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| Open AccessThe ecological origins of snakes as revealed by skull evolution
Three alternatives have been proposed for the ecological state of the ancestral snake: fossorial (burrowing), aquatic, or terrestrial. Here, the authors use an integrative geometric morphometric approach that suggests evolution from terrestrial to fossorial in the most recent common ancestor of extant snakes.
- Filipe O. Da Silva
- , Anne-Claire Fabre
- & Nicolas Di-Poï
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| Open AccessDevelopmental nonlinearity drives phenotypic robustness
Developmental processes often involve nonlinearities, but the consequences for translating genotype to phenotype are not well characterized. Here, Green et al. vary Fgf8 signaling across allelic series of mice and show that phenotypic robustness in craniofacial shape is explained by a nonlinear effect of Fgf8 expression.
- Rebecca M. Green
- , Jennifer L. Fish
- & Benedikt Hallgrímsson
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| Open AccessEvolutionary recruitment of flexible Esrp-dependent splicing programs into diverse embryonic morphogenetic processes
Epithelial-mesenchymal interplays are essential to many ontogenetic processes in vertebrates. Here Burguera et al. show diverse embryonic morphogenetic processes regulated by Epithelial Splicing Regulatory Protein (Esrp) in different deuterostome species.
- Demian Burguera
- , Yamile Marquez
- & Manuel Irimia
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| Open AccessAcoel regeneration mechanisms indicate an ancient role for muscle in regenerative patterning
Planarian regenerative mechanisms suggest that muscle has an instructive role in patterning. Here, the authors show that muscle is also responsible for regenerative patterning information in an early-branching bilaterian, Hofstenia miamia, dating this back to the dawn of the Bilateria, over 550 million years ago.
- Amelie A. Raz
- , Mansi Srivastava
- & Peter W. Reddien
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| Open AccessGenetic accommodation via modified endocrine signalling explains phenotypic divergence among spadefoot toad species
Genetic accommodation is a potential mechanism for the phenotypic divergence of species. Here, Kulkarni et al. compare endocrine responses of three spadefoot toad species to pond drying and suggest how evolution of mechanisms of developmental plasticity may account for trait variation among species.
- Saurabh S. Kulkarni
- , Robert J. Denver
- & Daniel R. Buchholz
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| Open AccessTopologically associating domains are ancient features that coincide with Metazoan clusters of extreme noncoding conservation
Metazoan genomes contain many clusters of conserved noncoding elements. Here, the authors provide evidence that these clusters coincide with distinct topologically associating domains in humans and Drosophila, revealing a conserved regulatory genomic architecture.
- Nathan Harmston
- , Elizabeth Ing-Simmons
- & Boris Lenhard
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| Open AccessCo-option of the cardiac transcription factor Nkx2.5 during development of the emu wing
The transcription factor Nkx2.5 is essential for heart development. Here, the authors identify a previously unknown expression domain for Nkx2.5 in the emu wing and explore its role in diminished wing bud development in the flightless emu, compared with three other birds that have functional wings.
- Peter G. Farlie
- , Nadia M. Davidson
- & Craig A. Smith
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| Open AccessTranscriptomic and macroevolutionary evidence for phenotypic uncoupling between frog life history phases
In animals with complex life cycles, selection on one life phase may constrain adaptation in another phase. Here the authors find that, during the adaptive radiation of mantellid frogs, the evolution of tadpole and adult morphologies has been uncoupled through phase-specific gene expression.
- Katharina C. Wollenberg Valero
- , Joan Garcia-Porta
- & Miguel Vences
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| Open AccessRotiferan Hox genes give new insights into the evolution of metazoan bodyplans
Rotifers are microscopic animals with an unusual, nonsegmented body plan consisting of a head, trunk and foot. Here, Fröbius and Funch investigate the role of Hox genes—which are widely used in animal body plan patterning—in rotifer embryogenesis and find non-canonical expression in the nervous system.
- Andreas C. Fröbius
- & Peter Funch
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| Open AccessA phenol-enriched cuticle is ancestral to lignin evolution in land plants
The phenolic polymer lignin is thought to have contributed to adaptation of early land plants to terrestrial environments. Here Renaultet al. show that moss, which does not produce lignin, contains an ancestral phenolic metabolism pathway that produces a phenol-enriched cuticle and prevents desiccation.
