tadpoles in microcosms, we found that Sc. couchii reduce feeding and avoid areas where both Spea carnivores and shrimp occur. We hypothesize that the recurrent expression of such behaviors in sympatric populations of Sc. couchii led to the evolutionary fixation of a detritivorous feeding strategy, which is associated with a reduced risk of predation from Spea carnivores. Generally, predator-mediated behavior might play a key role in promoting diversification of feeding strategies.

Spadefoot toads have emerged as a model system for addressing fundamental questions in ecological and evolutionary developmental biology (eco-evo-devo). Their tadpoles produce a wide range of adaptive phenotypes in direct response to diverse environmental stimuli. Such phenotypic plasticity offers an excellent opportunity to examine how an organism's ecology affects its development as well as how an organism's development influences its ecology and evolution. By characterizing and understanding the interconnectedness between an organism's environment, its development responses, and its ecological interactions in natural populations, such research promises to clarify further the role of the environment in not only selecting among diverse phenotypes, but also creating such phenotypes in the first place.

Explaining the origins of novel traits is central to evolutionary biology. Longstanding theory suggests that developmental plasticity, the ability of an individual to modify its development in response to environmental conditions, might facilitate the evolution of novel traits. Yet whether and how such developmental flexibility promotes innovations that persist over evolutionary time remains unclear. Here, we examine three distinct ways by which developmental plasticity can promote evolutionary innovation. First, we show how the process of genetic accommodation provides a feasible and possibly common avenue by which environmentally induced phenotypes can become subject to heritable modification. Second, we posit that the developmental underpinnings of plasticity increase the degrees of freedom by which environmental and genetic factors influence ontogeny, thereby diversifying targets for evolutionary processes to act on and increasing opportunities for the construction of novel, functional and potentially adaptive phenotypes. Finally, we examine the developmental genetic architectures of environment-dependent trait expression, and highlight their specific implications for the evolutionary origin of novel traits. We critically review the empirical evidence supporting each of these processes, and propose future experiments and tests that would further illuminate the interplay between environmental factors, condition-dependent development, and the initiation and elaboration of novel phenotypes.