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Ants are highly polyphenic Hymenoptera, with at least three distinct adult forms in the vast majority of species. Their sexual dimorphism, however, is overlooked to the point of being a nearly forgotten phenomenon. Using a multimodal approach, we interrogate the near total head microanatomy of the male of Dorylus helvolus, the "sausagefly," and compare it with the conspecific or near-conspecific female castes, the "driver ants." We found that no specific features were shared uniquely between the workers and males to the exclusion of the queens, indicating independence of male and worker development; males and queens, however, uniquely shared several features. Certain previous generalizations about ant sexual dimorphism are confirmed, while we also discover discrete muscular presences and absences, for which reason we provide a coarse characterization of functional morphology. Based on the unexpected retention of a medial carinate line on the structurally simplified mandible of the male, we postulate a series of developmental processes to explain the patterning of ant mandibles. We invoke functional and anatomical principles to classify sensilla. Critically, we observe an inversion of the expected pattern of male-queen mandible development: male Dorylus mandibles are extremely large while queen mandibles are poorly developed. To explain this, we posit that the reproductive-limited mandible phenotype is canalized in Dorylus, thus partially decoupling the queen and worker castes. We discuss alternative hypotheses and provide further comparisons to understand mandibular evolution in army ants. Furthermore, we hypothesize that the expression of the falcate phenotype in the queen is coincidental, that is, a "spandrel," and that the form of male mandibles is also generally coincidental across the ants. We conclude that the theory of ant development and evolution is incomplete without consideration of the male system, and we call for focused study of male anatomy and morphogenesis, and of trait limitation across all castes.

Evolutionary constraints may significantly bias phenotypic change, while “breaking” from such constraints can lead to expanded ecological opportunity. Ray-finned fishes have broken functional constraints by developing two jaws (oral-pharyngeal), decoupling prey capture (oral jaw) from processing (pharyngeal jaw). It is hypothesized that the oral and pharyngeal jaws represent independent evolutionary modules and this facilitated diversification in feeding architectures. Here we test this hypothesis in African cichlids. Contrary to our expectation, we find integration between jaws at multiple evolutionary levels. Next, we document integration at the genetic level, and identify a candidate gene, smad7, within a pleiotropic locus for oral and pharyngeal jaw shape that exhibits correlated expression between the two tissues. Collectively, our data show that African cichlid evolutionary success has occurred within the context of a coupled jaw system, an attribute that may be driving adaptive evolution in this iconic group by facilitating rapid shifts between foraging habitats, providing an advantage in a stochastic environment such as the East African Rift-Valley., Modular, rather than integrated systems are classically thought to allow functional diversity to evolve rapidly. A study of cichlid fish shows integration between divergent jaw systems at the phylogenetic, population, and genetic scales, suggesting integration can and does facilitate rapid, coordinated trait evolution.

The polychaete Boccardia wellingtonensis is a poecilogonous species that produces different larval types. Females may lay Type I capsules, in which only planktotrophic larvae are present, or Type III capsules that contain planktotrophic and adelphophagic larvae as well as nurse eggs. While planktotrophic larvae do not feed during encapsulation, adelphophagic larvae develop by feeding on nurse eggs and on other larvae inside the capsules and hatch at the juvenile stage. Previous works have not found differences in the morphology between the two larval types; thus, the factors explaining contrasting feeding abilities in larvae of this species are still unknown. In this paper, we use a transcriptomic approach to study the cellular and genetic mechanisms underlying the different larval trophic modes of B. wellingtonensis. By using approximately 624 million high-quality reads, we assemble the de novo transcriptome with 133,314 contigs, coding 32,390 putative proteins. We identify 5221 genes that are up-regulated in larval stages compared to their expression in adult individuals. The genetic expression profile differed between larval trophic modes, with genes involved in lipid metabolism and chaetogenesis over expressed in planktotrophic larvae. In contrast, up-regulated genes in adelphophagic larvae were associated with DNA replication and mRNA synthesis.

Sex allocation is one of the most studied traits in evolutionary biology because its theoretical predictions match the empirical data. Here, using the Ryukyu dry-wood termite Neotermes sugioi, we investigated several factors that could bias the sex allocation in three populations (Okinawa, Ishigaki/Iriomote, and Yonaguni). Our survey showed that there were more queen-only colonies than king-only colonies in these populations, suggesting a longer lifespan of the queens than that of the kings. In this condition, sex-asymmetric reproductive value (SRV) theory predicts female bias, because even after the short-lived kings die, the long-lived queens can continue reproduction with their sons. However, sex allocation in this species seemed to be biased toward males. Furthermore, we examined the possibility of intrasexual competition among siblings (ICS). If ICS is the cause of the bias, the allocation is expected to change depending on the total investment in sexual offspring. However, the biomass of both male and female alates increased linearly with the increase in the total biomass of the alates in these populations. Thus, neither the SRV nor the ICS theory could explain the male-biased sex ratio of N. sugioi. On the basis of these results, we discuss the remaining possibilities in this species.

The last common ancestor of all living arthropods had biramous postantennal appendages, with an endopodite and exopodite branching off the limb base. Morphological evidence for homology of these rami between crustaceans and chelicerates has, however, been challenged by data from clonal composition and from knockout of leg patterning genes. Cambrian arthropod fossils have been cited as providing support for competing hypotheses about biramy but have shed little light on additional lateral outgrowths, known as exites. Here we draw on microtomographic imaging of the Cambrian great-appendage arthropod Leanchoilia to reveal a previously undetected exite at the base of most appendages, composed of overlapping lamellae. A morphologically similar, and we infer homologous, exite is documented in the same position in members of the trilobite-allied Artiopoda. This early Cambrian exite morphology supplements an emerging picture from gene expression that exites may have a deeper origin in arthropod phylogeny than has been appreciated., The common ancestor of all living arthropods had biramous postantennal appendages, with an endopodite and exopodite branching off the limb base. This study uses microtomographic imaging of the Cambrian arthropod Leanchoilia to reveal a previously undetected exite at the base of most appendages, suggesting a deeper origin for exites in arthropod phylogeny.

RNA interference (RNAi) plays important roles in organism development through post-transcriptional regulation of specific target mRNAs. Target specificity is largely controlled by base-pair complementarity between micro-RNA (miRNA) regulatory elements and short regions of the target mRNA. The pattern of miRNA production in a cell interacts with the cell’s mRNA transcriptome to generate a specific network of post-transcriptional regulation that can play critical roles in cellular metabolism, differentiation, tissue/organ development and developmental timing. In plants, miRNA production is orchestrated in the nucleus by a suite of proteins that control transcription of the pri-miRNA gene, post-transcriptional processing and nuclear export of the mature miRNA. In the model plant, Arabidopsis thaliana, post-transcriptional processing of miRNAs is controlled by a pair of physically-interacting proteins, HYL1 and DCL1. However, the evolutionary history of the HYL1-DCL1 interaction is unknown, as is its structural basis. Here we use ancestral sequence reconstruction and functional characterization of ancestral HYL1 in vitro and in vivo to better understand the origin and evolution of the HYL1-DCL1 interaction and its impact on miRNA production and plant development. We found the ancestral plant HYL1 evolved high affinity for both double-stranded RNA (dsRNA) and its DCL1 partner very early in plant evolutionary history, before the divergence of mosses from seed plants (~500 Ma), and these high-affinity interactions remained largely conserved throughout plant evolutionary history. Structural modeling and molecular binding experiments suggest that the second of two double-stranded RNA-binding motifs (DSRMs) in HYL1 may interact tightly with the first of two C-terminal DCL1 DSRMs to mediate the HYL1-DCL1 physical interaction necessary for efficient miRNA production. Transgenic expression of the nearly 200 Ma-old ancestral flowering-plant HYL1 in A. thaliana was sufficient to rescue many key aspects of plant development disrupted by HYL1− knockout and restored near-native miRNA production, suggesting that the functional partnership of HYL1-DCL1 originated very early in and was strongly conserved throughout the evolutionary history of terrestrial plants. Overall, our results are consistent with a model in which miRNA-based gene regulation evolved as part of a conserved plant ‘developmental toolkit’; its role in generating developmental novelty is probably related to the relatively rapid evolution of miRNA genes.