- Hugues Renault
- , Annette Alber
- & Danièle Werck-Reichhart
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| Open AccessFunctional roles of Aves class-specific cis-regulatory elements on macroevolution of bird-specific features
The transition from non-avian dinosaurs to birds capable of powered flight represents a major evolutionary transition. Here the authors analyse 48 bird genomes and identify avian-specific highly conserved elements with roles in avian limb development.
- Ryohei Seki
- , Cai Li
- & Guojie Zhang
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| Open AccessEvolution of Shh endoderm enhancers during morphological transition from ventral lungs to dorsal gas bladder
Endoderm enhancer MACS1 of Sonic Hedgehog is conserved in animals with lungs. Here, the authors show that mouse without MACS1 has defective laryngeal development, and use phylogenetic analyses to show association of evolutionary lung-gas bladder transition with change of the enhancer.
- Tomoko Sagai
- , Takanori Amano
- & Toshihiko Shiroishi
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| Open AccessDiverse feather shape evolution enabled by coupling anisotropic signalling modules with self-organizing branching programme
Asymmetric feather vane shape was a critical innovation in feather evolution and adaptation for flight. Here, Li and colleagues characterize the multi-module regulatory network that controls feather vane shape and underlies feather diversification.
- Ang Li
- , Seth Figueroa
- & Cheng-Ming Chuong
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| Open AccessLimiting parental feedback disrupts vocal development in marmoset monkeys
The development of mature vocal patterns is shaped by parental influence in many animals. Here, Gultekin and Hage show that parental feedback not only influences vocal development, but is indeed necessary for juvenile marmosets to acquire normal vocal behaviour.
- Yasemin B. Gultekin
- & Steffen R. Hage
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| Open AccessTetrapod limb and sarcopterygian fin regeneration share a core genetic programme
Salamanders are unique among extant tetrapods for their ability to completely regenerate their limbs. Here, Nogueira and colleagues show that lungfishes, the sister clade of tetrapods, regenerate their fins using analogous gene regulatory changes and morphological steps.
- Acacio F. Nogueira
- , Carinne M. Costa
- & Igor Schneider
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| Open AccessRefuting the hypothesis that the acquisition of germ plasm accelerates animal evolution
The evolution of germ cell specification by maternal germ plasm has been proposed to accelerate vertebrate protein evolution by liberating selective constraints. Whittle and Extavour analyse global rates of protein evolution and find no support for this hypothesis in vertebrates or invertebrates.
- Carrie A. Whittle
- & Cassandra G. Extavour
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| Open AccessNotch signalling mediates reproductive constraint in the adult worker honeybee
In honeybees, pheromones produced by the queen inhibit reproduction by workers and enforce a eusocial division of labour. Here, Duncan, Hyink and Dearden show that this inhibition is mediated by the Notch signalling pathway in the workers' ovaries.
- Elizabeth J. Duncan
- , Otto Hyink
- & Peter K. Dearden
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| Open AccessGenome editing in butterflies reveals that spalt promotes and Distal-less represses eyespot colour patterns
Transcription factors Distal-less(Dll) and spalt were co-opted during the evolution of butterfly eyespots. Here, Zhang and Reed use CRISPR/Cas9 genome editing to show that while spalt is a positive regulator of eyespots as predicted, Dll knockouts have positive effects on both eyespot size and number, thus suggesting that Dllis an eyespot repressor, not an activator as previously thought.
- Linlin Zhang
- & Robert D. Reed
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| Open AccessPre-bilaterian origin of the blastoporal axial organizer
In vertebrate embryos, Wnt/β-catenin signaling induces an organizer area guiding the formation of body axes and inducing extra axes upon transplantation. Here, Kraus et al. show that Wnt ligands also induce an organizer in a sea anemone, indicating that the organizer dates back over 600 million years.
- Yulia Kraus
- , Andy Aman
- & Grigory Genikhovich
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| Open AccessA deuterostome origin of the Spemann organiser suggested by Nodal and ADMPs functions in Echinoderms
Establishment of the body plan in chordates is determined by an organizing centre located on the dorsal side of the embryo. Here, the authors show that the ventral ectoderm of the sea urchin embryo is an organizing centre that shares several fundamental properties with the amphibian Spemann organizer.
- François Lapraz
- , Emmanuel Haillot
- & Thierry Lepage
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| Open AccessAllometric growth in the extant coelacanth lung during ontogenetic development
The presence of a pulmonary system in fossil coelacanths has only recently been identified, with little known about homologues in living species. Here, Cupello et al. confirm the presence of a lung in the extant species Latimeria chalumnaeand report its growth during different stages of development.
