Coupled genomic evolutionary histories as signatures of organismal innovations in cephalopods: co-evolutionary signatures across levels of genome organization may shed light on functional linkage and origin of cephalopod novelties

© The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Ritschard, E. A., Whitelaw, B., Albertin, C. B., Cooke, I. R., Strugnell, J. M., & Simakov, O. Coupled genomic evolutionary histories as signatures of organismal innovations in cephalopods: co-evolutionary signatures across levels of genome organization may shed light on functional linkage and origin of cephalopod novelties. BioEssays, 41, (2019): 1900073, doi: 10.1002/bies.201900073.How genomic innovation translates into organismal organization remains largely unanswered. Possessing the largest invertebrate nervous system, in conjunction with many species‐specific organs, coleoid cephalopods (octopuses, squids, cuttlefishes) provide exciting model systems to investigate how organismal novelties evolve. However, dissecting these processes requires novel approaches that enable deeper interrogation of genome evolution. Here, the existence of specific sets of genomic co‐evolutionary signatures between expanded gene families, genome reorganization, and novel genes is posited. It is reasoned that their co‐evolution has contributed to the complex organization of cephalopod nervous systems and the emergence of ecologically unique organs. In the course of reviewing this field, how the first cephalopod genomic studies have begun to shed light on the molecular underpinnings of morphological novelty is illustrated and their impact on directing future research is described. It is argued that the application and evolutionary profiling of evolutionary signatures from these studies will help identify and dissect the organismal principles of cephalopod innovations. By providing specific examples, the implications of this approach both within and beyond cephalopod biology are discussed.E.A.R. and O.S. are supported by the Austrian Science Fund (Grant No. P30686‐B29). E.A.R. is supported by Stazione Zoologica Anton Dohrn (Naples, Italy) PhD Program. The authors wish to thank Graziano Fiorito (SZN, Italy), Hannah Schmidbaur (University of Vienna, Austria), Thomas Hummel (University of Vienna, Austria) for many insightful comments and reading of the draft manuscript. The authors would like to apologize to all colleagues whose work has been omitted due to space constraints

Analysis of psychomotor development and level of physical activity of children with extracurricular physical activities

Objetivo: Avaliar o desenvolvimento psicomotor nas áreas de habilidades motoras globais, equilíbrio e estrutura corporal e nível de atividade extracurricular escolar. Método: A amostra foi constituída por 30 indivíduos de ambos os sexos de 6 a 10 anos de idade, divididos em dois grupos: Grupo Extracurricular Ativo e Grupo Extracurricular Sedentário. A coleta de dados incluiu a caracterização dos sujeitos, os dados antropométricos e os testes Development Scale Motor e a versão curta do IPAQ. As variáveis ​​foram expressas em frequências e proporções, sendo o teste de Shapiro-Wilk utilizado e o teste t de Student para determinar a significância estatística. Quanto aos dados não normais, utilizou-se o teste de Mann Whitney, que foi considerado estatisticamente significativo p <0,05. Resultados: Mostraram que a classificação de IMC / idade de ambos os grupos foi eutrófica (53,3%) e o restante (46,6%) apresentou sobrepeso. O grupo sedentário apresentou melhores resultados no desenvolvimento motor global, e o grupo ativo no esquema do equilíbrio e do corpo. Conclusão: As crianças que realizam atividade extracurricular apresentaram melhor desenvolvimento de equilíbrio e estrutura corporal, quando comparadas com aquelas que não o fizeram.         Objective: The objective was to evaluate the psychomotor development in the areas of global motor skills, balance and body structure and level of school extracurricular physical activity. Method: The sample consisted of 30 individuals of both sexes from 6 to 10 years old, divided into two groups: Active Extracurricular Group and Sedentary Extracurricular Group. Data collection included the characterization of the subjects, anthropometric data, and the tests Development Scale Motor and the IPAQ short version. The variables were expressed as frequencies and proportions, the normality was tested with the Shapiro-Wilk test. Student t test was used to determine the statistical significance of normal data and Mann Whitney test for the non-normal data. Statistical significance was set at p0.05. Results: The classification of BMI / age of both groups was eutrophic (53.3%) and the remainder (46.6%) were overweight. The sedentary group had better results in overall motor development, and the active group in balance and body scheme. Conclusion: The children who engage in extracurricular physical activity showed better development in balance and body structure, when compared to those that do no