Premise of research. Staminodes are infertile stamens that have evolved numerous times in angiosperms and exhibit a vast array of forms and functions. Variation in staminodes suggests that numerous...

Background Amphiprion ocellaris is one of the rare reef fish species that can be reared in aquaria. It is increasingly used as a model species for Eco‐Evo‐Devo. Therefore, it is important to have an embryonic development table based on high quality images that will allow for standardized sampling by the scientific community. Results Here we provide high‐resolution time‐lapse videos to accompany a detailed description of embryonic development in A ocellaris. We describe a series of developmental stages and we define six broad periods of embryogenesis: zygote, cleavage, blastula, gastrula, segmentation, and organogenesis that we further subdivide into 32 stages. These periods highlight the changing spectrum of major developmental processes that occur during embryonic development. Conclusions We provide an easy system for the determination of embryonic stages, enabling the development of A ocellaris as a coral reef fish model species. This work will facilitate evolutionary development studies, in particular studies of the relationship between climate change and developmental trajectories in the context of coral reefs. Thanks to its lifestyle, complex behavior, and ecology, A ocellaris will undoubtedly become a very attractive model in a wide range of biological fields., Key Findings Six periods have been identified to describe the embryonic development of the false clown‐fish Amphiprion ocellaris.We provide a staging series organized similarly to other models allowing comparative stud‐ies of embryonic development.We provide high‐resolution time‐lapse videos to accompany a detailed description of embry‐onic development in Amphiprion ocellaris.These data provide a general framework that can be used as a tool to standardize studies and experimental procedures throughout false clownfish development.

Mammaliamorpha comprises the last common ancestor of Tritylodontidae and Mammalia plus all its descendants1. Tritylodontids are nonmammaliaform herbivorous cynodonts that originated in the Late Triassic epoch, diversified in the Jurassic period2–5 and survived into the Early Cretaceous epoch6,7. Eutriconodontans have generally been considered to be an extinct mammalian group, although different views exist8. Here we report a newly discovered tritylodontid and eutriconodontan from the Early Cretaceous Jehol Biota of China. Eutriconodontans are common in this biota9, but it was not previously known to contain tritylodontids. The two distantly related species show convergent features that are adapted for fossorial life, and are the first ‘scratch-diggers’ known from this biota. Both species also show an increased number of presacral vertebrae, relative to the ancestral state in synapsids or mammals10,11, that display meristic and homeotic changes. These fossils shed light on the evolutionary development of the axial skeleton in mammaliamorphs, which has been the focus of numerous studies in vertebrate evolution12–17 and developmental biology18–28. The phenotypes recorded by these fossils indicate that developmental plasticity in somitogenesis and HOX gene expression in the axial skeleton—similar to that observed in extant mammals—was already in place in stem mammaliamorphs. The interaction of these developmental mechanisms with natural selection may have underpinned the diverse phenotypes of body plan that evolved independently in various clades of mammaliamorph. Fossiomanus sinensis and Jueconodon cheni, a newly described Early Cretaceous tritylodontid and eutriconodotan, respectively, show convergence on a fossorial body plan and provide insights into the evolution of the axial skeleton in mammaliamorphs.

The origin of the jaw is a long-standing problem in vertebrate evolutionary biology. Classical hypotheses of serial homology propose that the upper and lower jaw evolved through modifications of dorsal and ventral gill arch skeletal elements, respectively. If the jaw and gill arches are derived members of a primitive branchial series, we predict that they would share common developmental patterning mechanisms. Using candidate and RNAseq/differential gene expression analyses, we find broad conservation of dorsoventral patterning mechanisms within the developing mandibular, hyoid and gill arches of a cartilaginous fish, the skate (Leucoraja erinacea). Shared features include expression of genes encoding members of the ventralising BMP and endothelin signalling pathways and their effectors, the joint markers bapx1 and gdf5 and pro-chondrogenic transcription factors barx1 and gsc, and the dorsalising transcription factor pou3f3. Additionally, we find that mesenchymal expression ofeya1/six1is an ancestral feature of the mandibular arch of jawed vertebrates, while differences in notch signalling distinguish the mandibular and gill arches in skate. Comparative transcriptomic analyses of mandibular and gill arch tissues reveal additional genes differentially expressed along the dorsoventral axis of the pharyngeal arches, includingscamp5as a novel marker of the dorsal mandibular arch, as well as distinct transcriptional features of mandibular and gill arch muscle progenitors and developing gill buds. Taken together, our findings reveal conserved patterning mechanisms in the pharyngeal arches of jawed vertebrates, consistent with serial homology of their skeletal derivatives, as well as unique transcriptional features that may underpin distinct jaw and gill arch morphologies.

Floral phyllotaxis is a relatively robust phenotype; trimerous and pentamerous arrangements are widely observed in monocots and core eudicots. Conversely, it also shows variability in some angiosperm clades such as ‘ANA’ grade (Amborellales, Nymphaeales, and Austrobaileyales), magnoliids, and Ranunculales. Regardless of the phylogenetic relationship, however, phyllotactic pattern formation appears to be a common process. What are the causes of the variability in floral phyllotaxis and how has the variation of floral phyllotaxis contributed to floral diversity? In this review, I summarize recent progress in studies on two related fields to develop answers to these questions. First, it is known that molecular and cellular stochasticity are inevitably found in biological systems, including plant development. Organisms deal with molecular stochasticity in several ways, such as dampening noise through gene networks or maintaining function through cellular redundancy. Recent studies on molecular and cellular stochasticity suggest that stochasticity is not always detrimental to plants and that it is also essential in development. Second, studies on vegetative and inflorescence phyllotaxis have shown that plants often exhibit variability and flexibility in phenotypes. Three types of phyllotaxis variations are observed, namely, fluctuation around the mean, transition between regular patterns, and a transient irregular organ arrangement called permutation. Computer models have demonstrated that stochasticity in the phyllotactic pattern formation plays a role in pattern transitions and irregularities. Variations are also found in the number and positioning of floral organs, although it is not known whether such variations provide any functional advantages. Two ways of diversification may be involved in angiosperm floral evolution: precise regulation of organ position and identity that leads to further specialization of organs and organ redundancy that leads to flexibility in floral phyllotaxis.

