Form, Function, Agency: Sources of Natural Purpose in Animal Evolution

The origination and evolution of multicellular form and function is generally thought to be based on gene-based variation, with natural selection changing the populational composition in the respective variants over time. The criterion for evolutionary success is differential fitness, the relative capacity to leave progeny in the next generation. Theoretical considerations show that this model implies that phenotypic evolution will generally be gradual, based on variations of small effect. But the fossil record of early phylogenesis, notably for the metazoans, or animals, does not support the gradualist scenario. Moreover, discordances of phenotype and genotype in extant species, along with the existence of a pan-metazoan developmental genetic toolkit, does not support the gene-variation-based evolutionary mechanism, at least at the level of phyla. Most importantly, all life-forms, including the cells that constitute animal embryos, exhibit agency, and associations of cells (even constructed ones with no history of natural selection) exhibit novel kinds of agency. This strongly suggests that new multicellular forms can invent new ways of life (e.g., ecological niches) and can persist without supplanting their populational cohorts. This chapter describes how anatomical (e.g., segments, appendages) and functional (e.g., muscle, nerve) phenotypes can emerge without cycles of gradual selection from inherent properties of metazoan cells and their aggregates. While such phenotypic “add-ons” could provide enablements for exploration of new niches, it is implausible that they arose as adaptations to external challenges. Reproductive fitness, which is essential for understanding biogeography and ecology, is unlikely to have played a role in phylum-level evolution.

Ankfn1-mutant vestibular defects require loss of both ancestral and derived paralogs for penetrance in zebrafish

How and to what degree gene duplication events create regulatory innovation, redundancy, or neofunctionalization remain important questions in animal evolution and comparative genetics. Ankfn1 genes are single copy in most invertebrates, partially duplicated in jawed vertebrates, and only the derived copy retained in most mammals. Null mutations in the single mouse homolog have vestibular and neurological abnormalities. Null mutation of the single Drosophila homolog is typically lethal with severe sensorimotor deficits in rare survivors. The functions and potential redundancy of paralogs in species with two copies is not known. Here we define a vestibular role for Ankfn1 homologs in zebrafish based on simultaneous disruption of each locus. Zebrafish with both paralogs disrupted showed vestibular defects and early lethality from swim bladder inflation failure. One intact copy at either locus was sufficient to prevent major phenotypes. Our results show that vertebrate Ankfn1 genes are required for vestibular-related functions, with at least partial redundancy between ancestral and derived paralogs.

An early Cambrian polyp reveals an anemone-like ancestor for medusozoan cnidarians

Extant cnidarians are a disparate phylum of non-bilaterians and their diploblastic body plan represents a key step in animal evolution. Anthozoans (anemones, corals) are benthic polyps, while adult medusozoans (jellyfishes) are dominantly pelagic medusae. A sessile polyp is present in both groups and is widely conceived as the ancestral form of their last common ancestor. However, the nature and anatomy of this ancestral polyp, particularly of medusozoans, are controversial, owing to the divergent body plans of both groups in the extant lineages and the rarity of medusozoan soft tissues in the fossil record. Here we redescribe the enigmatic Conicula striata Luo et Hu from the early Cambrian Chengjiang biota, south China, which has previously been interpreted as a polyp, lophophorate or deuterostome. We show that C. striata possessed features of both anthozoans and medusozoans. Its stalked polyp and fully encasing conical, annulated organic skeleton (periderm) are features of medusozoans. However, the gut is partitioned by ~28 mesenteries, and has a tubular pharynx, resembling anthozoans. Our phylogenetic analysis recovers C. striata as a stem medusozoan, indicating that the enormously diverse medusozoans were derived from an anemone-like ancestor, with the pharynx lost and number of mesenteries reduced prior to the origin of crown group Medusozoa.

