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Cis-regulatory interfaces reveal the molecular mechanisms underlying the notochord gene regulatory network of Ciona
The notochord is an essential hallmark of the chordate phylum. Here, Negrón-Piñeiro et al. study the notochord gene regulatory network in Ciona, and their findings illustrate how notochord transcription factors are coordinated by Brachyury and Foxa2.
- Lenny J. Negrón-Piñeiro
- , Yushi Wu
- & Anna Di Gregorio
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Article
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Extracellular DNA traps in a ctenophore demonstrate immune cell behaviors in a non-bilaterian
Identifying core mechanisms of immune cells is critical for understanding the evolution of animal immune function. Here, Vandepas et al. report that ctenophore immune-like cells release extracellular DNA traps when exposed to microbes.
- Lauren E. Vandepas
- , Caroline Stefani
- & Adam Lacy-Hulbert
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Single cell atlas of Xenoturbella bocki highlights limited cell-type complexity
Recent phylogenetic analyses have identified orphan clades, including Xenacoelomorphs, that can offer insights into bilaterian evolution. Here they generate a cell type atlas of Xenoturbella bockithat highlights cellular diversity in the nervous system and other tissues, reinforcing the idea of parallel evolution of cell types across animals.
- Helen E. Robertson
- , Arnau Sebé-Pedrós
- & Heather Marlow
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Evolutionary origin of Hoxc13-dependent skin appendages in amphibians
Hair is the main skin appendage of mammals. Here, the authors show that claws of clawed frogs and hair contain homologous keratins and depend on the same transcription factor, Hoxc13, suggesting a common evolutionary origin of these skin appendages.
- Marjolein Carron
- , Attila Placido Sachslehner
- & Leopold Eckhart
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Temporospatial hierarchy and allele-specific expression of zygotic genome activation revealed by distant interspecific urochordate hybrids
Wei et al. report a unique interspecific ascidian hybrid system and single-cell RNA sequencing to reveal the temporal hierarchy, spatial heterogeneity, and allele-specific expression of zygotic genome activation in urochordates.
- Jiankai Wei
- , Wei Zhang
- & Bo Dong
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Key homeobox transcription factors regulate the development of the firefly’s adult light organ and bioluminescence
Adult firefly light organs exhibit flashing signals important for courtship, though how these organs form during development is largely unknown. Here the authors demonstrate that homeobox transcription factors play a patterning role in the development of the adult light organs.
- Xinhua Fu
- & Xinlei Zhu
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Extensive DNA methylome rearrangement during early lamprey embryogenesis
DNA methylation plays a major role in establishing cell identity, but the dynamics of DNA methylation patterns are highly variable across species. Here, the authors discover extensive DNA methylation reprogramming during embryonic development of the sea lamprey, a jawless fish with a distinctive, highly disordered methylome.
- Allegra Angeloni
- , Skye Fissette
- & Ozren Bogdanovic
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Sea lamprey enlightens the origin of the coupling of retinoic acid signaling to vertebrate hindbrain segmentation
Retinoic acid signaling is involved in patterning the embryonic antero-posterior axis, and also regulates hindbrain segmentation in jawed vertebrates. Here they show that retinoic acid signaling plays important roles in hindbrain segmentation in a jawless vertebrate, the lamprey, thus indicating this feature of hindbrain development is conserved in all vertebrates.
- Alice M. H. Bedois
- , Hugo J. Parker
- & Robb Krumlauf
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A histone demethylase links the loss of plasticity to nongenetic inheritance and morphological change
A challenge for understanding plasticity is connecting macroevolutionary patterns to molecular mechanisms. Using a nematode model, this study identifies a mediator of nongenetic inheritance which is linked to multigenerational shifts in plasticity and morphology.
- Nicholas A. Levis
- & Erik J. Ragsdale
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A micro RNA mediates shoot control of root branching
Plant shoots and roots act in concert to ensure access to soil nutrients by adapting root growth. The manuscript identifies a key shoot signal, a mobile micro RNA, that systemically controls lateral root initiation to optimize nitrate supply.