Before limbs or fins, can be patterned and grow they must be initiated. Initiation of the limb first involves designating a portion of lateral plate mesoderm along the flank as the site of the future limb. Following specification, a myriad of cellular and molecular events interact to generate a bud that will grow and form the limb. The past three decades has provided a wealth of understanding on how those events generate the limb bud and how variations in them result in different limb forms. Comparatively, much less attention has been given to the earliest steps of limb formation and what impacts altering the position and initiation of the limb have had on evolution. Here, we first review the processes and pathways involved in these two phases of limb initiation, as determined from amniote model systems. We then broaden our scope to examine how variation in the limb initiation module has contributed to biological diversity in amniotes. Finally, we review what is known about limb initiation in fish and amphibians, and consider what mechanisms are conserved across vertebrates.

The field of evolutionary developmental biology can help address how morphological novelties evolve, a key question in evolutionary biology. In Arabidopsis thaliana, APETALA2 (AP2) plays a role in the development of key plant innovations including seeds, flowers, and fruits. AP2 belongs to the AP2/ETHYLENE RESPONSIVE ELEMENT BINDING FACTOR family which has members in all viridiplantae, making it one of the oldest and most diverse gene lineages. One key subclade, present across vascular plants is the euAPETALA2 (euAP2) clade, whose founding member is AP2. We reconstructed the evolution of the euAP2 gene lineage in vascular plants to better understand its impact on the morphological evolution of plants, identifying seven major duplication events. We also performed spatiotemporal expression analyses of euAP2/TOE3 genes focusing on less explored vascular plant lineages, including ferns, gymnosperms, early diverging angiosperms and early diverging eudicots. Altogether, our data suggest that euAP2 genes originally contributed to spore and sporangium development, and were subsequently recruited to ovule, fruit and floral organ development. Finally, euAP2 protein sequences are highly conserved; therefore, changes in the role of euAP2 homologs during development are most likely due to changes in regulatory regions.

Pristionchus pacificus has emerged as an important nematode species used to understand the evolution of development and behavior. While P. pacificus (Diplogasteridae) is only distantly related to Caenorhabditis elegans (Rhabditidae), both use an identical reproductive strategy, are easily reared on bacteria in Petri dishes and complete their life cycles within a few days. Over the past 25 years, several detailed light and electron microscopy studies have elucidated the anatomy of P. pacificus and have demonstrated clear homology to many cells in C. elegans. Despite this similarity, sufficient anatomical differences between C. elegans and P. pacificus have allowed the latter to be used in comparative evo-devo studies. For example, the stoma of P. pacificus contains a large dorsal tooth used during predation on other nematodes when supplementing its primarily bacterial diet. This review discusses the main anatomical features of P. pacificus with emphasis on comparison to C. elegans.

The homeobox transcription factor Caudal has conserved roles in all Bilateria in defining the posterior pole and in controlling posterior elongation. These roles are seemingly similar and are difficult to disentangle. We have carried out a detailed analysis of the expression, function and interactions of the caudal ortholog of the milkweed bug, Oncopeltus fasciatus, a hemimetabolous insect with a conservative early development process, in order to understand its different functions throughout development. In Oncopeltus, caudal is not maternally deposited, but has a sequence of roles in the posterior of the embryos throughout early development. It defines and maintains a posterior-anterior gradient in the blastoderm and modulates the activity of segmentation genes in simultaneous segmentation during the blastoderm stage. It later defines the invagination site and the posterior segment addition zone (SAZ) in the germband. It maintains the posterior SAZ cells in an undifferentiated proliferative state, while promoting dynamic expression of segmentation genes in the anterior SAZ. We show that rather than being a simple posterior determinant, Caudal is involved in several distinct regulatory networks, each with a distinct developmental role.

Changes in gene regulation underlie much of phenotypic evolution1. However, our understanding of the potential for regulatory evolution is biased, because most evidence comes from either natural variation or limited experimental perturbations2. Using an automated robotics pipeline, we surveyed an unbiased mutation library for a developmental enhancer in Drosophila melanogaster. We found that almost all mutations altered gene expression and that parameters of gene expression—levels, location, and state—were convolved. The widespread pleiotropic effects of most mutations may constrain the evolvability of developmental enhancers. Consistent with these observations, comparisons of diverse Drosophila larvae revealed apparent biases in the phenotypes influenced by the enhancer. Developmental enhancers may encode a higher density of regulatory information than has been appreciated previously, imposing constraints on regulatory evolution. A robotic pipeline is used to survey a library of mutations in a Drosphila gene enhancer, showing that most mutations altered gene expression and had widespread pleiotropic effects that are likely to constrain regulatory evolution.

The stalked jellyfish (Staurozoa) is an extraordinary clade within medusozoan cnidarians in which the medusa is attached to the substrate unlike the pelagic jellyfishes which compose the rest of the medusozoans. Along with this remarkable feature, staurozoans are characterized by an extremely low number of cells (

Although the development of the avian skeleton has attracted considerable attention, most of the studies have been concentrated on the embryonic period, while studies on the postnatal period are rare. We studied the postnatal development of the skeleton in two phylogenetically distant birds, an altricial passerine Acrocephalus scirpaceus and a semiprecocial charadriiform Chroicocephalus ridibundus. The neonates of the former, despite being altricial, have well-ossified skeleton-the degree of development approaches that of the semiprecocial gull. However, after hatching the limb bones (particularly those of the hind limb) ossify earlier in the gull which is probably related to faster acquisition of locomotor abilities. We have observed that, in contrast to previous reports from neognathous birds, in the ankle of the gull, the ascending process fuses with the astragalus rather than with the calcaneum. This type of development is present in palaeognaths and nonavian dinosaurs but has not yet been reported in neognaths. This indicates a greater diversity within Neognathae and suggests a more complex scenario for the evolution of the avian ankle. However, data from a greater number of species are needed to establish the developmental sequence ancestral for neognathous birds. Furthermore, the sequence of bone fusions in the wrist of Acrocephalus is similar to the fossil-documented evolutionary sequence observed in the phylogeny of early birds, with the semilunate carpal and major metacarpal fusing first, followed by the alular metacarpal fusing with the major metacarpal and then the major and minor metacarpal fusing proximally. These data underscore the importance of developmental studies for reconstructing the evolutionary history.

Regulatory genes are often multifunctional and constrained, which results in evolutionary conservation. It is difficult to understand how a regulatory gene could be lost from one species’ genome when it is essential for viability in closely related species. The gene paired is a classic Drosophila pair-rule gene, required for formation of alternate body segments in diverse insect species. Surprisingly, paired was lost in mosquitoes without disrupting body patterning. Here, we demonstrate that a paired family member, gooseberry, has acquired paired-like expression in the malaria mosquito Anopheles stephensi. Anopheles-gooseberry CRISPR-Cas9 knock-out mutants display pair-rule phenotypes and alteration of target gene expression similar to what is seen in Drosophila and beetle paired mutants. Thus, paired was functionally replaced by the related gene, gooseberry, in mosquitoes. Our findings document a rare example of a functional replacement of an essential regulatory gene and provide a mechanistic explanation of how such loss can occur., Cheatle Jarvela et al. demonstrate in the mosquito Anopheles stephensi that the paired gene was functionally replaced by the gene gooseberry, even though paired is essential in other insects such as fruit flies and beetles. This study contributes to the understanding of how essential genes are lost despite their importance during development.

