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1. The link between gene duplication and divergent patterns of gene expression across a complex life cycle

   https://doi.org/10.1093/evlett/qrae028  

   DuBose, James_G; de_Roode, Jacobus_C (July 2024, Evolution Letters)

   Abstract The diversification of many lineages throughout natural history has frequently been associated with evolutionary changes in life cycle complexity. However, our understanding of the processes that facilitate differentiation in the morphologies and functions expressed by organisms throughout their life cycles is limited. Theory suggests that the expression of traits is decoupled across life stages, thus allowing for their evolutionary independence. Although trait decoupling between stages is well established, explanations of how said decoupling evolves have seldom been considered. Because the different phenotypes expressed by organisms throughout their life cycles are coded for by the same genome, trait decoupling must be mediated through divergence in gene expression between stages. Gene duplication has been identified as an important mechanism that enables divergence in gene function and expression between cells and tissues. Because stage transitions across life cycles require changes in tissue types and functions, we investigated the potential link between gene duplication and expression divergence between life stages. To explore this idea, we examined the temporal changes in gene expression across the monarch butterfly (Danaus plexippus) metamorphosis. We found that within homologous groups, more phylogenetically diverged genes exhibited more distinct temporal expression patterns. This relationship scaled such that more phylogenetically diverse homologous groups showed more diverse patterns of gene expression. Furthermore, we found that duplicate genes showed increased stage-specificity relative to singleton genes. Overall, our findings suggest an important link between gene duplication and the evolution of complex life cycles. 

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2. Stage- and sex-specific transcriptome analyses reveal distinctive sensory gene expression patterns in a butterfly

   https://doi.org/10.1186/s12864-021-07819-4  

   Ernst, David A.; Westerman, Erica L. (August 2021, BMC Genomics)

   Abstract BackgroundAnimal behavior is largely driven by the information that animals are able to extract and process from their environment. However, the function and organization of sensory systems often change throughout ontogeny, particularly in animals that undergo indirect development. As an initial step toward investigating these ontogenetic changes at the molecular level, we characterized the sensory gene repertoire and examined the expression profiles of genes linked to vision and chemosensation in two life stages of an insect that goes through metamorphosis, the butterflyBicyclus anynana. ResultsUsing RNA-seq, we compared gene expression in the heads of late fifth instar larvae and newly eclosed adults that were reared under identical conditions. Over 50 % of all expressed genes were differentially expressed between the two developmental stages, with 4,036 genes upregulated in larval heads and 4,348 genes upregulated in adult heads. In larvae, upregulated vision-related genes were biased toward those involved with eye development, while phototransduction genes dominated the vision genes that were upregulated in adults. Moreover, the majority of the chemosensory genes we identified in theB. anynanagenome were differentially expressed between larvae and adults, several of which share homology with genes linked to pheromone detection, host plant recognition, and foraging in other species of Lepidoptera. ConclusionsThese results revealed promising candidates for furthering our understanding of sensory processing and behavior in the disparate developmental stages of butterflies and other animals that undergo metamorphosis. 

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3. Ontogeny drives shifts in skin bacterial communities in facultatively paedomorphic salamanders

   https://doi.org/10.1099/mic.0.001399  

   Hartmann, Arik M; McGrath-Blaser, Sarah E; Colón-Piñeiro, Zuania; Longo, Ana V (October 2023, Microbiology)

   Microbiomes are major determinants of host growth, development and survival. In amphibians, host-associated bacteria in the skin can inhibit pathogen infection, but many processes can influence the structure and composition of the community. Here we quantified the shifts in skin-associated bacteria across developmental stages in the striped newt (Notophthalmus perstriatus), a threatened salamander species with a complex life history and vulnerable to infection by the amphibian chytrid fungusBatrachochytrium dendrobatidisand ranavirus. Our analyses show that pre-metamorphic larval and paedomorphic stages share similar bacterial compositions, and that the changes in the microbiome coincided with physiological restructuring during metamorphosis. Newts undergoing metamorphosis exhibited microbiome compositions that were intermediate between paedomorphic and post-metamorphic stages, further supporting the idea that metamorphosis is a major driver of host-associated microbes in amphibians. We did not find support for infection-related disruption of the microbiome, though infection replicates were small for each respective life stage. 

