Regeneration among animals: An evolutionary hypothesis related to aquatic versus terrestrial environment.

The present hypothesis tries to explain animal regeneration in relation to the life cycles and environment of different animals. Regeneration is a basic phenomenon present since the origin of life in the sea, as testimonial in lower or more complex extant marine animals. Aquatic animals that evolved an indirect development, forming larvae and transiting into the adult stage through metamorphosis, use gene networks present in their genome for these transformations. In case of injury or organ loss as adults, they can re-utilize most or part of the gene networks previously activated during larval growth and metamorphosis. In contrast, terrestrial animals that evolved life cycles with the elimination of larvae and metamorphosis for the adaptation to land conditions lost some of the genes implicated in these post-developmental processes and consequently also the ability to regenerate. Few arthropods and lizards are capable to form hydrated regenerative blastemas with a similar consistence of embryonic tissues. The present hypothesis submits that regeneration cannot be activated in the dry land environment and consequently was largely or completely abolished in terrestrial animals. After injury or organ loss, nematodes, most arthropods and terrestrial vertebrates can only form scars or a limited healing or regengrow in juveniles. This is a process where somatic growth is superimposed to wound healing so that the apparent regeneration derives from the combination from both processes. When full growth is terminated these terrestrial animals can only heal by scarring.

Selection by differential survival among marine animals in the Phanerozoic.

The Gaia hypothesis posits that the Earth and its biosphere function as a single self-stabilizing system, but a key challenge is explaining how this could have arisen through Darwinian evolution. One theory is that of "selection by differential survival," in which a clade's extinction probability decreases with age as it accumulates adaptations resisting environmental disturbances. While this is hard to assess during early Earth history, we can assess whether this process operated among marine animal genera throughout the Phanerozoic. To that end, we analyzed time ranges of 36,117 extinct animal genera using fossil occurrence data from the Paleobiology Database in order to calculate marine metazoan extinction age selectivity, extinction rates, and speciation rates over the Phanerozoic. We identify four signatures of selection by differential survival: lower extinction rates among older lineages, heritability and taxonomically nested propagation of extinction resistance, reduced age selectivity during rare environmental perturbations, and differential extinction rather than speciation as the primary driver of the phenomenon. Evidence for this process at lower taxonomic levels also implies its possibility for life as a whole - indeed, the possibility of Gaia.

The ancestral type of the R-RAS protein has oncogenic potential.

BACKGROUND: The R-RAS2 is a small GTPase highly similar to classical RAS proteins at the regulatory and signaling levels. The high evolutionary conservation of R-RAS2, its links to basic cellular processes and its role in cancer, make R-RAS2 an interesting research topic. To elucidate the evolutionary history of R-RAS proteins, we investigated and compared structural and functional properties of ancestral type R-RAS protein with human R-RAS2. METHODS: Bioinformatics analysis were used to elucidate the evolution of R-RAS proteins. Intrinsic GTPase activity of purified human and sponge proteins was analyzed with GTPase-GloTM Assay kit. The cell model consisted of human breast cancer cell lines MCF-7 and MDA-MB-231 transiently transfected with EsuRRAS2-like or HsaRRAS2. Biological characterization of R-RAS2 proteins was performed by Western blot on whole cell lysates or cell adhesion protein isolates, immunofluorescence and confocal microscopy, MTT test, colony formation assay, wound healing and Boyden chamber migration assays. RESULTS: We found that the single sponge R-RAS2-like gene/protein probably reflects the properties of the ancestral R-RAS protein that existed prior to duplications during the transition to Bilateria, and to Vertebrata. Biochemical characterization of sponge and human R-RAS2 showed that they have the same intrinsic GTPase activity and RNA binding properties. By testing cell proliferation, migration and colony forming efficiency in MDA-MB-231 human breast cancer cells, we showed that the ancestral type of the R-RAS protein, sponge R-RAS2-like, enhances their oncogenic potential, similar to human R-RAS2. In addition, sponge and human R-RAS2 were not found in focal adhesions, but both homologs play a role in their regulation by increasing talin1 and vinculin. CONCLUSIONS: This study suggests that the ancestor of all animals possessed an R-RAS2-like protein with oncogenic properties similar to evolutionarily more recent versions of the protein, even before the appearance of true tissue and the origin of tumors. Therefore, we have unraveled the evolutionary history of R-RAS2 in metazoans and improved our knowledge of R-RAS2 properties, including its structure, regulation and function.

Irreducible Complexity of Hox Gene: Path to the Canonical Function of the Hox Cluster.