Soft tissue preservation in fossil birds provides a rare window into their anatomy, function, and development. Here, we present an exceptionally-preserved specimen of Confuciusornis which, through Laser-Stimulated Fluorescence imaging, is identified as preserving a disassociated rhamphotheca. Reconstruction of the in vivo position of the rhamphotheca validates the association of the rhamphotheca with two previous confuciusornithid specimens while calling that of a third specimen into question. The ease of dissociation is discussed and proposed with a fourth specimen alongside finite element analysis as evidence for preferential soft-food feeding. However, this proposition remains tentative until there is a better understanding of the functional role of beak attachment in living birds. Differences in post-rostral extent and possibly rhamphotheca curvature between confuciusornithids and modern birds hint at developmental differences between the two. Together, this information provides a wealth of new information regarding the nature of the beak outside crown Aves., Miller et al. present a disassociated rhamphotheca of a Cretaceous bird, which sheds light on the diet and developmental biology of some of the earliest birds. Exceptionally preserved fossils are rare but when soft tissue is preserved it can provide insight into the anatomy and behavior of extinct organisms.

Inferring the genetic architecture of evolution in the fossil record is difficult because genetic crosses are impossible, the acquisition of DNA is usually impossible and phenotype–genotype maps are rarely obvious. However, such inference is valuable because it reveals the genetic basis of microevolutionary change across many more generations than is possible in studies of extant taxa, thereby integrating microevolutionary process and macroevolutionary pattern. Here, we infer the genetic basis of pelvic skeleton reduction in Gasterosteus doryssus, a Miocene stickleback fish from a finely resolved stratigraphic sequence that spans nearly 17,000 years. Reduction in pelvic score, a categorical measure of pelvic structure, resulted primarily from reciprocal frequency changes of two discrete phenotypic classes. Pelvic vestiges also showed left-side larger asymmetry. These patterns implicate Pitx1, a large-effect gene whose deletion generates left-side larger asymmetry of pelvic vestiges in extant, closely related Gasterosteus aculeatus. In contrast, reductions in the length of the pelvic girdle and pelvic spines resulted from directional shifts of unimodal, continuous trait distributions, suggesting an additional suite of genes with minor, additive pelvic effects, again like G. aculeatus. Similar genetic architectures explain shared but phyletically independent patterns across 10 million years of stickleback evolution. The authors infer that pelvic skeleton reduction in a fossil sequence of the Miocene stickleback fish, Gasterosteus doryssus, proceeds through the same gene of large effect and a similar suite of genes of small effect as in a closely related extant species, Gasterosteus aculeatus.

Ectocarpus is a genus of filamentous, marine brown algae. Brown algae belong to the stramenopiles, a large supergroup of organisms that are only distantly related to animals, land plants and fungi. Brown algae are also one of only a small number of eukaryotic lineages that have evolved complex multicellularity. For many years, little information was available concerning the molecular mechanisms underlying multicellular development in the brown algae, but this situation has changed with the emergence of Ectocarpus as a model brown alga. Here we summarise some of the main questions that are being addressed and areas of study using Ectocarpus as a model organism and discuss how the genomic information, genetic tools and molecular approaches available for this organism are being employed to explore developmental questions in an evolutionary context.

Spiralia is a large, ancient and diverse clade of animals, with a conserved early developmental program but diverse larval and adult morphologies. One trait shared by many spiralians is the presence of ciliary bands used for locomotion and feeding. To learn more about spiralian-specific traits we have examined the expression of 20 genes with protein motifs that are strongly conserved within the Spiralia, but not detectable outside of it. Here, we show that two of these are specifically expressed in the main ciliary band of the mollusc Tritia (also known as Ilyanassa). Their expression patterns in representative species from five more spiralian phyla—the annelids, nemerteans, phoronids, brachiopods and rotifers—show that at least one of these, lophotrochin, has a conserved and specific role in particular ciliated structures, most consistently in ciliary bands. These results highlight the potential importance of lineage-specific genes or protein motifs for understanding traits shared across ancient lineages., Spiralians have ciliary bands, used for locomotion and feeding, but defining molecular features of these structures are unknown. Here, the authors report a gene, Lophotrochin, that contains a protein domain only found in spiralians, and specifically expressed in diverse ciliary bands across the group, which provides a molecular signature for these structures.

One of the most important evolutionary innovations of vertebrates is a complexly structured telencephalon, which provides higher forms of nervous activity in animals and humans. This work is devoted to the study of the appearance of the telencephalon in the early stages of vertebrate evolution. At the same time, there is reason to believe that lampreys, due to their evolutionary antiquity, could retain some ancient expression patterns of genes that regulate the development of the brain in the very first vertebrates. The study of the features of spatio-temporal expression patterns of key genes that regulate the development of the forebrain in lampreys compared with other vertebrates can help to understand the molecular mechanisms underlying the appearance and evolutionary development of this unique structure of vertebrates. This paper presents the results from analyzing the gene-expression dynamics of Lanf, FoxG1, Otx2, Goosecoid, and HoxB9 in the early stages of development of the European river lamprey Lampetra fluviatilis. It was shown that lamprey genes involved in telencephalon differentiation (Lanf and FoxG1) exhibit heterochrony of expression compared with more evolutionarily advanced representatives of vertebrates. This fact confirms the idea that the telencephalon, being evolutionarily the youngest part of the brain, could appear in vertebrate ancestors as a superstructure in the late stages of their embryonic development.

The transient larva-bearing biphasic life cycle is the hallmark of many metazoan phyla, but how metazoan larvae originated remains a major enigma in animal evolution. There are two hypotheses for larval origin. The ‘larva-first’ hypothesis suggests that the first metazoans were similar to extant larvae, with later evolution of the adult-added biphasic life cycle; the ‘adult-first’ hypothesis suggests that the first metazoans were adult forms, with the biphasic life cycle arising later via larval intercalation. Here, we investigate the evolutionary origin of primary larvae by conducting ontogenetic transcriptome profiling for Mollusca—the largest marine phylum characterized by a trochophore larval stage and highly variable adult forms. We reveal that trochophore larvae exhibit rapid transcriptome evolution with extraordinary incorporation of novel genes (potentially contributing to adult shell evolution), and that cell signalling/communication genes (for example, caveolin and innexin) are probably crucial for larval evolution. Transcriptome age analysis of eight metazoan species reveals the wide presence of young larval transcriptomes in both trochozoans and other major metazoan lineages, therefore arguing against the prevailing larva-first hypothesis. Our findings support an adult-first evolutionary scenario with a single metazoan larval intercalation, and suggest that the first appearance of proto-larva probably occurred after the divergence of direct-developing Ctenophora from a metazoan ancestor. Evolutionary analysis of transcriptomes across Metazoa supports a scenario of ancestral adult stages and a single intercalation event at the origin of larvae.

