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Abstract When a population experiences severe stress from a changing environment, evolution by natural selection can prevent its extinction, a process dubbed “evolutionary rescue.” However, evolution may be unable to track the sort ofrapidenvironmental change being experienced by many modern‐day populations. A potential solution is for organisms to respond to environmental change through phenotypic plasticity, which can buffer populations against change and thereby buy time for evolutionary rescue. In this review, we examine whether this process extends to situations in which the environmentally induced response is passed to offspring. As we describe, theoretical and empirical studies suggest that such “transgenerational plasticity” can increase population persistence. We discuss the implications of this process for conservation biology, outline potential limitations, and describe some applications. Generally, transgenerational plasticity may be effective at buying time for evolutionary rescue to occur. 

Abstract Polyphenism—in which multiple distinct phenotypes are produced from a single genotype owing to differing environmental conditions—is commonplace, but its molecular bases are poorly understood. Here, we examine the transcriptomic bases of a polyphenism in Mexican spadefoot toads (Spea multiplicata). Depending on their environment, their tadpoles develop into either a default “omnivore” morph or a novel “carnivore” morph. We compared patterns of gene expression among sibships that exhibited high versus low production of carnivores when reared in conditions that induce the carnivore morph versus those that do not. We found that production of the novel carnivore morph actually involved changes in fewer genes than did the maintenance of the default omnivore morph in the inducing environment. However, only body samples showed this pattern; head samples showed the opposite pattern. We also found that changes to lipid metabolism (especially cholesterol biosynthesis) and peroxisome contents and function might be crucial for establishing and maintaining differences between the morphs. Thus, our findings suggest that carnivore phenotype might have originally evolved following the breakdown of robustness mechanisms that maintain the default omnivore phenotype, and that the carnivore morph is developmentally regulated by lipid metabolism and peroxisomal form, function, and/or signaling. This study also serves as a springboard for further exploration into the nature and causes of plasticity in an emerging model system. 

Parental effects are often considered an evolved response, in which parents transmit information about the environment to enhance offspring fitness. However, these effects need not be adaptive. Here, we provide a striking example by presenting evidence that overfeeding of adult Mexican spadefoot toads, Spea multiplicata, is associated with decreased offspring survival. After a temporary change to their standard feeding regimen, S. multiplicata in our captive colony developed a much higher body condition (i.e. body mass for a given body length) than those in the wild. We analysed data from three subsequent experiments and found that although the body condition of a father was positively correlated with tadpole survival, mothers with a higher condition had lower tadpole survival. Our study highlights how obesity can negatively impact future generations via maladaptive maternal effects. Such effects could be especially likely for animals living in variable environments (such as spadefoots) that have evolved ‘thrifty phenotypes’ that make them prone to obesity. Our study also illustrates how husbandry conditions typically regarded as beneficial might be harmful. Given that captive breeding programmes are increasingly used to combat worldwide amphibian declines, these programmes must consider the ecology and evolutionary history of the focal species to minimize any maladaptive parental effects. 

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 ex- pressed 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. 

Developmental plasticity can occur at any life stage, but plasticity that acts early in development may give individuals a competitive edge later in life. Here, we asked if early (pre-feeding) exposure to a nutrient-rich resource impacts hatchling morphology in Mexican spadefoot toad tadpoles, Spea multiplicata . A distinctive carnivore morph can be induced when tadpoles eat live fairy shrimp. We investigated whether cues from shrimp––detected before individuals are capable of feeding––alter hatchling morphology such that individuals could potentially take advantage of this nutritious resource once they begin feeding. We found that hatchlings with early developmental exposure to shrimp were larger and had larger jaw muscles––traits that, at later stages, increase a tadpole's competitive ability for shrimp. These results suggest that early developmental stages can assess and respond to environmental cues by producing resource-use phenotypes appropriate for future conditions. Such anticipatory plasticity may be an important but understudied form of developmental plasticity. 

Increasing evidence suggests that many novel traits might have originated via plasticity-led evolution (PLE). Yet, little is known of the developmental processes that underpin PLE, especially in its early stages. One such process is ‘phenotypic accommodation’, which occurs when, in response to a change in the environment, an organism experiences adjustments across variable parts of its phenotype that improve its fitness. Here, we asked if environmentally induced changes in gene expression are enhanced or reversed during phenotypic accommodation of a novel, complex phenotype in spadefoot toad tadpoles ( Spea multiplicata ). More genes than expected were affected by both the environment and phenotypic accommodation in the liver and brain. However, although phenotypic accommodation primarily reversed environmentally induced changes in gene expression in liver tissue, it enhanced these changes in brain tissue. Thus, depending on the tissue, phenotypic accommodation may either minimize functional disruption via reversal of gene expression patterns or promote novelty via enhancement of existing expression patterns. Our study thereby provides insights into the developmental origins of a novel phenotype and the incipient stages of PLE. 

D o environmentally induced changes to individuals affect natural selection, a nd if so, how? 

What is character displacement? Character displacement is trait evolution that arises as a result of natural selection acting to lessen competition between species.