Ambulacrarian insulin-related peptides and their putative receptors suggest how insulin and similar peptides may have evolved from insulin-like growth factor

Background Some insulin/IGF-related peptides (irps) stimulate a receptor tyrosine kinase (RTK) that transfers the extracellular hormonal signal into an intracellular response. Other irps, such as relaxin, do not use an RTK, but a G-protein coupled receptor (GPCR). This is unusual since evolutionarily related hormones typically either use the same or paralogous receptors. In arthropods three different irps, i.e. arthropod IGF, gonadulin and Drosophila insulin-like peptide 7 (dilp7), likely evolved from a gene triplication, as in several species genes encoding these three peptides are located next to one another on the same chromosomal fragment. These arthropod irps have homologs in vertebrates, suggesting that the initial gene triplication was perhaps already present in the last common ancestor of deuterostomes and protostomes. It would be interesting to know whether this is indeed so and how insulin might be related to this trio of irps. Methodology Genes encoding irps as well as their putative receptors were identified in genomes and transcriptomes from echinoderms and hemichordates. Results A similar triplet of genes coding for irps also occurs in some ambulacrarians. Two of these are orthologs of arthropod IGF and dilp7 and the third is likely a gonadulin ortholog. In echinoderms, two novel irps emerged, gonad stimulating substance (GSS) and multinsulin, likely from gene duplications of the IGF and dilp7-like genes respectively. The structures of GSS diverged considerably from IGF, which would suggest they use different receptors from IGF, but no novel irp receptors evolved. If IGF and GSS use different receptors, and the evolution of GSS from a gene duplication of IGF is not associated with the appearance of a novel receptor, while irps are known to use two different types of receptors, the ancestor of GSS and IGF might have acted on both types of receptors while one or both of its descendants act on only one. There are three ambulacrarian GPCRs that have amino acid sequences suggestive of being irp GPCRs, two of these are orthologs of the gonadulin and dilp7 receptors. This suggests that the third might be an IGF receptor, and that by deduction, GSS only acts on the RTK. The evolution of GSS from IGF may represent a pattern, where IGF gene duplications lead to novel genes coding for shorter peptides that activate an RTK. It is likely this is how insulin and the insect neuroendocrine irps evolved independently from IGF. Conclusion The local gene triplication described from arthropods that yielded three genes encoding irps was already present in the last common ancestor of protostomes and deuterostomes. It seems plausible that irps, such as those produced by neuroendocrine cells in the brain of insects and echinoderm GSS evolved independently from IGF and, thus, are not true orthologs, but the result of convergent evolution.

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Ambulacrarian insulin-related peptides and their putative receptors suggest how insulin and similar peptides may have evolved from Insulin-like Growth Factor

10.1101/2021.04.15.440029 ◽

2021 ◽

Author(s):

Jan Adrianus Veenstra

Keyword(s):

