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The Evolution of Invertebrate Animals

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A special issue of Genes (ISSN 2073-4425). This special issue belongs to the section "Animal Genetics and Genomics".

Deadline for manuscript submissions: closed (15 June 2021) | Viewed by 42487

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Dr. Hector Escriva

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Guest Editor

Biologie Intégrative des Organismes Marins (BIOM), Sorbonne Université, CNRS, Banyuls-sur-Mer, France
Interests: amphioxus, EvoDevo, evolution, development

Dr. Stephanie Bertrand

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Guest Editor

Biologie Intégrative des Organismes Marins (BIOM), Sorbonne Université, CNRS, Banyuls-sur-Mer, France
Interests: amphioxus; EvoDevo; evolution; development

Special Issue Information

Dear colleagues,

The current diversity of metazoans has been achieved through a long process of evolution since the appearance of their unicellular ancestor about 1000 Mya. This evolutionary process has generated about 35–37 extant phyla of animals, which are composed by invertebrate animals, with the exception of a single subphylum, the vertebrates. Currently, the number of described living metazoan species is around 1,162,000, among which only about 50,000 are vertebrates (about 5%). In addition, invertebrate animals have been able to adapt to all types of ecosystems, both aquatic and terrestrial, making the study of the diversity and evolution of invertebrates essential to understanding extant animal biology.

To summarize the history of research on invertebrates or based on invertebrate animals would be too extensive. However, it should be noted that since its creation, the Nobel prize has on many occasions been awarded to researchers using invertebrate models. Some examples include research using Drosophila as a model (e.g., the role of chromosomes in heredity, circadian rhythm, mechanisms of innate immunity, odorant receptors, genetic control of early embryonic development), C. elegans (the mechanisms of programmed cell death, RNA interference), sea urchin (key regulators of the cell cycle), sea slug (signal transduction in the nervous system), bees (organization of social and behavior patterns), crabs (physiological and chemical visual processes), octopus (the ionic mechanisms involved in excitation and inhibition in the peripheral and central portions of the nerve cell membrane), or jellyfish (for the discovery and development of the green fluorescent protein, GFP).

In addition to this long history of invertebrate model-based research, we are now living in an exceptional era for two major reasons: first, because the first complete genome of an invertebrate animal has been sequenced (that of C. elegans in 2000) and thanks to the rapid development of NGS techniques, we now have access to about 1000 complete genome sequences of invertebrate animal species (deposited in the NCBI database) and, second, because thanks to the development of simple genome modification techniques, such as CRISPR or TALEN, we can carry out a series of functional experiments that were unthinkable even just a few years ago.

In this Special Issue, we aim to highlight research on “The Evolution of Invertebrate Animals”. We invite submissions of either review or original research articles on any aspect of research using invertebrate animal models. We invite studies that use genetic, genomic, and functional approaches to unravel basic questions of evolutionary biology on different invertebrate phyla.

Dr. Hector Escriva
Dr. Stephanie Bertrand
Guest Editors

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Keywords

Invertebrate
Evolution
Adaptation
Diversity
Genome editing
Phylogeny
Evo-Devo
Eco-Evo-Devo
Genomics
Epigenomics

Published Papers (12 papers)

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Editorial

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3 pages, 185 KiB

Open AccessEditorial

The Evolution of Invertebrate Animals

by Stephanie Bertrand and Hector Escriva

Genes 2022, 13(3), 454; https://doi.org/10.3390/genes13030454 - 2 Mar 2022

Cited by 2 | Viewed by 2703

Abstract

The current diversity of metazoans has been achieved through a long process of evolution since the appearance of their unicellular ancestor about 1000 Mya [...] Full article

(This article belongs to the Special Issue The Evolution of Invertebrate Animals)

Research

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16 pages, 8886 KiB

Open AccessArticle

Hydrophilic Shell Matrix Proteins of Nautilus pompilius and the Identification of a Core Set of Conchiferan Domains

by Davin H. E. Setiamarga, Kazuki Hirota, Masa-aki Yoshida, Yusuke Takeda, Keiji Kito, Makiko Ishikawa, Keisuke Shimizu, Yukinobu Isowa, Kazuho Ikeo, Takenori Sasaki and Kazuyoshi Endo