- Moritz Sexauer
- , Hemal Bhasin
- & Katharina Markmann
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Reproductive individuality of clonal fish raised in near-identical environments and its link to early-life behavioral individuality
Even in the absence of apparent genetic and environmental differences, substantial behavioral individuality emerges. This study demonstrates that such seemingly stochastic variation in a clonal fish species translates into predictable differences in life-history measures and ultimately fitness.
- Ulrike Scherer
- , Sean M. Ehlman
- & Max Wolf
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Determining zebrafish dorsal organizer size by a negative feedback loop between canonical/non-canonical Wnts and Tlr4/NFκB
Dorsal organizer initiates the dorsal-ventral axis formation in vertebrates. Here, the authors demonstrate that Tlr4/NFκB-mediated negative feedback regulation of Wnt/β-catenin signaling determines the precise size of the zebrafish dorsal organizer.
- Juqi Zou
- , Satoshi Anai
- & Tohru Ishitani
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Middle ear innovation in Early Cretaceous eutherian mammals
The evolution of the middle ear in early therians is unclear. Here, the authors report a reconstructed, detached middle ear in a eutherian mammal from the Early Cretaceous Jehol Biota, suggesting independent decoupling of hearing and chewing apparatuses.
- Haibing Wang
- & Yuanqing Wang
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Non-uniform temporal scaling of developmental processes in the mammalian cortex
Marsupial mammals take much longer to develop than similarly sized placental mammals, though how brain development occurs across these different periods is unclear. Here they show that the neurodevelopmental events of cortical neurogenesis, cell migration and axon extension do not all temporally scale to the same extent.
- Annalisa Paolino
- , Elizabeth H. Haines
- & Laura R. Fenlon
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Interlocking of co-opted developmental gene networks in Drosophila and the evolution of pre-adaptive novelty
During evolution, genes can be recruited to new positions to perform novel functions. This study shows one such co-option event, where the reused gene networks are initially interlocked, so that any changes because of their function in one organ are mirrored in the other organs even if they provide no selective advantage, opening the potential for acquiring a novel function.
- Sara Molina-Gil
- , Sol Sotillos
- & James C.-G. Hombría
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A single-cell atlas of West African lungfish respiratory system reveals evolutionary adaptations to terrestrialization
The water-to-land transition of vertebrates is a landmark event in evolutionary history. This work utilizes single-cell RNA sequencing to explore the adaptations in African lungfish lungs and gills to terrestrialization.
- Ruihua Zhang
- , Qun Liu
- & Guangyi Fan
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Serotonin signaling regulates actomyosin contractility during morphogenesis in evolutionarily divergent lineages
Serotonin signaling is well known for modulating animal behavior. Here the authors discovered it plays a developmental role in regulating actomyosin contractility driven cellular mechanics and tissue flows during gastrulation of insect and bird.
- Sanjay Karki
- , Mehdi Saadaoui
- & Thomas Lecuit
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Sinus venosus adaptation models prolonged cardiovascular disease and reveals insights into evolutionary transitions of the vertebrate heart
Nr2fs are conserved transcription factors that regulate atrial chamber and venous development. Here, the authors use adult zebrafish nr2f1a mutants to investigate compensatory remodeling of the inflow tract and hypotheses of cardiac evolution.
- Jacob T. Gafranek
- , Enrico D’Aniello
- & Joshua S. Waxman
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Bat teeth illuminate the diversification of mammalian tooth classes
Despite their key role in the evolution of mammals, the origin and diversification of tooth classes (incisors, canines, premolars and molars) remain relatively obscure. Here the authors use integrative approaches to explain the independent evolution and rapid diversification of two tooth classes, premolar and molars, in noctilionoid bats.
- Alexa Sadier
- , Neal Anthwal
- & Karen E. Sears
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NvPrdm14d-expressing neural progenitor cells contribute to non-ectodermal neurogenesis in Nematostella vectensis
Endodermal neurogenesis is an uncommon trait among animals. Here they identify a population of endoderm-specific neural progenitor cells in the cnidarian Nematostella vectensis that is characterized by the expression of the transcription factor prdm14d.