The emergence of the brain non-CpG methylation system in vertebrates

Mammalian brains feature exceptionally high levels of non-CpG DNA methylation alongside the canonical form of CpG methylation. Non-CpG methylation plays a critical regulatory role in cognitive function, which is mediated by the binding of MeCP2, the transcriptional regulator that when mutated causes Rett syndrome. However, it is unclear whether the non-CpG neural methylation system is restricted to mammalian species with complex cognitive abilities or has deeper evolutionary origins. To test this, we investigated brain DNA methylation across 12 distantly related animal lineages, revealing that non-CpG methylation is restricted to vertebrates. We discovered that in vertebrates, non-CpG methylation is enriched within a highly conserved set of developmental genes transcriptionally repressed in adult brains, indicating that it demarcates a deeply conserved regulatory program. We also found that the writer of non-CpG methylation, DNMT3A, and the reader, MeCP2, originated at the onset of vertebrates as a result of the ancestral vertebrate whole-genome duplication. Together, we demonstrate how this novel layer of epigenetic information assembled at the root of vertebrates and gained new regulatory roles independent of the ancestral form of the canonical CpG methylation. This suggests that the emergence of non-CpG methylation may have fostered the evolution of sophisticated cognitive abilities found in the vertebrate lineage.This work was supported by the Australian Research Council (ARC) Centre of Excellence programme in Plant Energy Biology (grant no. CE140100008). R.L. was supported by a Sylvia and Charles Viertel Senior Medical Research Fellowship, ARC Future Fellowship (no. FT120100862) and Howard Hughes Medical Institute International Research Scholarship. A.d.M. was funded by an EMBO long-term fellowship (no. ALTF 144-2014). J.L.G.-S. was supported by the Spanish government (grant no. BFU2016- 74961-P) and the institutional grant Unidad de Excelencia María de Maeztu (no. MDM-2016-0687). B.V. was supported by the Biomedical Research Council of the Agency for Science, Technology and Research of Singapore. F.G. was supported by an ARC Future Fellowship (no. FT160100267). C.W.R. was supported by an NSF grant (no. IOS-1354898). J.R.E. is an investigator of the Howard Hughes Medical Institute. Genomic data was generated at the Australian Cancer Research Foundation Centre for Advanced Cancer Genomics

Cephalopod genomics: a plan of strategies and organization

The Cephalopod Sequencing Consortium (CephSeq Consortium) was established at a NESCent Catalysis Group Meeting, "Paths to Cephalopod Genomics-Strategies, Choices, Organization," held in Durham, North Carolina, USA on May 24-27, 2012. Twenty-eight participants representing nine countries (Austria, Australia, China, Denmark, France, Italy, Japan, Spain and the USA) met to address the pressing need for genome sequencing of cephalopod mollusks. This group, drawn from cephalopod biologists, neuroscientists, developmental and evolutionary biologists, materials scientists, bioinformaticians and researchers active in sequencing, assembling and annotating genomes, agreed on a set of cephalopod species of particular importance for initial sequencing and developed strategies and an organization (CephSeq Consortium) to promote this sequencing. The conclusions and recommendations of this meeting are described in this white paper

Cephalopod genomics : a plan of strategies and organization

© The Author(s), 2012. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Standards in Genomic Sciences 7 (2012): 175-188, doi:10.4056/sigs.3136559.The Cephalopod Sequencing Consortium (CephSeq Consortium) was established at a NESCent Catalysis Group Meeting, “Paths to Cephalopod Genomics- Strategies, Choices, Organization,” held in Durham, North Carolina, USA on May 24-27, 2012. Twenty-eight participants representing nine countries (Austria, Australia, China, Denmark, France, Italy, Japan, Spain and the USA) met to address the pressing need for genome sequencing of cephalopod molluscs. This group, drawn from cephalopod biologists, neuroscientists, developmental and evolutionary biologists, materials scientists, bioinformaticians and researchers active in sequencing, assembling and annotating genomes, agreed on a set of cephalopod species of particular importance for initial sequencing and developed strategies and an organization (CephSeq Consortium) to promote this sequencing. The conclusions and recommendations of this meeting are described in this White Paper.The Catalysis Group Meeting was supported by the National Science Foundation through the National Evolutionary Synthesis Center (NESCent) under grant number NSF #EF-0905606

