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How organisms evolve under extreme environmental changes is a critical question in the face of global climate change. Genetic accommodation is an evolutionary process by which natural selection acts on novel phenotypes generated through repeated encounters with extreme environments. In this study, polyphenic and monophenic strains of theblackmutant tobacco hornworm,Manduca sexta, were evolved via genetic accommodation of heat stress-induced phenotypes, and the molecular differences between the two strains were explored. Transcriptomic analyses showed that epigenetic and hormonal differences underlie the differences between the two strains and their distinct responses to temperature. DNA methylation had diverged between the two strains potentially mediating genetic assimilation. Juvenile hormone (JH) signaling in the polyphenic strain was temperature sensitive, whereas in the monophenic strain, JH signaling remained low at all temperatures. Although 20-hydroxyecdysone titers were elevated under heat shock conditions in both strains, the strains did not differ in the titers. Tyrosine hydroxylase was also found to differ between the two strains at different temperatures, and its expression could be modulated by topical application of a JH analog. Finally, heat shock of unselectedblackmutants demonstrated that the expression of the JH-response gene,Krüppel-homolog 1(Kr-h1), increased within the first 30 min of heat shock, suggesting that JH levels respond readily to thermal stress. Our study highlights the critical role that hormones and epigenetics play during genetic accommodation and potentially in the evolution of populations in the face of climate change. 

Aposematic coloration offers an opportunity to explore the molecular mechanisms underlying canalization. In this study, the role of epigenetic regulation underlying robustness was explored in the aposematic coloration of the milkweed bug,Oncopeltus fasciatus. Polycomb(Pc) andEnhancer of zeste(E(z)), which encode components of the Polycomb repressive complex 1 (PRC1) and PRC2, respectively, andjing, which encodes a component of the PRC2.2 subcomplex, were knocked down in the fourth instar ofO. fasciatus. Knockdown of these genes led to alterations in scutellar morphology and melanization. In particular, whenPcwas knocked down, the adults developed a highly melanized abdomen, head and forewings at all temperatures examined. In contrast, theE(z)andjingknockdown led to increased plasticity of the dorsal forewing melanization across different temperatures. Moreover,jingknockdown adults exhibited increased plasticity in the dorsal melanization of the head and the thorax. These observations demonstrate that histone modifiers may play a key role during the process of canalization to confer robustness in the aposematic coloration. 

Many insects undergo the process of metamorphosis when larval precursor cells begin to differentiate to create the adult body. The larval precursor cells retain stem cell-like properties and contribute to the regenerative ability of larval appendages. Here we demonstrate that two Broad-complex/Tramtrack/Bric-à-brac Zinc-finger (BTB) domain transcription factors, Chronologically inappropriate morphogenesis (Chinmo) and Abrupt (Ab), act cooperatively to repress metamorphosis in the flour beetle, Tribolium castaneum. Knockdown of chinmo led to precocious development of pupal legs and antennae. We show that although topical application of juvenile hormone (JH) prevents the decrease in chinmo expression in the final instar, chinmo and JH act in distinct pathways. Another gene encoding the BTB domain transcription factor, Ab, was also necessary for the suppression of broad (br) expression in T. castaneum in a chinmo RNAi background, and simultaneous knockdown of ab and chinmo led to the precocious onset of metamorphosis. Furthermore, knockdown of ab led to the loss of regenerative potential of larval legs independently of br. In contrast, chinmo knockdown larvae exhibited pupal leg regeneration when a larval leg was ablated. Taken together, our results show that both ab and chinmo are necessary for the maintenance of the larval tissue identity and, apart from its role in repressing br, ab acts as a crucial regulator of larval leg regeneration. Our findings indicate that BTB domain proteins interact in a complex manner to regulate larval and pupal tissue homeostasis. 

Stored grains used in artificial diets are often treated with insecticides to control infestation by pests. In recent years, insect growth regulators (IGRs) have become an increasingly popular form of insect pest control in agricultural settings. Most IGRs specifically target insects by either disrupting their endocrine system or their chitin synthesis. One type of IGRs comprises of chemical analogs of juvenile hormone (JH), a major hormone involved in growth and development of insects. Here we demonstrate that conventional wheat germ contains JH activity and impacts growth and development of the tobacco hornworm, Manduca sexta . Feeding diet containing conventional wheat germ delayed the timing of metamorphosis in wildtype larvae by extending the duration of the final instar. Diet with conventional wheat germ also inhibited melanization of the black mutant larvae and induced the expression of the JH response gene, Krüppel homolog 1 . We demonstrate that the black mutant bioassay is a sensitive assay that can determine the amount of JH activity in stored grains and suggest that this assay may offer a quick and reliable assay to determine the amount of environmental juvenoids. Researchers are urged to use caution when purchasing stored grains for mass-rearing of research insects. 

We argue that developmental hormones facilitate the evolution of novel phenotypic innovations and timing of life history events by genetic accommodation. Within an individual’s life cycle, metamorphic hormones respond readily to environmental conditions and alter adult phenotypes. Across generations, the many effects of hormones can bias and at times constrain the evolution of traits during metamorphosis; yet, hormonal systems can overcome constraints through shifts in timing of, and acquisition of tissue specific responses to, endocrine regulation. Because of these actions of hormones, metamorphic hormones can shape the evolution of metamorphic organisms. We present a model called a developmental goblet, which provides a visual representation of how metamorphic organisms might evolve. In addition, because developmental hormones often respond to environmental changes, we discuss how endocrine regulation of postembryonic development may impact how organisms evolve in response to climate change. Thus, we propose that developmental hormones may provide a mechanistic link between climate change and organismal adaptation.