- Camila Cupello
- , Paulo M. Brito
- & Gaël Clément
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| Open AccessDevelopmental genetic bases behind the independent origin of the tympanic membrane in mammals and diapsids
The evolution of the amniote middle ear remains unclear. Here, the authors show that inactivation of the Edn1-Dlx5/6 cascade during development results in loss of the tympanic membrane in mouse and duplication in chicken, which suggests independent evolution of the tympanic membrane in different amniotes.
- Taro Kitazawa
- , Masaki Takechi
- & Hiroki Kurihara
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| Open AccessMolecular development of chondrichthyan claspers and the evolution of copulatory organs
Claspers are copulatory organs found in male cartilaginous fishes. Here, the authors show that androgen receptor signalling maintains the Shh pathway to promote clasper development in male skates and suggest the importance of hormonal regulation in the evolution of male copulatory organs.
- Katherine L. O’Shaughnessy
- , Randall D. Dahn
- & Martin J. Cohn
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Shared rules of development predict patterns of evolution in vertebrate segmentation
Despite apparent morphological diversity, developmental interactions create predictable patterns of variation. Here the authors show that variation in the proportion of limbs, digits and somites and their response to artificial selection follow a rule that predicts the size of sequentially forming structures.
- Nathan M. Young
- , Benjamin Winslow
- & Kathryn Kavanagh
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| Open AccessEvolutionary innovation and conservation in the embryonic derivation of the vertebrate skull
It is unclear whether the embryonic origin of skull bones is evolutionarily conserved. Here, the authors show that the pattern of cranial development of the Mexican axolotl is similar to that reported for other vertebrates, but the pattern in the African clawed frog, another amphibian, is unique.
- Nadine Piekarski
- , Joshua B. Gross
- & James Hanken
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Pigment cell interactions and differential xanthophore recruitment underlying zebrafish stripe reiteration and Danio pattern evolution
Fishes have diverse colour patterns, yet the mechanisms of pattern diversification are poorly understood. Here, the authors show that the uniform pigment pattern in Danio albolineatus is established by an early differentiation of xanthophores controlled by cis regulatory changes at the csf1alocus.
- Larissa B. Patterson
- , Emily J. Bain
- & David M. Parichy
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Shared developmental programme strongly constrains beak shape diversity in songbirds
The extent and mechanisms by which developmental process may constraint natural variation are poorly understood. Here, Fritz et al. show that beak shape in songbirds is strongly constrained by developmental mechanics shared by several bird species.
- Joerg A. Fritz
- , Joseph Brancale
- & Michael P. Brenner
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Wnt signalling underlies the evolution of new phenotypes and craniofacial variability in Lake Malawi cichlids
The molecular mechanisms that promote and constrain the evolution of morphological traits remain unclear. Here, Parsons et al. show that the Wnt pathway is associated with the development of a novel head form in Lake Malawi cichlid fish but also limits head plasticity later in life.
- Kevin J. Parsons
- , A. Trent Taylor
- & R. Craig Albertson
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| Open AccessThe origin of the bifurcated axial skeletal system in the twin-tail goldfish
The ornamental twin-tail goldfish has a bifurcated caudal skeleton that arose during domestication, but the developmental mechanisms that generate this tail are unknown. Here, Abe et al. show that a mutation in the chordingene affects embryonic dorsal–ventral patterning causing the bifurcated tail skeleton.
- Gembu Abe
- , Shu-Hua Lee
- & Kinya G. Ota
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Hemichordate neurulation and the origin of the neural tube
The evolutionary origins of the chordate neural tube and notochord are unclear. Here the authors show the expression patterns of chordate patterning genes in a hemichordate, which suggest that the hemichordate endoderm and collar cord might be homologous to the chordate notochord and neural tube, respectively.
- Norio Miyamoto
- & Hiroshi Wada
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Changes in the regulation of cortical neurogenesis contribute to encephalization during amniote brain evolution
Reptilian cortical development provides insights into amniote brain evolution. Here, the authors show that cortical neural progenitors in geckoes exhibit limited neurogenic potential, but generate multiple neuron subtypes similar to mammals.
- Tadashi Nomura
- , Hitoshi Gotoh
- & Katsuhiko Ono