- Quentin I. B. Lemaître
- , Natascha Bartsch
- & Fabian Rentzsch
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C. elegans ageing is accelerated by a self-destructive reproductive programme
Caenorhabditis elegans is used as a model species to investigate ageing, yet has a very high degree of plasticity in lifespan. This study argues that ageing in C. elegans is driven by suicidal reproductive effort, unlike many other organisms.
- Carina C. Kern
- , Shivangi Srivastava
- & David Gems
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RAS-independent ERK activation by constitutively active KSR3 in non-chordate metazoa
ERK signalling is a core developmental pathway that is canonically activated by RTKs through activated RAS. Here they show that the process of ERK activation in skeletogenic precursors of the sea urchin embryo is growth factor and RAS-independent, uncovering a new mode of ERK signalling in non-chordate metazoa.
- Aline Chessel
- , Noémie De Crozé
- & Thierry Lepage
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Divergent molecular signatures in fish Bouncer proteins define cross-fertilization boundaries
The egg membrane protein Bouncer is an important mediator of gamete interaction and prevents cross-fertilisation between medaka and zebrafish. This study demonstrates unique functional and structural differences in Bouncer proteins of these and other distantly related fish species which may determine which species can hybridize.
- Krista R. B. Gert
- , Karin Panser
- & Andrea Pauli
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Coordinated adaptations define the ontogenetic shift from worm- to fish-hunting in a venomous cone snail
Challenges rearing juvenile cone snails have limited our understanding of their developmental biology. This study cultured Conus magus cone snails and revealed how complex morphological, behavioural and molecular changes facilitate the ontogenetic shift from juvenile worm-hunters to fish-hunting adults.
- Aymeric Rogalski
- , S. W. A. Himaya
- & Richard J. Lewis
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Serine ADP-ribosylation in Drosophila provides insights into the evolution of reversible ADP-ribosylation signalling
In the DNA damage response, ADP-ribosylation is an essential signaling pathway. Here the authors utilize a multidisciplinary approach to establish its molecular basis in fruit flies and provide evidence for Drosophila’s suitability as model organism.
- Pietro Fontana
- , Sara C. Buch-Larsen
- & Ivan Ahel
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Higher-order epistasis shapes natural variation in germ stem cell niche activity
Stem cell niches regulate proliferation of stem cells, but variation in this control across natural populations has not been explored. Here they combine quantitative genetics and gene editing to show that natural variation in C. elegans germ stem cell niche activity is shaped by complex gene-gene interactions.
- Sarah R. Fausett
- , Asma Sandjak
- & Christian Braendle
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Patterns of ontogenetic evolution across extant marsupials reflect different allometric pathways to ecomorphological diversity
The high level of morphological diversity in Australasian marsupials compared to those from the Americas remains poorly understood. This study shows that variation in ontogenetic allometry among Australasian and American marsupials is similar, despite this great difference in ecomorphological diversity.
- Laura A. B. Wilson
- , Camilo López-Aguirre
- & Norberto P. Giannini
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Molecular mechanisms of tubulogenesis revealed in the sea star hydro-vascular organ
Understanding how cells organize into organs is a key effort in developmental biology. Here the authors introduce the sea star hydrovascular organ as a genetically tractable system to understand the contribution of cell migration and signaling pathways in tubulogenesis.
- Margherita Perillo
- , S. Zachary Swartz
- & Gary M. Wessel
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Acoel single-cell atlas reveals expression dynamics and heterogeneity of adult pluripotent stem cells
Multiple species can achieve whole-body regeneration through the action of adult stem cells, though little is known about how these cells compare across species. Here they investigated the stem cells of a marine worm, the acoel Hofstenia miamia, and identified heterogeneity of these cells during development and regeneration.
- Ryan E. Hulett
- , Julian O. Kimura
- & Mansi Srivastava
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A DBHS family member regulates male determination in the filariasis vector Armigeres subalbatus
The Armigeres subalbatus sex-determining locus, M, maps to the 3rd chromosome, but its identity was unknown. Here they identify a sex-specific gene, AsuMf, that is essential for male development and show that it is a novel male-determining factor derived from duplication and neofunctionalization of a conserved DBHS family member.