Receptor Tyrosine Kinase ◽

Common Ancestor ◽

Neuroendocrine Cells ◽

Last Common Ancestor ◽

Gene Duplications ◽

Hormonal Signal ◽

Intracellular Response ◽

G Protein Coupled ◽

The Brain ◽

Insulin Like Growth Factors

Background: Insulin is evolutionarily related to the insulin-like growth factors (IGFs) and like the latter stimulates a receptor tyrosine kinase (RTK) that transfers the extracellular hormonal signal into an intracellular response. Other hormones related to insulin, such as relaxin, do not use an RTK, but a G-protein coupled receptor (GPCR). This is unusual since evolutionarily related hormones typically either use the same or paralogous receptors. In arthropods three different IGF-related peptides likely evolved from a gene triplication, as in several species genes coding these three peptides are located next to one another on the same chromosomal fragment. Of these three hormones one, an IGF-like hormone, acts through an RTK, while the other two use a GPCR. This suggests that the ancestral IGF-like peptide may have used both types of receptors. These arthropod insulin-like peptides have homologs in vertebrates, which suggests that the initial gene triplication was perhaps already present in the last common ancestor of deuterostomes and protostomes. It would be interesting to know whether this is indeed so and to establish how insulin and other insulin-like peptides might be related to this trio of IGF-related hormones. Methodology: Genes coding insulin and related peptides as well as their putative receptors were identified in genomes and transcriptomes from echinoderms and hemichordates. Results: A similar triplet of genes coding insulin-like peptides is also found in some hemichordates and echinoderms. Two of the three ambulacrarian peptides are orthologs of arthropod IGF and Drosophila insulin-like peptide 7 (dilp7), while the third one looks like an ortholog of the arthropod peptide gonadulin. In echinoderms two novel insulin-like peptides emerged, gonad stimulating substance (GSS) and multinsulin, likely from gene duplications of the IGF and dilp7-like genes respectively. However, no novel receptors for insulin-like peptides evolved. If IGF were to act through both a GPCR and an RTK it would suggest that GSS acts on only one of the two receptors, possibly the RTK. The evolution of GSS from IGF may represent a pattern, where IGF gene duplications lead to novel genes coding shorter peptides that have lost their ability to activate a GPCR. It is likely this is how insulin and the insect neuroendocrine insulin-like peptides evolved independently from IGF. Conclusion: The local gene triplication previously described from arthropods that yielded three genes coding IGF-related peptides was already present in the last common ancestor of protostomes and deuterostomes. It seems plausible that insulin and other insulin-like peptides, such as those produced by neuroendocrine cells in the brain of insects and echinoderm GSS evolved independently from IGF and thus are not true orthologs, but the result of convergent evolution.

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Evolution of biosynthetic diversity

Biochemical Journal ◽

10.1042/bcj20160823 ◽

2017 ◽

Vol 474 (14) ◽

pp. 2277-2299 ◽

Cited By ~ 19

Author(s):

Anthony J. Michael

Keyword(s):

Common Ancestor ◽

Polyamine Metabolism ◽

Last Common Ancestor ◽

Protein Fold ◽

Last Universal Common Ancestor ◽

Endosymbiotic Gene Transfer ◽

Evolutionary Mechanisms ◽

Universal Common Ancestor ◽

Genes Encoding ◽

Domains Of Life

Since the emergence of the last common ancestor from which all extant life evolved, the metabolite repertoire of cells has increased and diversified. Not only has the metabolite cosmos expanded, but the ways in which the same metabolites are made have diversified. Enzymes catalyzing the same reaction have evolved independently from different protein folds; the same protein fold can produce enzymes recognizing different substrates, and enzymes performing different chemistries. Genes encoding useful enzymes can be transferred between organisms and even between the major domains of life. Organisms that live in metabolite-rich environments sometimes lose the pathways that produce those same metabolites. Fusion of different protein domains results in enzymes with novel properties. This review will consider the major evolutionary mechanisms that generate biosynthetic diversity: gene duplication (and gene loss), horizontal and endosymbiotic gene transfer, and gene fusion. It will also discuss mechanisms that lead to convergence as well as divergence. To illustrate these mechanisms, one of the original metabolisms present in the last universal common ancestor will be employed: polyamine metabolism, which is essential for the growth and cell proliferation of archaea and eukaryotes, and many bacteria.

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Carbonic Anhydrases: An Ancient Tool in Calcareous Sponge Biomineralization

Frontiers in Genetics ◽

10.3389/fgene.2021.624533 ◽

2021 ◽

Vol 12 ◽

Author(s):

Oliver Voigt ◽

Benedetta Fradusco ◽

Carolin Gut ◽

Charalampos Kevrekidis ◽

Sergio Vargas ◽

...

Keyword(s):

