An official website of the United States government
Abstract BackgroundAnimal behavior is largely driven by the information that animals are able to extract and process from their environment. However, the function and organization of sensory systems often change throughout ontogeny, particularly in animals that undergo indirect development. As an initial step toward investigating these ontogenetic changes at the molecular level, we characterized the sensory gene repertoire and examined the expression profiles of genes linked to vision and chemosensation in two life stages of an insect that goes through metamorphosis, the butterflyBicyclus anynana. ResultsUsing RNA-seq, we compared gene expression in the heads of late fifth instar larvae and newly eclosed adults that were reared under identical conditions. Over 50 % of all expressed genes were differentially expressed between the two developmental stages, with 4,036 genes upregulated in larval heads and 4,348 genes upregulated in adult heads. In larvae, upregulated vision-related genes were biased toward those involved with eye development, while phototransduction genes dominated the vision genes that were upregulated in adults. Moreover, the majority of the chemosensory genes we identified in theB. anynanagenome were differentially expressed between larvae and adults, several of which share homology with genes linked to pheromone detection, host plant recognition, and foraging in other species of Lepidoptera. ConclusionsThese results revealed promising candidates for furthering our understanding of sensory processing and behavior in the disparate developmental stages of butterflies and other animals that undergo metamorphosis.
more »
« less
Comparisons of cell proliferation and cell death from tornaria larva to juvenile worm in the hemichordate Schizocardium californicum
Abstract BackgroundThere are a wide range of developmental strategies in animal phyla, but most insights into adult body plan formation come from direct-developing species. For indirect-developing species, there are distinct larval and adult body plans that are linked together by metamorphosis. Some outstanding questions in the development of indirect-developing organisms include the extent to which larval tissue undergoes cell death during the process of metamorphosis and when and where the tissue that will give rise to the adult originates. How do the processes of cell division and cell death redesign the body plans of indirect developers? In this study, we present patterns of cell proliferation and cell death during larval body plan development, metamorphosis, and adult body plan formation, in the hemichordateSchizocardium californium(Cameron and Perez in Zootaxa 3569:79–88, 2012) to answer these questions. ResultsWe identified distinct patterns of cell proliferation between larval and adult body plan formation ofS. californicum. We found that some adult tissues proliferate during the late larval phase prior to the start of overt metamorphosis. In addition, using an irradiation and transcriptomic approach, we describe a genetic signature of proliferative cells that is shared across the life history states, as well as markers that are unique to larval or juvenile states. Finally, we observed that cell death is minimal in larval stages but begins with the onset of metamorphosis. ConclusionsCell proliferation during the development ofS. californicumhas distinct patterns in the formation of larval and adult body plans. However, cell death is very limited in larvae and begins during the onset of metamorphosis and into early juvenile development in specific domains. The populations of cells that proliferated and gave rise to the larvae and juveniles have a genetic signature that suggested a heterogeneous pool of proliferative progenitors, rather than a set-aside population of pluripotent cells. Taken together, we propose that the gradual morphological transformation ofS. californicumis mirrored at the cellular level and may be more representative of the development strategies that characterize metamorphosis in many metazoan animals.
more »
« less
- Award ID(s):
- 1656628
- PAR ID:
- 10367940
- Publisher / Repository:
- Springer Science + Business Media
- Date Published:
- Journal Name:
- EvoDevo
- Volume:
- 13
- Issue:
- 1
- ISSN:
- 2041-9139
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Amphibians undergo a variety of post‐embryonic transitions (PETr) that are partly governed by thyroid hormone (TH). Transformation into a terrestrial form follows an aquatic larval stage (biphasic) or precedes hatching (direct development). Some salamanders maintain larval characteristics and an aquatic lifestyle into adulthood (paedomorphosis), which obscures the conclusion of their larval period. Paedomorphic axolotls exhibit elevated TH during early development that is concomitant with transcriptional reprogramming and limb emergence. A recent perspective suggested this cryptic TH‐based PETr is uncoupled from metamorphosis in paedomorphs and concludes the larval period. This led to their question:“Are paedomorphs actual larvae?”. To clarify, paedomorphs are only considered larval in form, even though they possess some actual larval characteristics. However, we strongly agree that events during larval development inform amphibian life cycle evolution. We build upon their perspective by considering the evolution of limb emergence and metamorphosis. Limbless hatchling larval salamanders are generally associated with ponds, while limbed larvae are common to streams and preceded the evolution of direct development. Permian amphibians had limbed larvae, so their PETr was likely uncoupled from metamorphosis, equivalent to most extant biphasic and paedomorphic salamanders. Coupling of these events was likely derived in frogs and direct developing salamanders.more » « less