Genes 2021, 12(12), 1925; https://doi.org/10.3390/genes12121925 - 29 Nov 2021

Cited by 7 | Viewed by 3315

Abstract

Despite being a member of the shelled mollusks (Conchiferans), most members of extant cephalopods have lost their external biomineralized shells, except for the basally diverging Nautilids. Here, we report the result of our study to identify major Shell Matrix Proteins and their domains in the Nautilid Nautilus pompilius, in order to gain a general insight into the evolution of Conchiferan Shell Matrix Proteins. In order to do so, we performed a multiomics study on the shell of N. pompilius, by conducting transcriptomics of its mantle tissue and proteomics of its shell matrix. Analyses of obtained data identified 61 distinct shell-specific sequences. Of the successfully annotated 27 sequences, protein domains were predicted in 19. Comparative analysis of Nautilus sequences with four Conchiferans for which Shell Matrix Protein data were available (the pacific oyster, the pearl oyster, the limpet and the Euhadra snail) revealed that three proteins and six protein domains were conserved in all Conchiferans. Interestingly, when the terrestrial Euhadra snail was excluded, another five proteins and six protein domains were found to be shared among the four marine Conchiferans. Phylogenetic analyses indicated that most of these proteins and domains were probably present in the ancestral Conchiferan, but employed in shell formation later and independently in most clades. Even though further studies utilizing deeper sequencing techniques to obtain genome and full-length sequences, and functional analyses, must be carried out in the future, our results here provide important pieces of information for the elucidation of the evolution of Conchiferan shells at the molecular level. Full article

(This article belongs to the Special Issue The Evolution of Invertebrate Animals)

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14 pages, 4431 KiB

Open AccessArticle

Expansion and Diversification of Fluorescent Protein Genes in Fifteen Acropora Species during the Evolution of Acroporid Corals

by Rio Kashimoto, Kanako Hisata, Chuya Shinzato, Noriyuki Satoh and Eiichi Shoguchi

Genes 2021, 12(3), 397; https://doi.org/10.3390/genes12030397 - 11 Mar 2021

Cited by 3 | Viewed by 3212

Abstract

In addition to a purple, non-fluorescent chromoprotein (ChrP), fluorescent proteins (FPs) account for the vivid colors of corals, which occur in green (GFP), cyan (CFP), and red (RFP) FPs. To understand the evolution of the coral FP gene family, we examined the genomes of 15 Acropora species and three confamilial taxa. This genome-wide survey identified 219 FP genes. Molecular phylogeny revealed that the 15 Acropora species each have 9–18 FP genes, whereas the other acroporids examined have only two, suggesting a pronounced expansion of the FP genes in the genus Acropora. The data estimates of FP gene duplication suggest that the last common ancestor of the Acropora species that survived in the period of high sea surface temperature (Paleogene period) has already gained 16 FP genes. Different evolutionary histories of lineage-specific duplication and loss were discovered among GFP/CFPs, RFPs, and ChrPs. Synteny analysis revealed core GFP/CFP, RFP, and ChrP gene clusters, in which a tandem duplication of the FP genes was evident. The expansion and diversification of Acropora FPs may have contributed to the present-day richness of this genus. Full article

(This article belongs to the Special Issue The Evolution of Invertebrate Animals)

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9 pages, 2488 KiB

Open AccessArticle

Expression Pattern of Nitric Oxide Synthase during Development of the Marine Gastropod Mollusc, Crepidula fornicata

by Marta Truchado-Garcia, Filomena Caccavale, Cristina Grande and Salvatore D’Aniello

Genes 2021, 12(2), 314; https://doi.org/10.3390/genes12020314 - 22 Feb 2021

Cited by 7 | Viewed by 2289

Abstract

Nitric Oxide (NO) plays a key role in the induction of larval metamorphosis in several invertebrate phyla. The inhibition of the NO synthase in Crepidula fornicata, a molluscan model for evolutionary, developmental, and ecological research, has been demonstrated to block the initiation of metamorphosis highlighting that endogenous NO is crucial in the control of this developmental and morphological process. Nitric Oxide Synthase contributes to the development of shell gland, digestive gland and kidney, being expressed in cells that presumably correspond to FMRF-amide, serotoninergic and catecolaminergic neurons. Here we identified a single Nos gene in embryonic and larval transcriptomes of C. fornicata and studied its localization during development, through whole-mount in situ hybridization, in order to compare its expression pattern with that of other marine invertebrate animal models. Full article

(This article belongs to the Special Issue The Evolution of Invertebrate Animals)