Since the discovery two decades ago that transgenes are efficiently integrated into the genome by homologous recombination in the moss Physcomitrella patens, it has been a premier model system to study evolutionary development (evo-devo) questions, stem cell reprogramming, as well as explore the biology of non-vascular plants. P. patens was the first non-seed plant to have its genome sequenced and with this level of genomic information together with increasing molecular genetic tools, a large number of reverse genetic studies have propelled the use of this model system. However, a number of technological advances have recently opened the doors to forward genetics as well as extremely efficient and precise genome editing. Additionally, careful phylogenetic studies with increased resolution suggest that P. patens emerged from within Physcomitrium. Thus, rather than Physcomitrella patens the species should be named Physcomitrium patens. Here we review these advances and describe the areas where P. patens has had the most impact on plant biology.

While pregnancy-related proteins (PRP) are known to contribute to immunotolerance during pregnancy, their significance to development of invasive placenta is unclear. We compared PRP expression in humans and the common marmoset (Callithrix jacchus), a new-world monkey. Invasive placenta was observed at the maternal-foetal interface of marmoset placenta from green fluorescent protein (GFP)-expressing foetus and wild type mother. The pregnancy zone protein (PZP) and alpha-2 macroglobulin-like 1 (A2ML1) proteins exhibited the most prominent increase in expression during the second trimester in humans and marmoset, respectively. In humans, PZP accumulated at the maternal-foetal interface and A2ML1 accumulated in the amnion. Similarly, A2ML1 mRNA was detected in marmoset placenta. These proteins belong to the A2M family of protease inhibitors, and both PZP and A2ML1 share around 90% homology between human and marmoset and have highly conserved structures. However, the protease-reacting bait regions of the proteins had lower homology (56.8–60.7% in proteins) relative to the rest of the sequence. Notably, the cleavage site of a proinflammatory proline-endopeptidase was preserved in human PZP and marmoset A2ML1. These proteins contain multiple sites that are cleaved by proteases involving proline-endopeptidase. Systemic regulation of these A2M family proteins may be important in animals with invasive placenta.

Hookworms are intestinal parasites that cause major public health problems, especially in developing countries. To differentiate eggs from different hookworm species, it is necessary to use molecular methodologies, since the eggs are morphologically similar. Here, we performed the molecular identification of single hookworm eggs from six Brazilian states. Of the 634 eggs individually analyzed, 98.1% (622/634) represented Necator americanus, and surprisingly, 1.9% (12/634 eggs from the same patient) represented Ancylostoma caninum. DNA analysis of the A. caninum-positive stool sample revealed no contamination with animal feces. This is the first report of the presence of A. caninum eggs in human feces, which may have a direct implication for the epidemiology of hookworm infection caused by this species. This suggests the need for special attention regarding prophylaxis, as different reservoirs, previously not described, may have great relevance for the spread of A. caninum.

Carpels, the female reproductive organs of flowering plants, are of major economic importance since much of our food is ultimately derived from carpel tissue and they are a defining innovation for flowering plants. Amazingly, little is known about the origin and conservation of the developmental program of the carpel besides the knowledge generated by utilizing Arabidopsis thaliana. However, in the past few years advances in ancestral state reconstruction, developmental genetics, and phylogenetic analyses led to advances in the field of flower evodevo. Here, I summarize recent work on ancestral state reconstructions of carpels, and the functions of the major components of the genetic networks governing carpel development described for Arabidopsis. Then, I point out how the stepwise addition of genes during land plant evolution has generated the A. thaliana carpel's developmental toolkit. By merging these observations, I propose a basic version of the ancestral angiosperm carpel developmental network.

Animals that can reproduce vegetatively by fission or budding and also sexually via specialized gametes are found in all five primary animal lineages (Bilateria, Cnidaria, Ctenophora, Placozoa, Porifera). Many bilaterian lineages, including roundworms, insects, and most chordates, have lost the capability of vegetative reproduction and are obligately gametic. We suggest a developmental explanation for this evolutionary phenomenon: obligate gametic reproduction is the result of germline stem cells winning a winner-take-all competition with non-germline stem cells for control of reproduction and hence lineage survival. We develop this suggestion by extending Hamilton’s rule, which factors the relatedness between parties into the cost/benefit analysis that underpins cooperative behaviors, to include similarity of cellular state. We show how coercive or deceptive cell-cell signaling can be used to make costly cooperative behaviors appear less costly to the cooperating party. We then show how competition between stem-cell lineages can render an ancestral combination of vegetative reproduction with facultative sex unstable, with one or the other process driven to extinction. The increased susceptibility to cancer observed in obligately-sexual lineages is, we suggest, a side-effect of deceptive signaling that is exacerbated by the loss of whole-body regenerative abilities. We suggest a variety of experimental approaches for testing our predictions.

Background Alternative patterns of secondary growth in stems of Nyctaginaceae is present in all growth habits of the family and have been known for a long time. However, the interpretation of types of cambial variants have been controversial, given that different authors have given them different developmental interpretations. The different growth habits coupled with an enormous stem anatomical diversity offers the unique opportunity to investigate the evolution of complex developments, to address how these anatomies shifted within habits, and how the acquisition of novel cambial variants and habit transitions impacted the diversification of the family. Methods We integrated developmental data with a phylogenetic framework to investigate the diversity and evolution of stem anatomy in Nyctaginaceae using phylogenetic comparative methods, reconstructing ancestral states, and examining whether anatomical shifts correspond to species diversification rate shifts in the family. Results Two types of cambial variants, interxylary phloem and successive cambia, were recorded in Nyctaginaceae, which result from four different ontogenies. These ontogenetic trajectories depart from two distinct primary vascular structures (regular or polycyclic eustele) yet, they contain shared developmental stages which generate stem morphologies with deconstructed boundaries of morphological categories (continuum morphology). Unlike our a priori hypotheses, interxylary phloem is reconstructed as the ancestral character for the family, with three ontogenies characterized as successive cambia evolving in few taxa. Cambial variants are not contingent on habits, and their transitions are independent from species diversification. Conclusions Our findings suggest that multiple developmental mechanisms, such as heterochrony and heterotopy, generate the transitions between interxylary phloem and successive cambia. Intermediate between these two extremes are present in Nyctaginaceae, suggesting a continuum morphology across the family as a generator of anatomical diversity.

Understanding the origin of novelty is a key question in evolutionary developmental biology. In arthropods, the body wall has served as a repeated source of morphological novelty. In treehoppers, an ancestrally flat part of the dorsal body wall (the pronotum) was transformed into a three-dimensional structure (the helmet), which was subsequently moulded by natural selection into diverse shapes. Here, we test three hypotheses for the developmental origin of the helmet by comparing body-region transcriptomes in a treehopper and a leafhopper that retains more ancestral morphology. In leafhoppers, pronotal gene expression is most similar to that of its serial homologue, the mesonotum. By contrast, in treehoppers, helmet gene expression is most similar to that of wings, supporting the wing-patterning network co-option hypothesis for the origin of the helmet. These results suggest that serial homologues may diverge evolutionarily through replacement of, rather than tinkering with, their ancestrally shared patterning network.