-
Dubilier, Nicole (Ed.)ABSTRACT Diverse marine animals undergo a metamorphic larval-to-juvenile transition in response to surface-bound bacteria. Although this host-microbe interaction is critical to establishing and maintaining marine animal populations, the functional activity of bacterial products and how they activate the host’s metamorphosis program has not yet been defined for any animal. The marine bacteriumPseudoalteromonas luteoviolaceastimulates the metamorphosis of a tubeworm calledHydroides elegansby producing a molecular syringe called metamorphosis-associated contractile structures (MACs). MACs stimulate metamorphosis by injecting a protein effector termed metamorphosis-inducing factor 1 (Mif1) into tubeworm larvae. Here, we show that MACs bind to tubeworm cilia and form visible pores on the cilia membrane surface, which are smaller and less numerous in the absence of Mif1.In vitro, Mif1 associates with eukaryotic lipid membranes and possesses phospholipase activity. MACs can also deliver Mif1 to human cell lines and cause parallel phenotypes, including cell surface binding, membrane disruption, calcium flux, and mitogen-activated protein kinase activation. Finally, MACs can also stimulate metamorphosis by delivering two unrelated membrane-disrupting proteins, MLKL and RegIIIɑ. Our findings demonstrate that membrane disruption by MACs and Mif1 is necessary forHydroidesmetamorphosis, connecting the activity of a bacterial protein effector to the developmental transition of a marine animal. IMPORTANCEThis research describes a mechanism wherein a bacterium prompts the metamorphic development of an animal from larva to juvenile form by injecting a protein that disrupts membranes in the larval cilia. Specifically, results show that a bacterial contractile injection system and the protein effector it injects form pores in larval cilia, influencing critical signaling pathways like mitogen-activated protein kinase and calcium flux, ultimately driving animal metamorphosis. This discovery sheds light on how a bacterial protein effector exerts its activity through membrane disruption, a phenomenon observed in various bacterial toxins affecting cellular functions, and elicits a developmental response. This work reveals a potential strategy used by marine organisms to respond to microbial cues, which could inform efforts in coral reef restoration and biofouling prevention. The study’s insights into metamorphosis-associated contractile structures’ delivery of protein effectors to specific anatomical locations highlight prospects for future biomedical and environmental applications.more » « less
-
Fernandez-Valverde, Selene L (Ed.)The papillae of tunicate larvae contribute sensory, adhesive, and metamorphosis-regulating functions that are crucial for the biphasic lifestyle of these marine, non-vertebrate chordates. We have identified additional molecular markers for at least 5 distinct cell types in the papillae of the model tunicateCiona, allowing us to further study the development of these organs. Using tissue-specific CRISPR/Cas9-mediated mutagenesis and other molecular perturbations, we reveal the roles of key transcription factors and signaling pathways that are important for patterning the papilla territory into a highly organized array of different cell types and shapes. We further test the contributions of different transcription factors and cell types to the production of the adhesive glue that allows for larval attachment during settlement, and to the processes of tail retraction and body rotation during metamorphosis. With this study, we continue working towards connecting gene regulation to cellular functions that control the developmental transition between the motile larva and sessile adult ofCiona.more » « less
-
ABSTRACT Tunicates are the sister group to the vertebrates, yet most species have a life cycle split between swimming larva and sedentary adult phases. During metamorphosis, larval neurons are replaced by adult-specific ones. The regulatory mechanisms underlying this replacement remain largely unknown. Using tissue-specific CRISPR/Cas9-mediated mutagenesis in the tunicate Ciona, we show that orthologs of conserved hindbrain and branchiomeric neuron regulatory factors Pax2/5/8 and Phox2 are required to specify the ‘neck’, a cellular compartment set aside in the larva to give rise to cranial motor neuron-like neurons post-metamorphosis. Using bulk and single-cell RNA-sequencing analyses, we characterize the transcriptome of the neck downstream of Pax2/5/8. We present evidence that neck-derived adult ciliomotor neurons begin to differentiate in the larva and persist through metamorphosis, contrary to the assumption that the adult nervous system is formed after settlement and the death of larval neurons during metamorphosis. Finally, we show that FGF signaling during the larval phase alters the patterning of the neck and its derivatives. Suppression of FGF converts neck cells into larval neurons that fail to survive metamorphosis, whereas prolonged FGF signaling promotes an adult neural stem cell-like fate.more » « less