Gene Family ◽

Common Ancestor ◽

Last Common Ancestor ◽

Gene Duplications ◽

Carbonic Anhydrases ◽

Temporal Expression ◽

Additional Species ◽

Calcareous Sponges ◽

Membrane Bound

Enzymes of the α-carbonic anhydrase gene family (CAs) are essential for the deposition of calcium carbonate biominerals. In calcareous sponges (phylum Porifera, class Calcarea), specific CAs are involved in the formation of calcite spicules, a unique trait and synapomorphy of this class. However, detailed studies on the CA repertoire of calcareous sponges exist for only two species of one of the two Calcarea subclasses, the Calcaronea. The CA repertoire of the second subclass, the Calcinea, has not been investigated so far, leaving a considerable gap in our knowledge about this gene family in Calcarea. Here, using transcriptomic analysis, phylogenetics, and in situ hybridization, we study the CA repertoire of four additional species of calcareous sponges, including three from the previously unsampled subclass Calcinea. Our data indicate that the last common ancestor of Calcarea had four ancestral CAs with defined subcellular localizations and functions (mitochondrial/cytosolic, membrane-bound, and secreted non-catalytic). The evolution of membrane-bound and secreted CAs involved gene duplications and losses, whereas mitochondrial/cytosolic and non-catalytic CAs are evidently orthologous genes. Mitochondrial/cytosolic CAs are biomineralization-specific genes recruited for biomineralization in the last common ancestor of calcareous sponges. The spatial–temporal expression of these CAs differs between species, which may reflect differences between subclasses or be related to the secondary thickening of spicules during biomineralization that does not occur in all species. With this study, we extend the understanding of the role and the evolution of a key biomineralization gene in calcareous sponges.

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Analysis of fungal genomes reveals commonalities of intron gain or loss and functions in intron-poor species

Molecular Biology and Evolution ◽

10.1093/molbev/msab094 ◽

2021 ◽

Cited By ~ 1

Author(s):

Chun Shen Lim ◽

Brooke N Weinstein ◽

Scott W Roy ◽

Chris M Brown

Keyword(s):

Ribosome Biogenesis ◽

Evolutionary History ◽

Common Ancestor ◽

Intron Loss ◽

Fungal Species ◽

Last Common Ancestor ◽

Intron Evolution ◽

Protein Coding ◽

Genes Encoding ◽

Fungal Genomes

Abstract Previous evolutionary reconstructions have concluded that early eukaryotic ancestors including both the last common ancestor of eukaryotes and of all fungi had intron-rich genomes. By contrast, some extant eukaryotes have few introns, underscoring the complex histories of intron-exon structures, and raising the question as to why these few introns are retained. Here we have used recently available fungal genomes to address a variety of questions related to intron evolution. Evolutionary reconstruction of intron presence and absence using 263 diverse fungal species supports the idea that massive intron reduction through intron loss has occurred in multiple clades. The intron densities estimated in various fungal ancestors differ from zero to 7.6 introns per one kbp of protein-coding sequence. Massive intron loss has occurred not only in microsporidian parasites and saccharomycetous yeasts, but also in diverse smuts and allies. To investigate the roles of the remaining introns in highly-reduced species, we have searched for their special characteristics in eight intron-poor fungi. Notably, the introns of ribosome associated genes RPL7 and NOG2 have conserved positions; both intron-containing genes encoding snoRNAs. Furthermore, both the proteins and snoRNAs are involved in ribosome biogenesis, suggesting that the expression of the protein-coding genes and non-coding snoRNAs may be functionally coordinated. Indeed, these introns are also conserved in three-quarters of fungi species. Our study shows that fungal introns have a complex evolutionary history and underappreciated roles in gene expression.

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Co-expression of synaptic genes in the sponge Amphimedon queenslandica uncovers ancient neural submodules

Scientific Reports ◽

10.1038/s41598-019-51282-x ◽

2019 ◽

Vol 9 (1) ◽

Cited By ~ 3

Author(s):

Eunice Wong ◽

Jan Mölter ◽

Victor Anggono ◽

Sandie M. Degnan ◽

Bernard M. Degnan

Keyword(s):