The evolution of major taxa is often associated with the emergence of new gene families. In all multicellular animals except sponges and comb jellies, the genomes contain Hox genes, which are crucial regulators of development. The canonical function of Hox genes involves colinear patterning of body parts in bilateral animals. This general function is implemented through complex, precisely coordinated mechanisms, not all of which are evolutionarily conserved and fully understood. We suggest that the emergence of this regulatory complexity was preceded by a stage of cooperation between more ancient morphogenetic programs or their individual elements. Footprints of these programs may be present in modern animals to execute non-canonical Hox functions. Non-canonical functions of Hox genes are involved in maintaining terminal nerve cell specificity, autophagy, oogenesis, pre-gastrulation embryogenesis, vertical signaling, and a number of general biological processes. These functions are realized by the basic properties of homeodomain protein and could have triggered the evolution of ParaHoxozoa and Nephrozoa subsequently. Some of these non-canonical Hox functions are discussed in our review.

Metazoan endoparasites of snakes from Argentina: Review and checklist with distributional notes and remarks.

This article presents a checklist of metazoan parasites of snakes from Argentina, along with a comprehensive review of the relevant literature published between 1922 and June 2023, covering various aspects of interest. We compiled 34 species of metazoan endoparasites from 28 studies. The subclass Digenea showed the highest number of species (n = 22 species), followed by the phylum Nematoda (n = 8 species), and the subclass Pentastomida (n = 3 species and 1 taxa inquirenda). Dipsadidae was the family of snakes with the most species examined for metazoan endoparasites (n = 20 species). In contrast, Viperidae had the largest number of specimens surveyed (n = 343). Of 23 provinces, 15 (65.2%) presented at least one report of metazoan endoparasites in snakes. The northeastern provinces showed the highest richness of metazoan endoparasites and host diversity. Many articles focused on taxonomy, but studies on parasite ecology were not found. Although taxonomic accuracy was high in most reports, some records were correctly deposited in zoological collections or geo-referenced. This is the first attempt to include all groups of metazoan endoparasites of snakes from Argentina in a single checklist in the last century.

On the Unknown Proteins of Eukaryotic Proteomes.

To study unknown proteins on a large scale, a reference system has been set up for the three better studied eukaryotic kingdoms, built with 36 proteomes as taxonomically diverse as possible. Proteins from 362 other eukaryotic proteomes with no known homologue in this set were then analyzed, focusing noteworthy on singletons, that is, on such proteins with no known homologue in their own proteome. Consistently, for a given species, no more than 12% of the singletons thus found are known at the protein level, according to Uniprot. In addition, since they rely on the information found in the alignment of homologous sequences, predictions of AlphaFold2 for their tridimensional structure are poor. In the case of metazoan species, the number of singletons rarely exceeds 1000 for the species the closest to the reference system (divergence times below 75 Myr). Interestingly, in the cases of viridiplantae and fungi, larger amounts of singletons are found for such species, as if the timescale on which singletons are added to proteomes were different in metazoa and in other eukaryotic kingdoms. In order to confirm this phenomenon, further studies of proteomes closer to those of the reference system are, however, needed.

Evolutionary analyses of genes in Echinodermata offer insights towards the origin of metazoan phyla.

Despite recent studies discussing the evolutionary impacts of gene duplications and losses among metazoans, the genomic basis for the evolution of phyla remains enigmatic. Here, we employ phylogenomic approaches to search for orthologous genes without known functions among echinoderms, and subsequently use them to guide the identification of their homologs across other metazoans. Our final set of 14 genes was obtained via a suite of homology prediction tools, gene expression data, gene ontology, and generating the Strongylocentrotus purpuratus phylome. The gene set was subjected to selection pressure analyses, which indicated that they are highly conserved and under negative selection. Their presence across broad taxonomic depths suggests that genes required to form a phylum are ancestral to that phylum. Therefore, rather than de novo gene genesis, we posit that evolutionary forces such as selection on existing genomic elements over large timescales may drive divergence and contribute to the emergence of phyla.

Molecular complexity and gene expression controlling cell turnover during a digestive cycle of carnivorous sponge Lycopodina hypogea.

Lycopodina hypogea is a carnivorous sponge that tolerates laboratory husbandry very well. During a digestion cycle, performed without any digestive cavity, this species undergoes spectacular morphological changes leading to a total regression of long filaments that ensure the capture of prey and their reformation at the end of the cycle. This phenomenon is a unique opportunity to analyze the molecular and cellular determinants that ensure digestion in the sister group of all other metazoans. Using differential transcriptomic analysis coupled with cell biology studies of proliferation, differentiation, and programmed cell deaths (i.e., autophagy and the destructive/constructive function of apoptosis), we demonstrate that the molecular and cellular actors that ensure digestive homeostasis in a sister group of all remaining animals are similar in variety and complexity to those controlling tissue homeostasis in higher vertebrates. During a digestion cycle, most of these actors are finely tuned in a coordinated manner. Our data benefits from complementary approaches coupling in silico and cell biology studies and demonstrate that the nutritive function is provided by the coordination of molecular network that impacts the cells turnover in the entire organism.