SIVgsn-99CM71 Vpu employs different amino acids to antagonize human and greater spot-nosed monkey BST-2

Viral protein U (Vpu) is an accessory protein encoded by human immunodeficiency virus type 1 (HIV-1) and certain simian immunodeficiency virus (SIV) strains. Some of these viruses were reported to use Vpu to overcome restriction by BST-2 of their natural hosts. Our own recent report revealed that Vpu of SIVgsn-99CM71 (SIVgsn71) antagonizes human BST-2 through two AxxxxxxxW motifs (A 22 W 30 and A 25 W 33 ) whereas antagonizing BST-2 of its natural host, greater spot-nosed monkey (GSN), involved only A 22 W 30 motif. Here we show that residues A 22 , A 25 , W 30 , and W 33 of SIVgsn71 Vpu are all essential to antagonize human BST-2, while, neither single mutation of A 22 nor W 30 affected the ability to antagonize GSN BST-2. Similar to A 18 , which is located in the middle of the A 14 xxxxxxxW 22 motif in HIV-1 NL4-3 Vpu and is essential to antagonize human BST-2, A 29 , located in the middle of the A 25 W 33 motif of SIVgsn71 Vpu was found to be necessary for antagonizing human but not GSN BST-2. Further mutational analyses revealed that residues L 21 and K 32 of SIVgsn71 Vpu were also essential for antagonizing human BST-2. On the other hand, the ability of SIVgsn71 Vpu to target GSN BST-2 was unaffected by single amino acid substitutions but required multiple mutations to render SIVgsn71 Vpu inactive against GSN BST-2. These results suggest additional requirements for SIVgsn71 Vpu antagonizing human BST-2, implying evolution of the bst-2 gene under strong selective pressure. Importance Genes related to survival against life-threating pathogens are important determinants of natural selection in animal evolution. For instance, BST-2, a protein showing broad-spectrum antiviral activity, shows polymorphisms entailing different phenotypes even among primate species, suggesting that the bst-2 gene of primates has been subject to strong selective pressure during evolution. At the same time, viruses readily adapt to these evolutionary changes. Thus, we found that Vpu of an SIVgsn isolate (SIVgsn-99CM71) can target BST-2 from humans as well as from its natural host thus potentially facilitating zoonosis. Here we mapped residues in SIVgsn71 Vpu potentially contributing to cross-species transmission. We found that the requirements for targeting human BST-2 are distinct from and more complex than those for targeting GSN BST-2. Our results suggest that the human bst-2 gene might have evolved to acquire more restrictive phenotype than GSN bst-2 against viral proteins after being derived from their common ancestor.

A chelicerate Wnt gene expression atlas: novel insights into the complexity of arthropod Wnt-patterning

The Wnt genes represent a large family of secreted glycoprotein ligands that date back to early animal evolution. Multiple duplication events generated a set of 13 Wnt families of which 12 are preserved in protostomes. Embryonic Wnt expression patterns (Wnt-patterning) are complex, representing the plentitude of functions these genes play during development. Here, we comprehensively investigated the embryonic expression patterns of Wnt genes from three species of spiders covering both main groups of true spiders, Haplogynae and Entelegynae, a mygalomorph species (tarantula), as well as a distantly related chelicerate outgroup species, the harvestman Phalangium opilio. All spiders possess the same ten classes of Wnt genes, but retained partially different sets of duplicated Wnt genes after whole genome duplication, some of which representing impressive examples of sub- and neo-functionalization. The harvestman, however, possesses a more complete set of 11 Wnt genes but with no duplicates. Our comprehensive data-analysis suggests a high degree of complexity and evolutionary flexibility of Wnt-patterning likely providing a firm network of mutational protection. We discuss the new data on Wnt gene expression in terms of their potential function in segmentation, posterior elongation, and appendage development and critically review previous research on these topics. We conclude that earlier research may have suffered from the absence of comprehensive gene expression data leading to partial misconceptions about the roles of Wnt genes in development and evolution.

