Animals such as insects, crabs and spiders belong to one of the most species-rich animal groups, called the arthropods. These animals have exoskeletons, which are hard, external coverings that support their bodies. Arthropods shed their exoskeletons as they grow, a process called ecdysis or moulting, and this behaviour is controlled by a set of hormones and small protein-like molecules called neuropeptides that allow communication between neurons.

Other animals, such as roundworms, also moult; and together with arthropods they are classified into a group called the Ecdysozoa. Since moulting is a common behaviour in ecdysozoans, it was previously assumed that its signalling components had evolved in the common ancestor of roundworms and arthropods, although differences in the moulting machinery between both groups exist.

Here, De Oliveira et al. investigate the evolutionary origins of the arthropod moulting machinery and find that some of the hormones and neuropeptides involved appeared long before the arthropods themselves.

Database searches showed that important hormones and neuropeptides involved in arthropod moulting can be found in diverse animal groups, such as jellyfish, molluscs and starfish, confirming that these molecules evolved before the last common ancestor of roundworms and arthropods. These animals must therefore use the hormones and neuropeptides in many processes unrelated to moulting. De Oliveira et al. also found that roundworms have lost most of these molecules, and that moulting in these animals must be driven by a different complement of hormones and neuropeptides.

These results invite research into the role of moulting hormones and neuropeptides in animals outside the Ecdysozoa. They also show that signalling pathways and the processes they regulate are highly adaptable: two animals can use the same hormone in entirely different processes, but conversely, the same behaviour may be regulated by different molecules depending on the animal. This means that the evolution of a process and the evolution of its regulation can be decoupled, a finding that has important implications for the study of signalling pathways and their evolution.

Ecdysis or moulting, which describes the process of shedding the outer integument, the cuticle, is a defining feature of Ecdysozoa (arthropods, tardigrades, onychophorans, nematodes and related phyla) (Aguinaldo et al., 1997; Schmidt-Rhaesa et al., 1998; de Rosa et al., 1999; Dunn et al., 2008; Telford et al., 2008). Despite superficial similarities of the ‘moulting behaviour’ within Ecdysozoa, the neuroendocrine components underlying this process remain elusive for the majority of the ecdysozoans outside of Arthropoda. This includes well-established model organisms such as the nematode Caenorhabditis elegans, for which the gene regulatory network responsible for ecdysis remains to be fully resolved (Frand et al., 2005; reviewed by Page et al., 2014 and Lažetić and Fay, 2017).

In arthropods, ecdysis can be divided into three distinct stages, pre-ecdysis, ecdysis and post-ecdysis. Each of these stages correlates with major behavioural, molecular and cellular changes and encompasses a series of specific muscular contractions controlled by a cascade of hormones and neuropeptides (Truman, 2005). Studies in insects have revealed that the major components of this peptidergic signalling pathway are ecdysis-triggering hormone (ETH), eclosion hormone (EH), crustacean cardioactive peptide (CCAP) and bursicon (Gammie and Truman, 1997a; Gammie and Truman, 1997b; Zitnan et al., 1999; Clark et al., 2004; Kim et al., 2006a; Kim et al., 2006b; Arakane et al., 2008; Lee et al., 2013). The process begins with the release of prothoracicotropic hormone (PTTH) from neurohemal organs. PTTH initiates a signalling cascade that results in the biosynthesis of ecdysteroids (i.e., steroid hormones synthesised from ingested cholesterol), including ecdysone (E) and 20-hydroxyecdysone (20E) (Figure 1). The decline of the ecdysone titre due to the ecdysone-inactivating enzyme cytochrome P450 protein Cyp18a1 (Guittard et al., 2011; reviewed by Rewitz et al., 2013) triggers the release of ETH that, in turn, causes the release of EH. These two hormones mutually enhance one another in a positive feedback loop to control and regulate pre-ecdysis behaviour (Figure 1). With the ensuing release of CCAP, caused by EH, pre-ecdysis ceases and the ecdysis motor program is initiated. Finally, bursicon responds to the increasing levels of CCAP and initiates post-ecdysis behaviour and cuticle tanning (Figure 1).

Figure 1

Download asset Open asset

Comparative biochemical, genomic and transcriptomic analyses revealed that ecdysteroids and the required genes responsible for their biosynthesis are present outside of Ecdysozoa, showing that some key molecular players of moulting predate the origin of Ecdysozoa (Mendis et al., 1984; Nolte et al., 1986; Garcia et al., 1989; Barker et al., 1990; Schumann et al., 2018). Such integrative and comparative analyses have so far not been conducted on the major components of the peptidergic signalling system underlying moulting. To fill this gap in knowledge, we explored the distribution of PTTH, ETH, EH, CCAP and bursicon ligand-receptor pairs across Metazoa.