A glimpse on metazoan ZNFX1 helicases, ancient players of antiviral innate immunity.

The human zinc finger NFX1-type containing 1 (ZNFX1) is an interferon-stimulated protein associated to the outer mitochondrial membrane, able to bind dsRNAs and interact with MAVS proteins, promoting type I IFN response in the early stage of viral infection. An N-terminal Armadillo (ARM)-type fold and a large helicase core (P-loop) and zinc fingers confer RNA-binding and ATPase activities to ZNFX1. We studied the phylogenetic distribution of metazoan ZNFX1s, ZNFX1 gene expression trends and genomic and protein signatures during viral infection of invertebrates. Based on 221 ZNFX1 sequences, we obtained a polyphyletic tree with a taxonomy-consistent branching at the phylum-level only. In metazoan genomes, ZNFX1 genes were found either in single copy, with up to some tens of exons in vertebrates, or in multiple copies, with one or a few exons and one of them sometimes encompassing most of the coding sequence, in invertebrates like sponges, sea urchins and mollusks. Structural analyses of selected ZNFX1 proteins showed high conservation of the helicase region (P-loop), an overall conserved region and domain architecture, an ARM-fold mostly traceable, and the presence of intrinsically disordered regions of varying length and position. The remarkable over-expression of ZNFX1 in bivalve and gastropod mollusks infected with dsDNA viruses underscores the antiviral role of ZNFX1, whereas nothing similar was found in virus-infected nematodes and corals. Whether the functional diversification reported in the C. elegans ZNFX1 occurs in other metazoan proteins remains to be established.

Parasite communities and their ecological implications: comparative approach on three sympatric clupeiform fish populations (Actinopterygii: Clupeiformes), off Rio de Janeiro, Brazil.

Fish parasite communities can be directly influenced by characteristics of host species. However, little is known about the host-parasite relationships in commercially important fish of the southeastern Atlantic. To address this knowledge gap, a comparative analysis of the parasite communities of three sympatric Clupeiformes was conducted. Cetengraulis edentulus (Engraulidae), Opisthonema oglinum (Clupeidae) and Sardinella brasiliensis (Clupeidae) were collected from an estuarine lagoon near Rio de Janeiro, Brazil. Prevalence, abundance and aggregation were estimated for infrapopulations; richness, diversity, evenness and dominance for infracommunities. The three component communities were compared using both quantitative and qualitative components. Canonical discriminant analysis was used to determine if a host population could be characterised by the component community of its parasites. Multivariate models revealed that host species, a proxy for diet and phylogenetic relationships, was the main factor influencing the composition of parasite infracommunities. Diet was found to be the main factor shaping the communities of endoparasites, in which digeneans were dominant and best indicator of host population. Ectoparasites (copepods, isopods and monogeneans) displayed strong host-specificity with some species restricted to a single host population. The similarity of the component communities of the two clupeid populations demonstrated the influence of host phylogeny. Parasite infracommunities exhibited low diversity and high dominance, with many taxa restricted to a single host species (specialists) and few occurring in more than one (generalists). Host phylogeny and by extension, diet, morphology and coevolution with parasites appear to be important factors in determining the host-parasite relationships of clupeiform fish in the southeastern Atlantic.

Use of 6 Nucleotide Length Words to Study the Complexity of Gene Sequences from Different Organisms.

In this paper, we attempted to find a relation between bacteria living conditions and their genome algorithmic complexity. We developed a probabilistic mathematical method for the evaluation of k-words (6 bases length) occurrence irregularity in bacterial gene coding sequences. For this, the coding sequences from different bacterial genomes were analyzed and as an index of k-words occurrence irregularity, we used W, which has a distribution similar to normal. The research results for bacterial genomes show that they can be divided into two uneven groups. First, the smaller one has W in the interval from 170 to 475, while for the second it is from 475 to 875. Plants, metazoan and virus genomes also have W in the same interval as the first bacterial group. We suggested that second bacterial group coding sequences are much less susceptible to evolutionary changes than the first group ones. It is also discussed to use the W index as a biological stress value.

Adaptation to a Viscous Snowball Earth Ocean as a Path to Complex Multicellularity.