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14 pages, 2317 KiB

Open AccessArticle

WNT-FRIZZLED-LRP5/6 Signaling Mediates Posterior Fate and Proliferation during Planarian Regeneration

by Eudald Pascual-Carreras, Miquel Sureda-Gómez, Ramon Barrull-Mascaró, Natàlia Jordà, Maria Gelabert, Pablo Coronel-Córdoba, Emili Saló and Teresa Adell

Genes 2021, 12(1), 101; https://doi.org/10.3390/genes12010101 - 15 Jan 2021

Cited by 8 | Viewed by 3684

Abstract

An organizer is defined as a group of cells that secrete extracellular proteins that specify the fate of surrounding cells according to their concentration. Their function during embryogenesis is key in patterning new growing tissues. Although organizers should also participate in adult development when new structures are regenerated, their presence in adults has only been identified in a few species with striking regenerative abilities, such as planarians. Planarians provide a unique model to understand the function of adult organizers, since the presence of adult pluripotent stem cells provides them with the ability to regenerate any body part. Previous studies have shown that the differential activation of the WNT/β-catenin signal in each wound is fundamental to establish an anterior or a posterior organizer in the corresponding wound. Here, we identify the receptors that mediate the WNT/β-catenin signal in posterior-facing wounds. We found that Wnt1-Fzd1-LRP5/6 signaling is evolutionarily conserved in executing a WNT/β-catenin signal to specify cell fate and to trigger a proliferative response. Our data allow a better understanding of the mechanism through which organizers signal to a “competent” field of cells and integrate the patterning and growth required during de novo formation of organs and tissues. Full article

(This article belongs to the Special Issue The Evolution of Invertebrate Animals)

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13 pages, 1925 KiB

Open AccessArticle

The ADAR Family in Amphioxus: RNA Editing and Conserved Orthologous Site Predictions

by Michał Zawisza-Álvarez, Claudia Pérez-Calles, Giacomo Gattoni, Jordi Garcia-Fernàndez, Èlia Benito-Gutiérrez and Carlos Herrera-Úbeda

Genes 2020, 11(12), 1440; https://doi.org/10.3390/genes11121440 - 30 Nov 2020

Cited by 2 | Viewed by 3558

Abstract

RNA editing is a relatively unexplored process in which transcribed RNA is modified at specific nucleotides before translation, adding another level of regulation of gene expression. Cephalopods use it extensively to increase the regulatory complexity of their nervous systems, and mammals use it too, but less prominently. Nevertheless, little is known about the specifics of RNA editing in most of the other clades and the relevance of RNA editing from an evolutionary perspective remains unknown. Here we analyze a key element of the editing machinery, the ADAR (adenosine deaminase acting on RNA) gene family, in an animal with a key phylogenetic position at the root of chordates: the cephalochordate amphioxus. We show, that as in cephalopods, ADAR genes in amphioxus are predominantly expressed in the nervous system; we identify a number of RNA editing events in amphioxus; and we provide a newly developed method to identify RNA editing events in highly polymorphic genomes using orthology as a guide. Overall, our work lays the foundations for future comparative analysis of RNA-editing events across the metazoan tree. Full article

(This article belongs to the Special Issue The Evolution of Invertebrate Animals)

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15 pages, 5184 KiB

Open AccessArticle

Role of PB1 Midbody Remnant Creating Tethered Polar Bodies during Meiosis II

by Alex McDougall, Celine Hebras, Gerard Pruliere, David Burgess, Vlad Costache, Remi Dumollard and Janet Chenevert