Species retaining ancestral features, such as species called living fossils, are often regarded as less derived than their sister groups, but such discussions are usually based on qualitative enumeration of conserved traits. This approach creates a major barrier, especially when quantifying the degree of phenotypic evolution or degree of derivedness, since it focuses only on commonly shared traits, and newly acquired or lost traits are often overlooked. To provide a potential solution to this problem, especially for inter-species comparison of gene expression profiles, we propose a new method named “derivedness index” to quantify the degree of derivedness. In contrast to the conservation-based approach, which deals with expressions of commonly shared genes among species being compared, the derivedness index also considers those that were potentially lost or duplicated during evolution. By applying our method, we found that the gene expression profiles of penta-radial phases in echinoderm tended to be more highly derived than those of the bilateral phase. However, our results suggest that echinoderms may not have experienced much larger modifications to their developmental systems than chordates, at least at the transcriptomic level. In vertebrates, we found that the mid-embryonic and organogenesis stages were generally less derived than the earlier or later stages, indicating that the conserved phylotypic period is also less derived. We also found genes that potentially explain less derivedness, such as Hox genes. Finally, we highlight technical concerns that may influence the measured transcriptomic derivedness, such as read depth and library preparation protocols, for further improvement of our method through future studies. We anticipate that this index will serve as a quantitative guide in the search for constrained developmental phases or processes.

All females adopt an evolutionary conserved reproduction strategy; under unfavorable conditions such as scarcity of food or mates, oocytes remain quiescent. However, the signals to maintain oocyte quiescence are largely unknown. Here, we report that in four different species – Caenorhabditis elegans, Caenorhabditis remanei, Drosophila melanogaster, and Danio rerio – octopamine and norepinephrine play an essential role in maintaining oocyte quiescence. In the absence of mates, the oocytes of Caenorhabditis mutants lacking octopamine signaling fail to remain quiescent, but continue to divide and become polyploid. Upon starvation, the egg chambers of D. melanogaster mutants lacking octopamine signaling fail to remain at the previtellogenic stage, but grow to full-grown egg chambers. Upon starvation, D. rerio lacking norepinephrine fails to maintain a quiescent primordial follicle and activates an excessive number of primordial follicles. Our study reveals an evolutionarily conserved function of the noradrenergic signal in maintaining quiescent oocytes., Kim et al. show noradrenergic signaling for stress responses such as flight and fight, also serves as a conserved signal for maintaining oocyte quiescence under unfavorable conditions in worms, flies, and fish.

The Rio Pearlfish Nematolebias whitei is a bi-annual killifish species inhabiting seasonal pools of the Rio de Janeiro region that dry twice per year. Embryos enter dormant diapause stages in the soil, waiting for the inundation of the habitat which triggers hatching and commencement of a new life cycle. This species represents a convergent, independent origin of annualism from other emerging killifish model species. While some transcriptomic datasets are available for Rio Pearlfish, thus far a sequenced genome has been unavailable. Here we present a high quality, 1.2Gb chromosome-level genome assembly, genome annotations and a comparative genomic investigation of the Rio Pearlfish as representative of a vertebrate clade that evolved environmentally-cued hatching. We show conservation of 3-D genome structure across teleost fish evolution, developmental stages, tissues and cell types. Our analysis of mobile DNA shows that Rio Pearlfish, like other annual killifishes, possesses an expanded transposable element profile with implications for rapid aging and adaptation to harsh conditions. We use the Rio Pearlfish genome to identify its hatching enzyme gene repertoire and the location of the hatching gland, a key first step in understanding the developmental genetic control of hatching. The Rio Pearlfish genome expands the comparative genomic toolkit available to study convergent origins of seasonal life histories, diapause, and rapid aging phenotypes. We present the first set of genomic resources for this emerging model organism, critical for future functional genetic and multi-omic explorations of “Eco-Evo-Devo” phenotypes in resilience and adaptation to extreme environments.Significance:Seasonal or annual killifishes are emerging models for aging, life history adaptions to extreme environments, and ecological evolutionary developmental biology (Eco-Evo-Devo). Most studies have thus far focused on the African turquoise killifish Nothobranchius furzeri and the South American Austrofundulus limneaus. We sequenced and analyzed the genome of the Rio Pearlfish Nematolebias whitei from the Rio de Janeiro region, a seasonal species representing a convergent origin of seasonality from other sequenced killifish species, strengthening the comparative potential of Aplocheiloid killifishes as a model clade for the comparative and functional genomics of animal resilience to environmental change.

The development of sexual fruiting bodies is one of the most complex morphogenetic processes in fungi. Mycologists have long been fascinated by the morphological and developmental diversity of fruiting bodies; however, evolutionary developmental biology of fungi still lags significantly behind that of animals or plants. Here, we summarize the current state of knowledge on fruiting bodies of mushroom-forming Basidiomycota, focusing on phylogenetic and developmental biology. Phylogenetic approaches have revealed a complex history of morphological transformations and convergence in fruiting body morphologies. Frequent transformations and convergence is characteristic of fruiting bodies in contrast to animals or plants, where main body plans are highly conserved. At the same time, insights into the genetic bases of fruiting body development have been achieved using forward and reverse genetic approaches in selected model systems. Phylogenetic and developmental studies of fruiting bodies have each yielded major advances, but they have produced largely disjunct bodies of knowledge. An integrative approach, combining phylogenetic, developmental, and functional biology, is needed to achieve a true fungal evolutionary developmental biology (evo-devo) synthesis for fungal fruiting bodies.

The metabolic scaling in the animal has been discussed for over 90 years, but no consensus has been reached. Our analysis of 2,126 species of vertebrates reveals a significant allometric exponent heterogeneity. We show that classes of terrestrial vertebrates exhibit the evolution of metabolic scaling. Both the allometric coefficient "a" and the allometric exponent "b" change naturally, but differently depending on the geological time of group formation. The allometric coefficient "a" shows the measure of the evolutionary development of systems that forms resting metabolism in animals. Endothermic classes, such as birds and mammals, have a metabolic rate that is in an order of magnitude higher than that in ectothermic classes, including amphibians and reptiles. In the terrestrial vertebrate phylogeny, we find that the metabolic scaling is characterized by three main allometric exponent values: b = 3/4 (mammals), b > 3/4 (ectotherms, such as amphibians and reptiles), and b < 3/4 (birds). The heterogeneity of the allometric exponent is a natural phenomenon associated with the general evolution of vertebrates. The scaling factor decreases depending on both the external design and the size (birds vs mammals) of the animal. The metabolic rate and uniformity of species within a class increase as the geological start date of formation of the class approaches the present time. The higher the mass-specific standard metabolic rate in the class, the slower metabolic rate grows with increasing body size in this class. Our results lay the groundwork for further exploration of the evolutionary and ecological aspects of the development of metabolic scaling in animals. This article is protected by copyright. All rights reserved.

The Porifera are one of the best candidates as the sister group to all other metazoans. Studies on this phylum are therefore expected to shed light on the origin and early evolution of key animal features. Transcriptomic or genomic data acquired during the last 10 years have highlighted the conservation of most of the main genes and pathways involved in the development of the other metazoans. The next step is to determine how similar genetic tool boxes can result in widely dissimilar body plan organization, dynamics, and life histories. To answer these questions, three main axes of research are necessary: (1) conducting more gene expression studies; (2) developing knockdown protocols; and (3) reinterpreting sponge cell biology using modern tools. In this chapter we focus on the in situ hybridization (ISH) technique, needed to establish the spatiotemporal expression of genes, both on whole mount individuals and paraffin sections, and at different stages of development (adults, embryos, larvae, buds) of the homoscleromorph sponge Oscarella lobularis.