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4. Transcriptomic evidence for visual adaptation during the aquatic to terrestrial metamorphosis in leopard frogs

   https://doi.org/10.1186/s12915-022-01341-z  

   Schott, Ryan K.; Bell, Rayna C.; Loew, Ellis R.; Thomas, Kate N.; Gower, David J.; Streicher, Jeffrey W.; Fujita, Matthew K. (June 2022, BMC Biology)

   Abstract BackgroundDifferences in morphology, ecology, and behavior through ontogeny can result in opposing selective pressures at different life stages. Most animals, however, transition through two or more distinct phenotypic phases, which is hypothesized to allow each life stage to adapt more freely to its ecological niche. How this applies to sensory systems, and in particular how sensory systems adapt across life stages at the molecular level, is not well understood. Here, we used whole-eye transcriptomes to investigate differences in gene expression between tadpole and juvenile southern leopard frogs (Lithobates sphenocephalus), which rely on vision in aquatic and terrestrial light environments, respectively. Because visual physiology changes with light levels, we also tested the effect of light and dark exposure. ResultsWe found 42% of genes were differentially expressed in the eyes of tadpoles versus juveniles and 5% for light/dark exposure. Analyses targeting a curated subset of visual genes revealed significant differential expression of genes that control aspects of visual function and development, including spectral sensitivity and lens composition. Finally, microspectrophotometry of photoreceptors confirmed shifts in spectral sensitivity predicted by the expression results, consistent with adaptation to distinct light environments. ConclusionsOverall, we identified extensive expression-level differences in the eyes of tadpoles and juveniles related to observed morphological and physiological changes through metamorphosis and corresponding adaptive shifts to improve vision in the distinct aquatic and terrestrial light environments these frogs inhabit during their life cycle. More broadly, these results suggest that decoupling of gene expression can mediate the opposing selection pressures experienced by organisms with complex life cycles that inhabit different environmental conditions throughout ontogeny. 

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5. Comparisons of cell proliferation and cell death from tornaria larva to juvenile worm in the hemichordate Schizocardium californicum

   https://doi.org/10.1186/s13227-022-00198-1  

   Bump, Paul; Khariton, Margarita; Stubbert, Clover; Moyen, Nicole E.; Yan, Jia; Wang, Bo; Lowe, Christopher J. (June 2022, EvoDevo)

   Abstract BackgroundThere are a wide range of developmental strategies in animal phyla, but most insights into adult body plan formation come from direct-developing species. For indirect-developing species, there are distinct larval and adult body plans that are linked together by metamorphosis. Some outstanding questions in the development of indirect-developing organisms include the extent to which larval tissue undergoes cell death during the process of metamorphosis and when and where the tissue that will give rise to the adult originates. How do the processes of cell division and cell death redesign the body plans of indirect developers? In this study, we present patterns of cell proliferation and cell death during larval body plan development, metamorphosis, and adult body plan formation, in the hemichordateSchizocardium californium(Cameron and Perez in Zootaxa 3569:79–88, 2012) to answer these questions. ResultsWe identified distinct patterns of cell proliferation between larval and adult body plan formation ofS. californicum. We found that some adult tissues proliferate during the late larval phase prior to the start of overt metamorphosis. In addition, using an irradiation and transcriptomic approach, we describe a genetic signature of proliferative cells that is shared across the life history states, as well as markers that are unique to larval or juvenile states. Finally, we observed that cell death is minimal in larval stages but begins with the onset of metamorphosis. ConclusionsCell proliferation during the development ofS. californicumhas distinct patterns in the formation of larval and adult body plans. However, cell death is very limited in larvae and begins during the onset of metamorphosis and into early juvenile development in specific domains. The populations of cells that proliferated and gave rise to the larvae and juveniles have a genetic signature that suggested a heterogeneous pool of proliferative progenitors, rather than a set-aside population of pluripotent cells. Taken together, we propose that the gradual morphological transformation ofS. californicumis mirrored at the cellular level and may be more representative of the development strategies that characterize metamorphosis in many metazoan animals. 

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