Genes 2020, 11(12), 1394; https://doi.org/10.3390/genes11121394 - 24 Nov 2020

Cited by 2 | Viewed by 2426

Abstract

Polar body (PB) formation is an extreme form of unequal cell division that occurs in oocytes due to the eccentric position of the small meiotic spindle near the oocyte cortex. Prior to PB formation, a chromatin-centered process causes the cortex overlying the meiotic chromosomes to become polarized. This polarized cortical subdomain marks the site where a cortical protrusion or outpocket forms at the oocyte surface creating the future PBs. Using ascidians, we observed that PB1 becomes tethered to the fertilized egg via PB2, indicating that the site of PB1 cytokinesis directed the precise site for PB2 emission. We therefore studied whether the midbody remnant left behind following PB1 emission was involved, together with the egg chromatin, in defining the precise cortical site for PB2 emission. During outpocketing of PB2 in ascidians, we discovered that a small structure around 1 µm in diameter protruded from the cortical outpocket that will form the future PB2, which we define as the “polar corps”. As emission of PB2 progressed, this small polar corps became localized between PB2 and PB1 and appeared to link PB2 to PB1. We tested the hypothesis that this small polar corps on the surface of the forming PB2 outpocket was the midbody remnant from the previous round of PB1 cytokinesis. We had previously discovered that Plk1::Ven labeled midbody remnants in ascidian embryos. We therefore used Plk1::Ven to follow the dynamics of the PB1 midbody remnant during meiosis II. Plk1::Ven strongly labeled the small polar corps that formed on the surface of the cortical outpocket that created PB2. Following emission of PB2, this polar corps was rich in Plk1::Ven and linked PB2 to PB1. By labelling actin (with TRITC-Phalloidin) we also demonstrated that actin accumulates at the midbody remnant and also forms a cortical cap around the midbody remnant in meiosis II that prefigured the precise site of cortical outpocketing during PB2 emission. Phalloidin staining of actin and immunolabelling of anti-phospho aPKC during meiosis II in fertilized eggs that had PB1 removed suggested that the midbody remnant remained within the fertilized egg following emission of PB1. Dynamic imaging of microtubules labelled with Ens::3GFP, MAP7::GFP or EB3::3GFP showed that one pole of the second meiotic spindle was located near the midbody remnant while the other pole rotated away from the cortex during outpocketing. Finally, we report that failure of the second meiotic spindle to rotate can lead to the formation of two cortical outpockets at anaphase II, one above each set of chromatids. It is not known whether the midbody remnant of PB1 is involved in directing the precise location of PB2 since our data are correlative in ascidians. However, a review of the literature indicates that PB1 is tethered to the egg surface via PB2 in several species including members of the cnidarians, lophotrochozoa and echinoids, suggesting that the midbody remnant formed during PB1 emission may be involved in directing the precise site of PB2 emission throughout the invertebrates. Full article

(This article belongs to the Special Issue The Evolution of Invertebrate Animals)

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9 pages, 2373 KiB

Open AccessArticle

Application of CRISPR/Cas9 Nuclease in Amphioxus Genome Editing

by Liuru Su, Chenggang Shi, Xin Huang, Yiquan Wang and Guang Li

Genes 2020, 11(11), 1311; https://doi.org/10.3390/genes11111311 - 5 Nov 2020

Cited by 9 | Viewed by 2842

Abstract

The cephalochordate amphioxus is a promising animal model for studying the origin of vertebrates due to its key phylogenetic position among chordates. Although transcription activator-like effector nucleases (TALENs) have been adopted in amphioxus genome editing, its labor-intensive construction of TALEN proteins limits its usage in many laboratories. Here we reported an application of the CRISPR/Cas9 system, a more amenable genome editing method, in this group of animals. Our data showed that while co-injection of Cas9 mRNAs and sgRNAs into amphioxus unfertilized eggs caused no detectable mutations at targeted loci, injections of Cas9 mRNAs and sgRNAs at the two-cell stage, or of Cas9 protein and sgRNAs before fertilization, can execute efficient disruptions of targeted genes. Among the nine tested sgRNAs (targeting five genes) co-injected with Cas9 protein, seven introduced mutations with efficiency ranging from 18.4% to 90% and four caused specific phenotypes in the injected embryos. We also demonstrated that monomerization of sgRNAs via thermal treatment or modifying the sgRNA structure could increase mutation efficacies. Our study will not only promote application of genome editing method in amphioxus research, but also provide valuable experiences for other organisms in which the CRISPR/Cas9 system has not been successfully applied. Full article

(This article belongs to the Special Issue The Evolution of Invertebrate Animals)

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13 pages, 8149 KiB

Open AccessArticle

Rimbp, a New Marker for the Nervous System of the Tunicate Ciona robusta

by Ugo Coppola, Paola Olivo, Enrico D’Aniello, Christopher J. Johnson, Alberto Stolfi and Filomena Ristoratore

Genes 2020, 11(9), 1006; https://doi.org/10.3390/genes11091006 - 27 Aug 2020

Cited by 3 | Viewed by 2527

Abstract

Establishment of presynaptic mechanisms by proteins that regulate neurotransmitter release in the presynaptic active zone is considered a fundamental step in animal evolution. Rab3 interacting molecule-binding proteins (Rimbps) are crucial components of the presynaptic active zone and key players in calcium homeostasis. Although Rimbp involvement in these dynamics has been described in distantly related models such as fly and human, the role of this family in most invertebrates remains obscure. To fill this gap, we defined the evolutionary history of Rimbp family in animals, from sponges to mammals. We report, for the first time, the expression of the two isoforms of the unique Rimbp family member in Ciona robusta in distinct domains of the larval nervous system. We identify intronic enhancers that are able to drive expression in different nervous system territories partially corresponding to Rimbp endogenous expression. The analysis of gene expression patterns and the identification of regulatory elements of Rimbp will positively impact our understanding of this family of genes in the context of Ciona embryogenesis. Full article