Common Ancestor ◽

Expression Profiles ◽

Life Cycle Stage ◽

Developmental Expression ◽

Last Common Ancestor ◽

Cell Type ◽

Amphimedon Queenslandica ◽

Genes Encoding ◽

Cell Type Specific ◽

Receptor Clusters

Abstract The synapse is a complex cellular module crucial to the functioning of neurons. It evolved largely through the exaptation of pre-existing smaller submodules, each of which are comprised of ancient sets of proteins that are conserved in modern animals and other eukaryotes. Although these ancient submodules themselves have non-neural roles, it has been hypothesized that they may mediate environmental sensing behaviors in aneural animals, such as sponges. Here we identify orthologues in the sponge Amphimedon queenslandica of genes encoding synaptic submodules in neural animals, and analyse their cell-type specific and developmental expression to determine their potential to be co-regulated. We find that genes comprising certain synaptic submodules, including those involved in vesicle trafficking, calcium-regulation and scaffolding of postsynaptic receptor clusters, are co-expressed in adult choanocytes and during metamorphosis. Although these submodules may contribute to sensory roles in this cell type and this life cycle stage, total synaptic gene co-expression profiles do not support the existence of a functional synapse in A. queenslandica. The lack of evidence for the co-regulation of genes necessary for pre- and post-synaptic functioning in A. queenslandica suggests that sponges, and perhaps the last common ancestor of sponges and other extant animals, had the ability to promulgate sensory inputs without complete synapse-like functionalities. The differential co-expression of multiple synaptic submodule genes in sponge choanocytes, which have sensory and feeding roles, however, is consistent with the metazoan ancestor minimally being able to undergo exo- and endocytosis in a controlled and localized manner.

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Evolution of Antennapedia-Class Homeobox Genes

Genetics ◽

10.1093/genetics/142.1.295 ◽

1996 ◽

Vol 142 (1) ◽

pp. 295-303 ◽

Cited By ~ 1

Author(s):

Jianzhi Zhang ◽

Masatoshi Nei

Keyword(s):

Gene Expression ◽

Homeobox Genes ◽

Amino Acid Sequences ◽

Gene Arrangement ◽

Gene Duplications ◽

Group I ◽

Group 3 ◽

Group Ii ◽

Anterior Posterior

Antennapedia (Antp)-class homeobox genes are involved in the determination of pattern formation along the anterior-posterior axis of the animal embryo. A phylogenetic analysis of Antp-class homeodomains of the nematode, Drosophila, amphioxus, mouse, and human indicates that the 13 cognate group genes of this gene family can be divided into two major groups, i.e., groups I and II. Group I genes can further be divided into subgroups A (cognate groups 1–2), B (cognate group 3), and C (cognate groups 4–8), and group II genes can be divided into subgroups D (cognate groups 9–10) and E (cognate groups 11–13), though this classification is somewhat ambiguous. Evolutionary distances among different amino acid sequences suggest that the divergence between group I and group II genes occurred ∼1000 million years (MY) ago, and the five different subgroups were formed by ∼600 MY ago, probably before the divergence of Pseudocoelomates (e.g., nematodes) and Coelomates (e.g., insects and chordates). Our results show that the genes that are phylogenetically close are also closely located in the chromosome, suggesting that the colinearity between the gene expression and gene arrangement was generated by successive tandem gene duplications and that the gene arrangement has been maintained by some sort of selection.

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A Cluster of Cuticle Protein Genes of Drosophila melanogaster at 65A: Sequence, Structure and Evolution

Genetics ◽

10.1093/genetics/147.3.1213 ◽

1997 ◽

Vol 147 (3) ◽

pp. 1213-1224

Author(s):

Jean-Philippe Charles ◽

Carol Chihara ◽

Shamim Nejad ◽

Lynn M Riddiford

Keyword(s):

Drosophila Melanogaster ◽

Genomic Dna ◽

Multiple Copy ◽

Sequence Structure ◽

Coding Regions ◽

The Third ◽

Genetic Complexity ◽

Genes Encoding ◽

Cuticle Protein ◽

Cuticle Proteins

A 36-kb genomic DNA segment of the Drosophila melanogaster genome containing 12 clustered cuticle genes has been mapped and partially sequenced. The cluster maps at 65A 5-6 on the left arm of the third chromosome, in agreement with the previously determined location of a putative cluster encompassing the genes for the third instar larval cuticle proteins LCP5, LCP6 and LCP8. This cluster is the largest cuticle gene cluster discovered to date and shows a number of surprising features that explain in part the genetic complexity of the LCP5, LCP6 and LCP8 loci. The genes encoding LCP5 and LCP8 are multiple copy genes and the presence of extensive similarity in their coding regions gives the first evidence for gene conversion in cuticle genes. In addition, five genes in the cluster are intronless. Four of these five have arisen by retroposition. The other genes in the cluster have a single intron located at an unusual location for insect cuticle genes.