The birth of piRNAs: how mammalian piRNAs are produced, originated, and evolved

PIWI-interacting RNAs (piRNAs), small noncoding RNAs 24–35 nucleotides long, are essential for animal fertility. They play critical roles in a range of functions, including transposable element suppression, gene expression regulation, imprinting, and viral defense. In mammals, piRNAs are the most abundant small RNAs in adult testes and the only small RNAs that direct epigenetic modification of chromatin in the nucleus. The production of piRNAs is a complex process from transcription to post-transcription, requiring unique machinery often distinct from the biogenesis of other RNAs. In mice, piRNA biogenesis occurs in specialized subcellular locations, involves dynamic developmental regulation, and displays sexual dimorphism. Furthermore, the genomic loci and sequences of piRNAs evolve much more rapidly than most of the genomic regions. Understanding piRNA biogenesis should reveal novel RNA regulations recognizing and processing piRNA precursors and the forces driving the gain and loss of piRNAs during animal evolution. Such findings may provide the basis for the development of engineered piRNAs capable of modulating epigenetic regulation, thereby offering possible single-dose RNA therapy without changing the genomic DNA. In this review, we focus on the biogenesis of piRNAs in mammalian adult testes that are derived from long non-coding RNAs. Although piRNA biogenesis is believed to be evolutionarily conserved from fruit flies to humans, recent studies argue for the existence of diverse, mammalian-specific RNA-processing pathways that convert precursor RNAs into piRNAs, perhaps associated with the unique features of mammalian piRNAs or germ cell development. We end with the discussion of major questions in the field, including substrate recognition and the birth of new piRNAs.

De novo birth of functional, human-specific microproteins

We now have a growing understanding that functional short proteins can be translated out of small Open Reading Frames (sORF). Such ″microproteins″ can perform crucial biological tasks and can have considerable phenotypic consequences. However, their size makes them less amenable to genomic analysis, and their evolutionary origins and conservation are poorly understood. Given their short length it is plausible that some of these functional microproteins have recently originated entirely de novo from non-coding sequence. Here we test the possibility that de novo gene birth can produce microproteins that are functional ″out-of-the-box″. We reconstructed the evolutionary origins of human microproteins previously found to have measurable, statistically significant fitness effects. By tracing the appearance of each ORF and its transcriptional activation, we were able to show that, indeed, novel small proteins with significant phenotypic effects have emerged de novo throughout animal evolution, including many after the human-chimpanzee split. We show that traditional methods for assessing the coding potential of such sequences often fall short, due to the high variability present in the alignments and the absence of telltale evolutionary signatures that are not yet measurable. Thus we provide evidence that the functional potential intrinsic to sORFs can be rapidly, and frequently realised through de novo gene birth.

The Evolutionary Relevance of Social Learning and Transmission in Non-Social Arthropods with a Focus on Oviposition-Related Behaviors

Research on social learning has centered around vertebrates, but evidence is accumulating that small-brained, non-social arthropods also learn from others. Social learning can lead to social inheritance when socially acquired behaviors are transmitted to subsequent generations. Using oviposition site selection, a critical behavior for most arthropods, as an example, we first highlight the complementarities between social and classical genetic inheritance. We then discuss the relevance of studying social learning and transmission in non-social arthropods and document known cases in the literature, including examples of social learning from con- and hetero-specifics. We further highlight under which conditions social learning can be adaptive or not. We conclude that non-social arthropods and the study of oviposition behavior offer unparalleled opportunities to unravel the importance of social learning and inheritance for animal evolution.

Comparative analysis of genome-encoded viral sequences reveals the evolutionary history of Flaviviridae.

The flaviviruses (family Flaviviridae) are a group of positive-strand RNA viruses, many of which pose serious risks to human health on a global scale. Here, we calibrate the timeline of flavivirus evolution using flavivirus-derived DNA sequences identified in animal genomes. We demonstrate that the family is at least 100 million years old and show that this timing can be integrated with dates inferred from co-phylogenetic analysis and paleontological records to produce a cohesive overview of flavivirus evolution in which the main subgroups originate early in animal evolution and broadly co-diverge with animal phyla. In addition, we show that the arthropod-borne 'classical' flaviviruses first evolved from tick-specific viruses, and only later adapted to become insect-borne. Our findings demonstrate that the biological properties of flaviviruses have been acquired over many millions of years of evolution, implying that broad-scale comparative analysis can reveal fundamental insights into flavivirus biology. We implement a novel approach to computational genomic studies of viruses that can support these efforts by enabling more efficient utilization of evolution-related domain knowledge in virus research.