(This article belongs to the Special Issue The Evolution of Invertebrate Animals)

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Review

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21 pages, 2244 KiB

Open AccessReview

Diversity of Modes of Reproduction and Sex Determination Systems in Invertebrates, and the Putative Contribution of Genetic Conflict

by Marion Anne Lise Picard, Beatriz Vicoso, Stéphanie Bertrand and Hector Escriva

Genes 2021, 12(8), 1136; https://doi.org/10.3390/genes12081136 - 27 Jul 2021

Cited by 15 | Viewed by 5995

Abstract

About eight million animal species are estimated to live on Earth, and all except those belonging to one subphylum are invertebrates. Invertebrates are incredibly diverse in their morphologies, life histories, and in the range of the ecological niches that they occupy. A great variety of modes of reproduction and sex determination systems is also observed among them, and their mosaic-distribution across the phylogeny shows that transitions between them occur frequently and rapidly. Genetic conflict in its various forms is a long-standing theory to explain what drives those evolutionary transitions. Here, we review (1) the different modes of reproduction among invertebrate species, highlighting sexual reproduction as the probable ancestral state; (2) the paradoxical diversity of sex determination systems; (3) the different types of genetic conflicts that could drive the evolution of such different systems. Full article

(This article belongs to the Special Issue The Evolution of Invertebrate Animals)

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24 pages, 3910 KiB

Open AccessReview

Neuromesodermal Lineage Contribution to CNS Development in Invertebrate and Vertebrate Chordates

by Clare Hudson and Hitoyoshi Yasuo

Genes 2021, 12(4), 592; https://doi.org/10.3390/genes12040592 - 17 Apr 2021

Cited by 9 | Viewed by 3534

Abstract

Ascidians are invertebrate chordates and the closest living relative to vertebrates. In ascidian embryos a large part of the central nervous system arises from cells associated with mesoderm rather than ectoderm lineages. This seems at odds with the traditional view of vertebrate nervous system development which was thought to be induced from ectoderm cells, initially with anterior character and later transformed by posteriorizing signals, to generate the entire anterior-posterior axis of the central nervous system. Recent advances in vertebrate developmental biology, however, show that much of the posterior central nervous system, or spinal cord, in fact arises from cells that share a common origin with mesoderm. This indicates a conserved role for bi-potential neuromesoderm precursors in chordate CNS formation. However, the boundary between neural tissue arising from these distinct neural lineages does not appear to be fixed, which leads to the notion that anterior-posterior patterning and neural fate formation can evolve independently. Full article

(This article belongs to the Special Issue The Evolution of Invertebrate Animals)

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21 pages, 1392 KiB

Open AccessReview

Nuclear Receptors and Development of Marine Invertebrates

by Angelica Miglioli, Laura Canesi, Isa D. L. Gomes, Michael Schubert and Rémi Dumollard

Genes 2021, 12(1), 83; https://doi.org/10.3390/genes12010083 - 11 Jan 2021

Cited by 18 | Viewed by 3682

Abstract

Nuclear Receptors (NRs) are a superfamily of transcription factors specific to metazoans that have the unique ability to directly translate the message of a signaling molecule into a transcriptional response. In vertebrates, NRs are pivotal players in countless processes of both embryonic and adult physiology, with embryonic development being one of the most dynamic periods of NR activity. Accumulating evidence suggests that NR signaling is also a major regulator of development in marine invertebrates, although ligands and transactivation dynamics are not necessarily conserved with respect to vertebrates. The explosion of genome sequencing projects and the interpretation of the resulting data in a phylogenetic context allowed significant progress toward an understanding of NR superfamily evolution, both in terms of molecular activities and developmental functions. In this context, marine invertebrates have been crucial for characterizing the ancestral states of NR-ligand interactions, further strengthening the importance of these organisms in the field of evolutionary developmental biology. Full article

(This article belongs to the Special Issue The Evolution of Invertebrate Animals)

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