- Peiwen Liu
- , Wenqiang Yang
- & Xiao-Guang Chen
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DNMT1 mutant ants develop normally but have disrupted oogenesis
The role of DNA methylation in insects is poorly understood. Here, the authors knock out the DNA methyltransferase DNMT1 in an ant and find no obvious effects on development, rather showing that this enzyme seems to play a crucial role during early oogenesis.
- Iryna Ivasyk
- , Leonora Olivos-Cisneros
- & Daniel J. C. Kronauer
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Histone 4 lysine 5/12 acetylation enables developmental plasticity of Pristionchus mouth form
Developmental plasticity allows organisms to match traits to their environment, however, there are few known molecular mechanisms underlying such plasticity. Here, the authors show that feeding morphs in adult Pristionchus nematodes are set during a critical window in juveniles and identify H4K5/12ac as the environmental information carrier.
- Michael S. Werner
- , Tobias Loschko
- & Ralf J. Sommer
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Muscle cell-type diversification is driven by bHLH transcription factor expansion and extensive effector gene duplications
Different muscle cell types account for specific abilities in animals, yet how their diversification arose remains unclear. Here, the authors show that gene duplications of bHLH transcription factors and effector genes contributed to the diversification of muscle cell types in the sea anemone Nematostella.
- Alison G. Cole
- , Stefan M. Jahnel
- & Ulrich Technau
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A male-killing gene encoded by a symbiotic virus of Drosophila
Maternally inherited symbionts that kill male insect hosts are well known in bacteria, but are also beginning to be recognised in viruses. In this study, the authors identify a gene from a symbiotic virus genome that is responsible for the male-killing phenotype of this virus in the fly Drosophila biauraria.
- Daisuke Kageyama
- , Toshiyuki Harumoto
- & Masayoshi Watada
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Single-cell atavism reveals an ancient mechanism of cell type diversification in a sea anemone
Understanding how new cell types arise is essential for understanding the evolution of animal diversity. This study shows that a single gene, NvSox2, acts as a simple switch controlling the development of two alternative types of stinging cells in the sea anemone Nematostella vectensis.
- Leslie S. Babonis
- , Camille Enjolras
- & Mark Q. Martindale
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The function and evolution of a genetic switch controlling sexually dimorphic eye differentiation in honeybees
Sexual dimorphism results in widely diverse animal forms, but sexual determination is generally attributed to a single gene in animal models. Here they find that the glu gene regulates sexual dimorphism of honeybee eyes, demonstrating diversification of genetic programs for dimorphism.
- Oksana Netschitailo
- , Yidong Wang
- & Martin Beye
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N6-methyladenosine modification governs liver glycogenesis by stabilizing the glycogen synthase 2 mRNA
Here the authors find that the mRNA of GYS2, the liver-specific glycogen synthase, is a substrate of METTL3 and IGF2BP2 and that m6A-mediated regulation of Gys2 mRNA is critical for the maintenance of liver glycogenesis in mammals during growth, such as mice and rats.
- Xiang Zhang
- , Huilong Yin
- & Rui Zhang
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The transcription factor Zfh1 acts as a wing-morph switch in planthoppers
The molecular mechanisms underlying wing polyphenism remain poorly understood. Here the authors use plant hoppers to show that the development of long and short wing morphs is balanced by the relative activities of the Zfh1-FoxO and insulin signaling cascades.
- Jin-Li Zhang
- , Sun-Jie Chen
- & Hai-Jun Xu
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Evolutionary origin of vertebrate OCT4/POU5 functions in supporting pluripotency
By constructing an evolutionary trajectory of the cyclostome-gnathostome Pou5 gene family and comparing the structural and phenotypic protein variations, the authors uncover the origin of functional characteristics for the pluripotency factor Oct4.