AbstractAnimals, fungi, and algae with complex multicellular bodies all evolved independently from unicellular ancestors. The early history of these major eukaryotic multicellular clades, if not their origins, co-occur with an extreme phase of global glaciations known as the Snowball Earth. Here, I propose that the long-term loss of low-viscosity environments due to several rounds global glaciation drove the multiple origins of complex multicellularity in eukaryotes and the subsequent radiation of complex multicellular groups into previously unoccupied niches. In this scenario, life adapts to Snowball Earth oceans by evolving large size and faster speeds through multicellularity, which acts to compensate for high-viscosity seawater and achieve fluid flow at sufficient levels to satisfy metabolic needs. Warm, low-viscosity seawater returned with the melting of the Snowball glaciers, and with it, by virtue of large and fast multicellular bodies, new ways of life were unveiled.

Molecular form and function of the cytokinetic ring.

Animal cells, amoebas and yeast divide using a force-generating, actin- and myosin-based contractile ring or 'cytokinetic ring' (CR). Despite intensive research, questions remain about the spatial organization of CR components, the mechanism by which the CR generates force, and how other cellular processes are coordinated with the CR for successful membrane ingression and ultimate cell separation. This Review highlights new findings about the spatial relationship of the CR to the plasma membrane and the arrangement of molecules within the CR from studies using advanced microscopy techniques, as well as mechanistic information obtained from in vitro approaches. We also consider advances in understanding coordinated cellular processes that impact the architecture and function of the CR.

Transfection of Capsaspora owczarzaki, a close unicellular relative of animals.

How animals emerged from their unicellular ancestor remains a major evolutionary question. New genome data from the closest unicellular relatives of animals have provided important insights into the evolution of animal multicellularity. We know that the unicellular ancestor of animals had an unexpectedly complex genetic repertoire, including many genes that are key to animal development and multicellularity. Thus, assessing the function of these genes among unicellular relatives of animals is key to understanding how they were co-opted at the onset of the Metazoa. However, such analyses have been hampered by the lack of genetic tools. Progress has been made in choanoflagellates and teretosporeans, two of the three lineages closely related to animals, whereas no tools are yet available for functional analysis in the third lineage: the filastereans. Importantly, filastereans have a striking repertoire of genes involved in transcriptional regulation and other developmental processes. Here, we describe a reliable transfection method for the filasterean Capsaspora owczarzaki We also provide a set of constructs for visualising subcellular structures in live cells. These tools convert Capsaspora into a unique experimentally tractable organism to use to investigate the origin and evolution of animal multicellularity.

Developmental processes in Ediacara macrofossils.

The Ediacara Biota preserves the oldest fossil evidence of abundant, complex metazoans. Despite their significance, assigning individual taxa to specific phylogenetic groups has proved problematic. To better understand these forms, we identify developmentally controlled characters in representative taxa from the Ediacaran White Sea assemblage and compare them with the regulatory tools underlying similar traits in modern organisms. This analysis demonstrates that the genetic pathways for multicellularity, axial polarity, musculature, and a nervous system were likely present in some of these early animals. Equally meaningful is the absence of evidence for major differentiation of macroscopic body units, including distinct organs, localized sensory machinery or appendages. Together these traits help to better constrain the phylogenetic position of several key Ediacara taxa and inform our views of early metazoan evolution. An apparent lack of heads with concentrated sensory machinery or ventral nerve cords in such taxa supports the hypothesis that these evolved independently in disparate bilaterian clades.

Animal chromosome counts reveal a similar range of chromosome numbers but with less polyploidy in animals compared to flowering plants.

Understanding the mechanisms that underlie chromosome evolution could provide insights into the processes underpinning the origin, persistence and evolutionary tempo of lineages. Here, we present the first database of chromosome counts for animals (the Animal Chromosome Count database, ACC) summarizing chromosome numbers for ~15,000 species. We found remarkable a similarity in the distribution of chromosome counts between animals and flowering plants. Nevertheless, the similarity in the distribution of chromosome numbers between animals and plants is likely to be explained by different drivers. For instance, we found that while animals and flowering plants exhibit similar frequencies of speciation-related changes in chromosome number, plant speciation is more often related to changes in ploidy. By leveraging the largest data set of chromosome counts for animals, we describe a previously undocumented pattern across the Tree of Life-animals and flowering plants show remarkably similar distributions of haploid chromosome numbers.

Evolution of metazoan morphological disparity.

