2023 |
Labib Rouhana; Allison Edgar; Fredrik Hugosson; Valeria Dountcheva; Mark Q. Martindale; Joseph F. Ryan Cytoplasmic polyadenylation is an ancestral hallmark of early development in animals Journal Article In: Molecular Biology and Evolution, vol. 40, iss. 6, 2023. Abstract | Links | BibTeX | Tags: Cnidaria, Ctenophora, cytoplasmic polyadenylation, Evolution, post-transcriptional regulation @article{Rouhana_2023, Differential regulation of gene expression has produced the astonishing diversity of life on Earth. Understanding the origin and evolution of mechanistic innovations for control of gene expression is therefore integral to evolutionary and developmental biology. Cytoplasmic polyadenylation is the biochemical extension of polyadenosine at the 3′-end of cytoplasmic mRNAs. This process regulates the translation of specific maternal transcripts and is mediated by the Cytoplasmic Polyadenylation Element-Binding Protein family (CPEBs). Genes that code for CPEBs are amongst a very few that are present in animals but missing in nonanimal lineages. Whether cytoplasmic polyadenylation is present in non-bilaterian animals (i.e., sponges, ctenophores, placozoans, and cnidarians) remains unknown. We have conducted phylogenetic analyses of CPEBs, and our results show that CPEB1 and CPEB2 subfamilies originated in the animal stem lineage. Our assessment of expression in the sea anemone, Nematostella vectensis (Cnidaria), and the comb jelly, Mnemiopsis leidyi (Ctenophora), demonstrates that maternal expression of CPEB1 and the catalytic subunit of the cytoplasmic polyadenylation machinery (GLD2) is an ancient feature that is conserved across animals. Furthermore, our measurements of poly(A)-tail elongation reveal that key targets of cytoplasmic polyadenylation are shared between vertebrates, cnidarians, and ctenophores, indicating that this mechanism orchestrates a regulatory network that is conserved throughout animal evolution. We postulate that cytoplasmic polyadenylation through CPEBs was a fundamental innovation that contributed to animal evolution from unicellular life. |
2022 |
Allison Edgar; José Miguel Ponciano; Mark Q. Martindale Ctenophores are direct developers that reproduce continuously beginning very early after hatching Journal Article In: Proceedings of the National Academy of Sciences, vol. 119, no. 18, 2022. Abstract | Links | BibTeX | Tags: Ctenophora, dissogeny, Evolution, larval reproduction, life history, Mnemiopsis leidyi @article{Edgar_2022, A substantial body of literature reports that ctenophores exhibit an apparently unique life history characterized by biphasic sexual reproduction, the first phase of which is called larval reproduction or dissogeny. Whether this strategy is plastically deployed or a typical part of these species’ life history was unknown. In contrast to previous reports, we show that the ctenophore Mnemiopsis leidyi does not have separate phases of early and adult reproduction, regardless of the morphological transition to what has been considered the adult form. Rather, these ctenophores begin to reproduce at a small body size and spawn continuously from this point onward under adequate environmental conditions. They do not display a gap in productivity for metamorphosis or other physiological transition at a certain body size. Furthermore, nutritional and environmental constraints on fecundity are similar in both small and large animals. Our results provide critical parameters for understanding resource partitioning between growth and reproduction in this taxon, with implications for management of this species in its invaded range. Finally, we report an observation of similarly small-size spawning in a beroid ctenophore, which is morphologically, ecologically, and phylogenetically distinct from other ctenophores reported to spawn at small sizes. We conclude that spawning at small body size should be considered as the default, on-time developmental trajectory rather than as precocious, stress-induced, or otherwise unusual for ctenophores. The ancestral ctenophore was likely a direct developer, consistent with the hypothesis that multiphasic life cycles were introduced after the divergence of the ctenophore lineage. |
2020 |
Lingyu Wang; Jennifer W. Israel; Allison Edgar; Rudolf A. Raff; Elizabeth C. Raff; Maria Byrne; Gregory A. Wray Genetic basis for divergence in developmental gene expression in two closely related sea urchins Journal Article In: Nature Ecology & Evolution, vol. 4, no. 6, pp. 831–840, 2020. Abstract | Links | BibTeX | Tags: developmental biology, Evolution, evolutionary genetics, molecular evolution @article{Wang_2020, The genetic basis for divergence in developmental gene expression among species is poorly understood, despite growing evidence that such changes underlie many interesting traits. Here we quantify transcription in hybrids of Heliocidaris tuberculata and Heliocidaris erythrogramma, two closely related sea urchins with highly divergent developmental gene expression and life histories. We find that most expression differences between species result from genetic influences that affect one stage of development, indicating limited pleiotropic consequences for most mutations that contribute to divergence in gene expression. Activation of zygotic transcription is broadly delayed in H. erythrogramma, the species with the derived life history, despite its overall faster premetamorphic development. Altered expression of several terminal differentiation genes associated with the derived larval morphology of H. erythrogramma is based largely on differences in the expression or function of their upstream regulators, providing insights into the genetic basis for the evolution of key life history traits. |
Publications
2023 |
Cytoplasmic polyadenylation is an ancestral hallmark of early development in animals Journal Article In: Molecular Biology and Evolution, vol. 40, iss. 6, 2023. |
2022 |
Ctenophores are direct developers that reproduce continuously beginning very early after hatching Journal Article In: Proceedings of the National Academy of Sciences, vol. 119, no. 18, 2022. |
2020 |
Genetic basis for divergence in developmental gene expression in two closely related sea urchins Journal Article In: Nature Ecology & Evolution, vol. 4, no. 6, pp. 831–840, 2020. |