The gene regulatory network for segmentation in arthropods offers valuable insights into how networks evolve owing to the breadth of species examined and the extremely detailed knowledge gained in the model organism Drosophila melanogaster. These studies have shown that Drosophila's network represents a derived state that acquired changes to accelerate segment patterning, whereas most insects specify segments gradually as the embryo elongates. Such heterochronic shifts in segmentation have potentially emerged multiple times within holometabolous insects, resulting in many mechanistic variants and difficulties in isolating underlying commonalities that permit such shifts. Recent studies identified regulatory genes that work as timing factors, coordinating gene expression transitions during segmentation. These studies predict that changes in timing factor deployment explain shifts in segment patterning relative to other developmental events. Here, we test this hypothesis by characterizing the temporal and spatial expression of the pair-rule patterning genes in the malaria vector mosquito, Anopheles stephensi. This insect is a Dipteran (fly), like Drosophila, but represents an ancient divergence within this clade, offering a useful counterpart for evo-devo studies. In mosquito embryos, we observe anterior to posterior sequential addition of stripes for many pair-rule genes and a wave of broad timer gene expression across this axis. Segment polarity gene stripes are added sequentially in the wake of the timer gene wave and the full pattern is not complete until the embryo is fully elongated. This "progressive segmentation" mode in Anopheles displays commonalities with both Drosophila's rapid segmentation mechanism and sequential modes used by more distantly related insects.

The larval skeleton of the echinoderm is believed to have been acquired through co-option of a pre-existing gene regulatory network (GRN); that is, the mechanism for adult skeleton formation in the echinoderm was deployed in early embryogenesis during echinoderm diversification. To explore the evolutionary changes that occurred during co-option, we examined the mechanism for adult skeletogenesis using the starfish Patiria pectinifera. Expression patterns of skeletogenesis-related genes (vegf, vegfr, ets1/2, erg, alx1, ca1, and clect) suggest that adult skeletogenic cells develop from the posterior coelom after the start of feeding. Treatment with inhibitors and gene knockout using transcription activator-like effector nucleases (TALENs) suggest that the feeding-nutrient sensing pathway activates Vegf signaling via target of rapamycin (TOR) activity, leading to the activation of skeletogenic regulatory genes in starfish. In the larval skeletogenesis of sea urchins, the homeobox gene pmar1 activates skeletogenic regulatory genes, but in starfish, localized expression of the pmar1-related genes phbA and phbB was not detected during the adult skeleton formation stage. Based on these data, we provide a model for the adult skeletogenic GRN in the echinoderm and propose that the upstream regulatory system changed from the feeding-TOR-Vegf pathway to a homeobox gene-system during co-option of the skeletogenic GRN.

Genetic mechanisms controlling root development are well-understood in plant model species, and emerging frontier research is currently dissecting how some of these mechanisms control root development in cacti. Here we show the patterns of root architecture development in a gradient of divergent lineages, from populations to species in Mammillaria. First, we show the patterns of variation in natural variants of the species Mammillaria haageana. Then we compare this variation to closely related species within the Series Supertexta in Mammillaria (diverging for the last 2.1 million years) in which M. haageana is inserted. Finally, we compared these patterns of variation to what is found in a set of Mammillaria species belonging to different Series (diverging for the last 8 million years). When plants were grown in controlled environments, we found that the variation in root architecture observed at the intra-specific level, partially recapitulates the variation observed at the inter-specific level. These phenotypic outcomes at different evolutionary time-scales can be interpreted as macroevolution being the cumulative outcome of microevolutionary phenotypic divergence, such as the one observed in Mammillaria accessions and species.

Controlling the distribution of stomata is crucial for the adaptation of plants to new, or changing environments. While many plant species produce stomata predominantly on the abaxial leaf surface (hypostomy), some produce stomata on both surfaces (amphistomy), and the remaining few produce them only on the adaxial surface (hyperstomy). Various selective pressures have driven the evolution of these three modes of stomatal distribution. Despite recent advances in our understanding of stomatal development and dorsiventral leaf polarity, the genetic basis for the evolution of different stomatal distributions is still unclear. Here, we propose the genus Callitriche as a new model system to investigate patterns in the evolution of stomatal distribution. Callitriche comprises species with diverse lifestyles, including terrestrial, amphibious, and obligately aquatic plants. We found that species in this genus cover all three modes of dorsiventral stomatal distribution, making it a desirable model for comparative and evolutionary analyses on distribution modes. We further characterized the genetic basis of the different distribution modes, focusing on the stomatal key transcription factor SPEECHLESS. Future research using the promising model system Callitriche would open a new direction for evolutionary developmental biology studies on stomata.

Marsupials exhibit unique biological features that provide fascinating insights into many aspects of mammalian development. These include their distinctive mode of reproduction, altricial stage at birth, and the associated heterochrony that is required for their crawl to the pouch and teat attachment. Marsupials are also an invaluable resource for mammalian comparative biology, forming a distinct lineage from the extant placental and egg-laying monotreme mammals. Despite their unique biology, marsupial resources are lagging behind those available for placentals. The fat-tailed dunnart (Sminthopsis crassicaudata) is a laboratory based marsupial model, with simple and robust husbandry requirements and a short reproductive cycle making it amenable to experimental manipulations. Here we present a detailed staging series for the fat-tailed dunnart, focusing on their accelerated development of the forelimbs and jaws. This study provides the first skeletal developmental series on S. crassicaudata and provides a fundamental resource for future studies exploring mammalian diversification, development and evolution., Cook, Pask and colleagues describe the ossification of the skull and forelimbs in the developing postnatal fat-tailed dunnart. As one of the most altricial marsupials at birth with a short reproductive cycle and simple lab husbandry, this species is a promising model organism for jaw and forelimb development in mammals.

Summary Asymmetric and oriented stem cell divisions enable the continued production of patterned tissues. The molecules that guide these divisions include several "polarity proteins" that are localized to discrete plasma membrane domains, are differentially inherited during asymmetric divisions, and whose scaffolding activities can guide division plane orientation and subsequent cell fates. In the stomatal lineages on the surfaces of plant leaves, asymmetric and oriented divisions create distinct cell types in physiologically optimized patterns. The polarity protein BREAKING OF ASYMMETRY IN THE STOMATAL LINEAGE (BASL) is a major regulator of stomatal lineage division and cell fate asymmetries in Arabidopsis, but its role in the stomatal lineages of other plants is unclear. Here, using phylogenetic and functional assays, we demonstrate that BASL is a eudicot-specific polarity protein. Dicot BASL orthologs can polarize in heterologous systems and rescue the Arabidopsis BASL mutant. The more widely distributed BASL-like proteins, although they share BASL's conserved C-terminal domain, are neither polarized nor do they function in asymmetric divisions of the stomatal lineage. Comparison of BASL protein localization and loss of function BASL phenotypes in Arabidopsis and tomato revealed previously unappreciated differences in how asymmetric cell divisions are employed for pattern formation in different species. This multi-species analysis therefore provides insight into the evolution of a unique polarity regulator and into the developmental choices available to cells as they build and pattern tissues.