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The assembled and annotated genome of the pigeon louse Columbicola columbae, a model ectoparasite

G3 Genes|Genome|Genetics ◽

10.1093/g3journal/jkab009 ◽

2021 ◽

Vol 11 (2) ◽

Author(s):

James G Baldwin-Brown ◽

Scott M Villa ◽

Anna I Vickrey ◽

Kevin P Johnson ◽

Sarah E Bush ◽

...

Keyword(s):

Low Cost ◽

Single Copy ◽

Odorant Receptors ◽

Rna Seq ◽

Pediculus Humanus ◽

Final Assembly ◽

Oxford Nanopore ◽

Genes Encoding ◽

Host Parasite ◽

G Protein Coupled

Abstract The pigeon louse Columbicola columbae is a longstanding and important model for studies of ectoparasitism and host-parasite coevolution. However, a deeper understanding of its evolution and capacity for rapid adaptation is limited by a lack of genomic resources. Here, we present a high-quality draft assembly of the C. columbae genome, produced using a combination of Oxford Nanopore, Illumina, and Hi-C technologies. The final assembly is 208 Mb in length, with 12 chromosome-size scaffolds representing 98.1% of the assembly. For gene model prediction, we used a novel clustering method (wavy_choose) for Oxford Nanopore RNA-seq reads to feed into the MAKER annotation pipeline. High recovery of conserved single-copy orthologs (BUSCOs) suggests that our assembly and annotation are both highly complete and highly accurate. Consistent with the results of the only other assembled louse genome, Pediculus humanus, we find that C. columbae has a relatively low density of repetitive elements, the majority of which are DNA transposons. Also similar to P. humanus, we find a reduced number of genes encoding opsins, G protein-coupled receptors, odorant receptors, insulin signaling pathway components, and detoxification proteins in the C. columbae genome, relative to other insects. We propose that such losses might characterize the genomes of obligate, permanent ectoparasites with predictable habitats, limited foraging complexity, and simple dietary regimes. The sequencing and analysis for this genome were relatively low cost, and took advantage of a new clustering technique for Oxford Nanopore RNAseq reads that will be useful to future genome projects.

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Experimental evidence for yawn contagion in orangutans (Pongo pygmaeus)

Scientific Reports ◽

10.1038/s41598-020-79160-x ◽

2020 ◽

Vol 10 (1) ◽

Author(s):

Evy van Berlo ◽

Alejandra P. Díaz-Loyo ◽

Oscar E. Juárez-Mora ◽

Mariska E. Kret ◽

Jorg J. M. Massen

Keyword(s):

Experimental Evidence ◽

Common Ancestor ◽

Great Apes ◽

Pongo Pygmaeus ◽

Last Common Ancestor ◽

Contagious Yawning ◽

Proximate Mechanism ◽

Social Species ◽

Ultimate Causation

AbstractYawning is highly contagious, yet both its proximate mechanism(s) and its ultimate causation remain poorly understood. Scholars have suggested a link between contagious yawning (CY) and sociality due to its appearance in mostly social species. Nevertheless, as findings are inconsistent, CY’s function and evolution remains heavily debated. One way to understand the evolution of CY is by studying it in hominids. Although CY has been found in chimpanzees and bonobos, but is absent in gorillas, data on orangutans are missing despite them being the least social hominid. Orangutans are thus interesting for understanding CY’s phylogeny. Here, we experimentally tested whether orangutans yawn contagiously in response to videos of conspecifics yawning. Furthermore, we investigated whether CY was affected by familiarity with the yawning individual (i.e. a familiar or unfamiliar conspecific and a 3D orangutan avatar). In 700 trials across 8 individuals, we found that orangutans are more likely to yawn in response to yawn videos compared to control videos of conspecifics, but not to yawn videos of the avatar. Interestingly, CY occurred regardless of whether a conspecific was familiar or unfamiliar. We conclude that CY was likely already present in the last common ancestor of humans and great apes, though more converging evidence is needed.

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