The animal kingdom exhibits a great diversity of organismal form (i.e., disparity). Whether the extremes of disparity were achieved early in animal evolutionary history or clades continually explore the limits of possible morphospace is subject to continuing debate. Here we show, through analysis of the disparity of the animal kingdom, that, even though many clades exhibit maximal initial disparity, arthropods, chordates, annelids, echinoderms, and mollusks have continued to explore and expand the limits of morphospace throughout the Phanerozoic, expanding dramatically the envelope of disparity occupied in the Cambrian. The "clumpiness" of morphospace occupation by living clades is a consequence of the extinction of phylogenetic intermediates, indicating that the original distribution of morphologies was more homogeneous. The morphological distances between phyla mirror differences in complexity, body size, and species-level diversity across the animal kingdom. Causal hypotheses of morphologic expansion include time since origination, increases in genome size, protein repertoire, gene family expansion, and gene regulation. We find a strong correlation between increasing morphological disparity, genome size, and microRNA repertoire, but no correlation to protein domain diversity. Our results are compatible with the view that the evolution of gene regulation has been influential in shaping metazoan disparity whereas the invasion of terrestrial ecospace appears to represent an additional gestalt, underpinning the post-Cambrian expansion of metazoan disparity.

Emergence of a Thrombospondin Superfamily at the Origin of Metazoans.

Extracellular matrix (ECM) is considered central to the evolution of metazoan multicellularity; however, the repertoire of ECM proteins in nonbilaterians remains unclear. Thrombospondins (TSPs) are known to be well conserved from cnidarians to vertebrates, yet to date have been considered a unique family, principally studied for matricellular functions in vertebrates. Through searches utilizing the highly conserved C-terminal region of TSPs, we identify undisclosed new families of TSP-related proteins in metazoans, designated mega-TSP, sushi-TSP, and poriferan-TSP, each with a distinctive phylogenetic distribution. These proteins share the TSP C-terminal region domain architecture, as determined by domain composition and analysis of molecular models against known structures. Mega-TSPs, the only form identified in ctenophores, are typically >2,700 aa and are also characterized by N-terminal leucine-rich repeats and central cadherin/immunoglobulin domains. In cnidarians, which have a well-defined ECM, Mega-TSP was expressed throughout embryogenesis in Nematostella vectensis, with dynamic endodermal expression in larvae and primary polyps and widespread ectodermal expression in adult Nematostella vectensis and Hydra magnipapillata polyps. Hydra Mega-TSP was also expressed during regeneration and siRNA-silencing of Mega-TSP in Hydra caused specific blockade of head regeneration. Molecular phylogenetic analyses based on the conserved TSP C-terminal region identified each of the TSP-related groups to form clades distinct from the canonical TSPs. We discuss models for the evolution of the newly defined TSP superfamily by gene duplications, radiation, and gene losses from a debut in the last metazoan common ancestor. Together, the data provide new insight into the evolution of ECM and tissue organization in metazoans.

Sodium action potentials in placozoa: Insights into behavioral integration and evolution of nerveless animals.

Placozoa are small disc-shaped animals, representing the simplest known, possibly ancestral, organization of free-living animals. With only six morphological distinct cell types, without any recognized neurons or muscle, placozoans exhibit fast effector reactions and complex behaviors. However, little is known about electrogenic mechanisms in these animals. Here, we showed the presence of rapid action potentials in four species of placozoans (Trichoplax adhaerens [H1 haplotype], Trichoplax sp.[H2], Hoilungia hongkongensis [H13], and Hoilungia sp. [H4]). These action potentials are sodium-dependent and can be inducible. The molecular analysis suggests the presence of 5-7 different types of voltage-gated sodium channels, which showed substantial evolutionary radiation compared to many other metazoans. Such unexpected diversity of sodium channels in early-branched metazoan lineages reflect both duplication events and parallel evolution of unique behavioral integration in these nerveless animals.

Cell Communications among Microorganisms, Plants, and Animals: Origin, Evolution, and Interplays.

Cellular communications play pivotal roles in multi-cellular species, but they do so also in uni-cellular species. Moreover, cells communicate with each other not only within the same individual, but also with cells in other individuals belonging to the same or other species. These communications occur between two unicellular species, two multicellular species, or between unicellular and multicellular species. The molecular mechanisms involved exhibit diversity and specificity, but they share common basic features, which allow common pathways of communication between different species, often phylogenetically very distant. These interactions are possible by the high degree of conservation of the basic molecular mechanisms of interaction of many ligand-receptor pairs in evolutionary remote species. These inter-species cellular communications played crucial roles during Evolution and must have been positively selected, particularly when collectively beneficial in hostile environments. It is likely that communications between cells did not arise after their emergence, but were part of the very nature of the first cells. Synchronization of populations of non-living protocells through chemical communications may have been a mandatory step towards their emergence as populations of living cells and explain the large commonality of cell communication mechanisms among microorganisms, plants, and animals.