The three anterior-most segments in arthropods contain the ganglia that make up the arthropod brain. These segments, the pre-gnathal segments (PGS), are known to exhibit many developmental differences to other segments, believed to reflect their divergent morphology. We have analyzed the expression and function of the genes involved in the conserved segment-polarity network, including genes from the Wnt and Hedgehog pathways, in the PGS, compared with the trunk segments, in the hemimetabolous insect Oncopeltus fasciatus. Gene function was tested by manipulating expression through RNA interference against components of the two pathways. We show that there are fundamental differences in the expression patterns of the segment polarity genes, in the timing of their expression and in the interactions among them in the process of pre-gnathal segment generation, relative to all other segments. We argue that given these differences, the PGS should not be considered serially homologous to trunk segments. This realization raises important questions about the differing evolutionary ancestry of different regions of the arthropod head.

The sex determination gene doublesex (dsx) encodes a transcription factor with two domains, oligomerization domain 1 (OD1) and OD2, and is present throughout insects. Sex-specific Dsx splicing isoforms regulate the transcription of target genes and trigger sex differentiation in all Holometabola examined to date. However, in some hemimetabolous insects, dsx is not spliced sexually and its sequence is less conserved. Here, to elucidate evolutionary changes in dsx in domain organisation and regulation in termites, we searched genome and/or transcriptome databases for the dsx OD1 and OD2 in seven termite species and their sister group (Cryptocercus woodroaches). Molecular phylogenetic and synteny analyses identified OD1 sequences of termites and C. punctulatus that clustered with dsx of Holometabola and regarded them as dsx orthologues. The Cryptocercus dsx orthologue containing OD2 was spliced sexually, as previously shown in other insects. However, OD2 was not found in all termite dsx orthologues. These orthologues were encoded by a single exon in three termites for which genome information is available; they were not alternatively spliced but transcribed in a male-specific manner in two examined species. Evolution of dsx regulation from sex-specific splicing to male-specific transcription may have occurred at an early stage of social evolution in termites.

The transformation of paired fins into tetrapod limbs is one of the most intensively scrutinized events in animal evolution. Early anatomical and embryological datasets identified distinctive morphological regions within the appendage and posed hypotheses about how the loss, gain, and transformation of these regions could explain the observed patterns of both extant and fossil appendage diversity. These hypotheses have been put to the test by our growing understanding of patterning mechanisms that regulate formation of the appendage axes, comparisons of gene expression data from an array of phylogenetically informative taxa, and increasingly sophisticated and elegant experiments leveraging the latest molecular approaches. Together, these data demonstrate the remarkable conservation of developmental mechanisms, even across phylogenetically and morphologically disparate taxa, as well as raising new questions about the way we view homology, evolutionary novelty, and the often non-linear connection between morphology and gene expression. In this review, we present historical hypotheses regarding paired fin evolution and limb origins, summarize key aspects of central appendage patterning mechanisms in model and non-model species, address how modern comparative developmental data interface with our understanding of appendage anatomy, and highlight new approaches that promise to provide new insight into these well-traveled questions.

The social amoeba Dictyostelium discoideum commonly forms chimeric fruiting bodies by aggregation of different strains. Genetic variants that produce a higher proportion of spores are predicted to undercut multicellular organization unless cooperators assort positively. Cell adhesion is considered a primary factor driving such assortment, but evolution of adhesion has not been experimentally connected to changes in social performance. In this study we modified by experimental evolution the properties of individual cells, selecting for higher and lower adhesion to substrate. We then quantified the effects of these changes on cell-cell adhesion, development, and social behaviour. Unlike strains selected based on relative reproductive success in the social stage, we found that in binary chimeras both derived strains produce a smaller fraction of spores than the ancestor. Thus, evolution appears to have produced social cooperators. Examination of development revealed that this is however achieved via two opposed paths. Cells selected to be more adhesive to the substrate disproportionately contribute to the structural stability of fruiting bodies, as one would expect for cooperators. On the contrary, less adhesive cells behave as cheaters that undermine their own success more than that of the ancestor. These differences are reflected by a metric for social success that generalizes the classically used variation in frequency during the multicellular phase. Our work shows that cell mechanical interactions can constrain evolution of development and assortment in chimeras, and calls for integrating cell-level processes in conceptualizing the emergence of multicellular organization. Author summary The multicellular life cycle of Dictyostelium discoideum is as amazing as puzzling. Genetically different cells commonly co-aggregate, so that collective functions – that repose on cooperation among cells – are constantly threatened by the presence of exploitative variants, commonly called ‘cheaters’. Most previous studies focused on how reproductive success in the multicellular phase of the life cycle can be compensated by positive assortment of cooperating cells, but recent models have stressed the impact of non-aggregated cells on the evolutionary dynamics. We use experimental evolution to explore how selection acting on single-cell adhesion impacts social behaviour. Cell adhesion is held as a fundamental mechanism for cells to direct their cooperative behaviour towards kin, but the way it interplays with social behaviour during evolution has been so far only theoretically explored. Higher levels of cooperation appear to evolve as a result of both increased and decreased cell-substrate adhesion. However, such phenotypes are associated to opposite developmental dynamics in chimeric aggregates. Differences in social behaviour are captured if spore production of isolated strains is also considered, suggesting that in both cases cooperative behaviour is associated to stronger adhesion.

The transformation of the bird skull from an ancestral akinetic, heavy, and toothed dinosaurian morphology to a highly derived, lightweight, edentulous, and kinetic skull is an innovation as significant as powered flight and feathers. Our understanding of evolutionary assembly of the modern form and function of avian cranium has been impeded by the rarity of early bird fossils with well-preserved skulls. Here, we describe a new enantiornithine bird from the Early Cretaceous of China that preserves a nearly complete skull including the palatal elements, exposing the components of cranial kinesis. Our three-dimensional reconstruction of the entire enantiornithine skull demonstrates that this bird has an akinetic skull indicated by the unexpected retention of the plesiomorphic dinosaurian palate and diapsid temporal configurations, capped with a derived avialan rostrum and cranial roof, highlighting the highly modular and mosaic evolution of the avialan skull., In addition to major innovations in their locomotor system, early birds evolved highly derived skulls. Here, Wang et al. three dimensionally reconstruct the skull of a new enantiornithine bird from the Early Cretaceous that illustrates the early avialan transitions in skull morphology and function.

Understanding the genetic architecture of complex trait adaptation in natural populations requires the continued development of tractable models that explicitly confront organismal and environmental complexity. A decade of high-throughput sequencing-based investigations into the genomic basis of migration points to an integrative framework that incorporates quantitative genetics, evolutionary developmental biology, phenotypic plasticity, and epigenetics to explain migration evolution. In this perspective, I argue that the transcontinental migration of the monarch butterfly (Danaus plexippus) can serve as a compelling system to study the mechanism of evolutionary lability of a complex trait. Monarchs show significant phenotypic and genotypic diversity across their global range, with phenotypic switching that allows for explicit study of evolutionary lability. A developmental approach for elucidating how migratory traits are generated and functionally integrated will be important for understanding the evolution of monarch migration traits. I propose a plasticity threshold model to describe migration lability, and I describe novel functional techniques that will help resolve open questions and model assumptions. I conclude by considering the relationships between adaptive genetic architecture, anthropogenic climate change, and conservation management practice and the timeliness of the monarch migration model to illuminate these connections given the rapid decline of the North American migration.