The Molecular Embryology of a Cephalopod Mollusc, Octopus bimaculoides

Cephalopods have a highly derived body plan and a suite of innovations with no obvious correlates in other animals. One of the most striking novelties in cephalopods is their embryogenesis, which lacks any trace of the spiral cleavage pattern found in non-cephalopod molluscs and other spiralians. Instead, cephalopod embryos undergo bilateral, meroblastic cleavage on top of a large yolk, greatly resembling early embryogenesis in fish and constituting a striking convergence between these two distantly related groups. In this thesis, I explore cephalopod development from a molecular perspective, leveraging genomics, transcriptomics, and gene expression studies to shed light on the development of these remarkable animals. To identify the gene networks important in this highly derived developmental program, we analyzed the genome and transcriptomes of the California two-spot octopus, Octopus bimaculoides. The core developmental gene repertoire of the octopus is broadly similar to that found in typical invertebrate bilaterians, except for massive expansions in the protocadherins and the C2H2 zinc finger transcription factor gene families. I identified hundreds of cephalopod-specific genes, many of which showed elevated expression levels in such specialized cephalopod structures as the skin, the suckers, and the nervous system. Comparative genome structure analysis suggests that substantial expansion of a handful of gene families, along with extensive remodeling of genome linkages, drove the evolution of cephalopod morphological novelties. A prominent cephalopod innovation is their large, complex nervous system. The morphological structure of the cephalopod embryonic brain was studied with molecular markers of neuronal development. Expression of pan-neuronal genes indicated that early neurogenic territories in octopus are arranged as concentric cords rather than pairs of ganglia, an arrangement hypothesized to be characteristic of the ancestral molluscan nervous system. The expression of a highly conserved developmental transcription factor cassette that is characteristic of the vertebrate midbrain-hindbrain boundary identified the major division in the cephalopod brain, that between the supraesophageal and subesophageal masses. Similar to the vertebrate midbrain-hindbrain boundary, this territory is a signaling center, although the signaling ligands detected in octopus are greatly expanded from those described in other animals. Gene expression study later in development indicated a shared transcription factor “fingerprint” between cephalopods and other animals of neurosecretory and higher motor centers. In contrast, the cephalopod frontal-vertical system, which is a higher integrative center implicated in learning, memory and decision-making, proved to have a different molecular signature from that of the analogous structures in vertebrates and annelids. Finally, I examined the deployment of highly conserved developmental toolkit genes using both bioinformatics and gene expression. Analysis of Hox gene expression indicated that, despite the absence of a Hox genomic cluster, these genes are expressed in a canonical pattern of anterior-posterior nested domains, one modified to reflect the radial morphology of the cephalopod embryo. Bioinformatic analyses detected the Hox genes and other highly conserved developmental toolkit genes primarily during stages that coincide with the emergence of the body plan, but not before. Notably, many of the genes differentially expressed in the early transcriptomes are taxonomically restricted. Our results support a mid-developmental period of highly conserved toolkit gene expression preceded by the deployment of taxonomically restricted genes. These results suggest the surprising conclusion that it is cephalopod-specific genes that underlie the “fish-like” embryogenesis of cephalopods

Genome and transcriptome mechanisms driving cephalopod evolution.

Cephalopods are known for their large nervous systems, complex behaviors and morphological innovations. To investigate the genomic underpinnings of these features, we assembled the chromosomes of the Boston market squid, Doryteuthis (Loligo) pealeii, and the California two-spot octopus, Octopus bimaculoides, and compared them with those of the Hawaiian bobtail squid, Euprymna scolopes. The genomes of the soft-bodied (coleoid) cephalopods are highly rearranged relative to other extant molluscs, indicating an intense, early burst of genome restructuring. The coleoid genomes feature multi-megabase, tandem arrays of genes associated with brain development and cephalopod-specific innovations. We find that a known coleoid hallmark, extensive A-to-I mRNA editing, displays two fundamentally distinct patterns: one exclusive to the nervous system and concentrated in genic sequences, the other widespread and directed toward repetitive elements. We conclude that coleoid novelty is mediated in part by substantial genome reorganization, gene family expansion, and tissue-dependent mRNA editing