- Woranop Sukparangsi
- , Elena Morganti
- & Joshua M. Brickman
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Construction of the axolotl cell landscape using combinatorial hybridization sequencing at single-cell resolution
The Mexican axolotl is a well-established tetrapod model for regeneration and development. Here the authors report a scRNA-seq method to profile neotenic, metamorphic and limb development stages, highlighting unique perturbation patterns of cell type-related gene expression throughout metamorphosis.
- Fang Ye
- , Guodong Zhang
- & Guoji Guo
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Article
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MRTF specifies a muscle-like contractile module in Porifera
Myocytes are a key cell type that enable animal movement, but their evolutionary origins remain unclear. Colgren and Nichols describe molecular and functional similarities between a contractile module in tissues of a sponge and muscle tissues in other animals, indicating a common evolutionary origin.
- J. Colgren
- & S. A. Nichols
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Matters Arising
| Open Access
Complexity of biological scaling suggests an absence of systematic trade-offs between sensory modalities in Drosophila
- Max S. Farnworth
- & Stephen H. Montgomery
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Article
| Open Access
Regulation of the evolutionarily conserved muscle myofibrillar matrix by cell type dependent and independent mechanisms
Recent work has shown that mammalian muscle cells are comprised of multiple branching sarcomeres, though how this connectivity is regulated has remained unknown. Here the authors show three different mechanisms which regulate connectivity of the muscle contractile apparatus.
- Peter T. Ajayi
- , Prasanna Katti
- & Brian Glancy
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ERK1/2 is an ancestral organising signal in spiral cleavage
How invertebrates with spiral cleavage establish their body plans is unclear. Here the authors show that, like molluscs, a basal annelid uses ERK1/2 to instruct body patterning, suggesting that this is a deep ancestral trait in animal embryogenesis.
- Océane Seudre
- , Allan M. Carrillo-Baltodano
- & José M. Martín-Durán
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Emergence of novel cephalopod gene regulation and expression through large-scale genome reorganization
Cephalopods are an enigmatic animal group with complex and adaptive behaviors such as camouflage; however the genetic basis for these traits is not well understood. Here the authors reveal a set of cephalopod-restricted rearranged genomic loci, involving known neuronal regulators but also unexpected gene families, that confer topological organization and gene regulation.
- Hannah Schmidbaur
- , Akane Kawaguchi
- & Oleg Simakov
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Trade-off between reducing mutational accumulation and increasing commitment to differentiation determines tissue organization
The observation that tissues that undergo more stem cell divisions are less prone to develop cancer presents a paradox as these tissues should have more opportunity to accumulate cancer-causing mutations. Here, the authors present a solution to the paradox by showing how hierarchical tissues can maintain low cancer incidence by balancing mutation accumulation and the cells’ commitment to differentiation.
- Márton Demeter
- , Imre Derényi
- & Gergely J. Szöllősi
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A hemimetabolous wing development suggests the wing origin from lateral tergum of a wingless ancestor
Here, the authors investigate wing development in cricket and find support for evolution of the novel insect wing from the pre-existing dorsal body wall of a wingless ancestor by activation of an evolutionarily conserved growth mechanism.
- Takahiro Ohde
- , Taro Mito
- & Teruyuki Niimi
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Histone demethylase Lsd1 is required for the differentiation of neural cells in Nematostella vectensis
The evolutionary point where chromatin modifier function integrated into regulation of specific cell types is unclear. In the cnidarian Nematostella vectensis, the authors here show that lysine specific demethylase Lsd1 is developmentally regulated and required for normal development including cnidocyte differentiation.
- James M. Gahan
- , Ian U. Kouzel
- & Fabian Rentzsch
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Temperature sensitivity of Notch signaling underlies species-specific developmental plasticity and robustness in amniote brains
Ambient temperature significantly affects embryogenesis, but adaptive molecular mechanisms that respond to temperature remain unclear. Here, the authors identified species-specific thermal sensitivity of Notch signaling in developing amniote brains.
- Tadashi Nomura
- , Kohjiro Nagao
- & Katsuhiko Ono
Annelid adult cell type diversity and their pluripotent cellular origins