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Synopsis Human activities are rapidly changing ecosystems around the world. These changes have widespread implications for the preservation of biodiversity, agricultural productivity, prevalence of zoonotic diseases, and sociopolitical conflict. To understand and improve the predictive capacity for these and other biological phenomena, some scientists are now relying on observatory networks, which are often composed of systems of sensors, teams of field researchers, and databases of abiotic and biotic measurements across multiple temporal and spatial scales. One well-known example is NEON, the US-based National Ecological Observatory Network. Although NEON and similar networks have informed studies of population, community, and ecosystem ecology for years, they have been minimally used by organismal biologists. NEON provides organismal biologists, in particular those interested in NEON's focal taxa, with an unprecedented opportunity to study phenomena such as range expansions, disease epidemics, invasive species colonization, macrophysiology, and other biological processes that fundamentally involve organismal variation. Here, we use NEON as an exemplar of the promise of observatory networks for understanding the causes and consequences of morphological, behavioral, molecular, and physiological variation among individual organisms. 

Relatively little is known about whether and how nongenetic inheritance interacts with selection to impact the evolution of phenotypic plasticity. Here, we empirically evaluated how stabilizing selection and a common form of nongenetic inheritance—maternal environmental effects—jointly influence the evolution of phenotypic plasticity in natural populations of spadefoot toads. We compared populations that previous fieldwork has shown to have evolved conspicuous plasticity in resource‐use phenotypes (“resource polyphenism”) with those that, owing to stabilizing selection favouring a narrower range of such phenotypes, appear to have lost this plasticity. We show that: (a) this apparent loss of plasticity in nature reflects a condition‐dependent maternal effect and not a genetic loss of plasticity, that is “genetic assimilation,” and (b) this plasticity is not costly. By shielding noncostly plasticity from selection, nongenetic inheritance generally, and maternal effects specifically, can preclude genetic assimilation from occurring and consequently impede adaptive (genetic) evolution. 

Plasticity-led evolution occurs when a change in the environment triggers a change in phenotype via phenotypic plasticity, and this pre-existing plasticity is subsequently refined by selection into an adaptive phenotype. A critical, but largely untested prediction of plasticity-led evolution (and evolution by natural selection generally) is that the rate and magnitude of evolutionary change should be positively associated with a phenotype’s frequency of expression in a population. Essentially, the more often a phenotype is expressed and exposed to selection, the greater its opportunity for adaptive refinement. We tested this prediction by competing against each other spadefoot toad tadpoles from different natural populations that vary in how frequently they express a novel, environmentally induced carnivore ecomorph. As expected, laboratory-reared tadpoles whose parents were derived from populations that express the carnivore ecomorph more frequently were superior competitors for the resource for which this ecomorph is specialized—fairy shrimp. These tadpoles were better at using this resource both because they were more efficient at capturing and consuming shrimp and because they produced more exaggerated carnivore traits. Moreover, they exhibited these more carnivore-like features even without experiencing the inducing cue, suggesting that this ecomorph has undergone an extreme form of plasticity-led evolution—genetic assimilation. Thus, our findings provide evidence that the frequency of trait expression drives the magnitude of adaptive refinement, thereby validating a key prediction of plasticity-led evolution specifically and adaptive evolution generally. 

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. 

Ecological character displacement is considered crucial in promoting diversification, yet relatively little is known of its underlying mechanisms. We examined whether evolutionary shifts in gene expression plasticity (‘genetic accommodation’) mediate character displacement in spadefoot toads. Where Spea bombifrons and S. multiplicata occur separately in allopatry (the ancestral condition), each produces alternative, diet-induced, larval ecomorphs: omnivores, which eat detritus, and carnivores, which specialize on shrimp. By contrast, where these two species occur together in sympatry (the derived condition), selection to minimize competition for detritus has caused S. bombifrons to become nearly fixed for producing only carnivores, suggesting that character displacement might have arisen through an extreme form of genetic accommodation (‘genetic assimilation’) in which plasticity is lost. Here, we asked whether we could infer a signature of this process in regulatory changes of specific genes. In particular, we investigated whether genes that are normally expressed more highly in one morph (‘biased’ genes) have evolved reduced plasticity in expression levels among S. bombifrons from sympatry compared to S. bombifrons from allopatry. We reared individuals from sympatry vs. allopatry on detritus or shrimp and measured the reaction norms of nine biased genes. Although different genes displayed different patterns of gene regulatory evolution, the combined gene expression profiles revealed that sympatric individuals had indeed lost the diet-induced gene expression plasticity present in allopatric individuals. Our data therefore pro- vide one of the few examples from natural populations in which genetic accommodation/assimilation can be traced to regulatory changes of specific genes. Such genetic accommodation might mediate character displacement in many systems. 

Intraspecific variation in resource-use traits can have profound ecological and evolutionary implications. Among the most strik- ing examples are resource polymorphisms, where alternative morphs that utilize different resources evolve within a population. An underappreciated aspect of their evolution is that the same conditions that favor resource polymorphism—competition and ecological opportunity—might foster additional rounds of diversification within already existing morphs. We examined these issues in spadefoot toad tadpoles that develop into either a generalist "omnivore" or a specialist "carnivore" morph. Specifically, we assessed the morphological diversity of tadpoles from natural ponds and experimentally induced carnivores reared on al- ternative diets. We also surveyed natural ponds to determine if the strength of intramorph competition and the diversity and abundance of dietary resources (measures of ecological opportunity) influenced the diversity of within-morph variation. We found that five omnivore and four carnivore types were present in natural ponds; alternative diets led to shape differences, some of which mirrored variation in the wild; and both competition and ecological opportunity were associated with enhanced morpho- logical diversity in natural ponds. Such fine-scale intraspecific variation might represent an underappreciated form of biodiversity and might constitute a crucible of evolutionary innovation and diversification.