PTTH is a neurohormone with a proposed origin at the base of Arthropoda that is believed to have evolved from the duplication of the ancient and widely distributed bilaterian signalling molecule-encoding gene trunk (Rewitz et al., 2009; Jékely, 2013). By screening 39 metazoan genomes and 57 transcriptomes (Supplementary file 1), we found that the PTTH peptide is present in Drosophila and Tribolium but absent in the house spider Parasteatoda tepidariorum and the crustacean Parhyale hawaiensis, suggesting that PTTH is an insect innovation (Figure 2A,B, Figure 2—figure supplement 1A, Figure 2—source data 1). The ablation of PTTH-producing neurons in Drosophila generates an imbalance in ecdysone biosynthesis, causing developmental delay, prolonged duration of feeding and larger individuals with reduced fecundity (McBrayer et al., 2007). These findings indicate that PTTH, at least in Drosophila, regulates developmental timing and body size, but is not essential for moulting. Trunk, the paralog of ptth, has previously been identified in arthropods, annelids, mollusks and the cephalochordate Branchiostoma floridae (Jékely, 2013). Our study expands the phyletic distribution of trunk to onychophorans, tardigrades, gastrotrichs, brachiopods, nemerteans, ectoprocts, phoronids and hemichordates (Figure 2A,B, Figure 2—figure supplement 1A, Figure 2—source data 1). Although we did not find a trunk ortholog in the genome of the sea anemone Nematostella vectensis, our similarity searches against the NCBI protein database led to the identification of this protein in other anthozoans, namely Stylophora pistillata (PFX31008.1) and Orbicella faveolata (XP_020630744.1 and XP_020630745.1). More importantly, our multi-species screen also recovered a trunk-like peptide in the ctenophore Mnemiopsis leidyi with high similarity (p-value < 1e-05) to lophotrochozoan, deuterostome and ecdysozoan trunk sequences (Figure 2—figure supplement 1A; Figure 3A,B). By similarity-based clustering we were able to demonstrate homology of the ctenophore trunk-like peptide with the insect trunk paralog, ptth (Figure 3A, Figure 3—source data 1; see also Rewitz et al., 2009; Jékely, 2013). This extends the phyletic distribution of trunk to the ctenophores (see, e.g., Halanych, 2004; Dunn et al., 2008; Moroz et al., 2014; Jékely et al., 2015; Pisani et al., 2015 for discussion).

Figure 2 with 6 supplements see all

Download asset Open asset

Figure 2—source data 1

PTTH/trunk/torso proteins and tree associated files.

Compressed. zip file containing the 3D-cluster map of the PTTH and trunk ligands in. rtf format, the torso receptor proteins in fasta format, the multiple sequence alignment of the receptor (trimmed and untrimmed), and the tree files genereted by RAxML, PhyML and mrbayes programs. The 3D cluster peptide map can be visualised and manipulated using the program clans (Frickey and Lupas, 2004; see ftp://ftp.tuebingen.mpg.de/pub/protevo/CLANS/). The multiple sequence alignment files can be viewed with aliview (Larsson, 2014). The phylogenetic tree files can be viewed using Figtree (http://tree.bio.ed.ac.uk/software/figtree/) or TreeGraph2 (Stöver and Müller, 2010).

https://doi.org/10.7554/eLife.46113.011

Download elife-46113-fig2-data1-v2.zip

Figure 2—source data 2

ETH/ETH-receptor proteins and tree associated files.

Compressed. zip file containing the 3D-cluster map of the ETH ligands in. rtf format, the ETH receptor proteins in fasta format, the multiple sequence alignment of the receptor (trimmed and untrimmed), and the tree files genereted by RAxML, PhyML and mrbayes programs. The 3D cluster peptide map can be visualised and manipulated using the program clans (Frickey and Lupas, 2004a; see ftp://ftp.tuebingen.mpg.de/pub/protevo/CLANS/). The multiple sequence alignment files can be viewed with aliview (Larsson, 2014a). The phylogenetic tree files can be viewed using Figtree (http://tree.bio.ed.ac.uk/software/figtree/) or TreeGraph2 (Stöver and Müller, 2010a).

https://doi.org/10.7554/eLife.46113.012

Download elife-46113-fig2-data2-v2.zip

Figure 2—source data 3

EH/EH-receptor proteins and tree associated files.

Compressed. zip file containing the 3D-cluster map of the EH ligands in. rtf format, the EH receptor proteins in fasta format, the multiple sequence alignment of the receptor (trimmed and untrimmed), and the tree files genereted by RAxML, PhyML and mrbayes programs. The 3D cluster peptide map can be visualised and manipulated using the program clans (see ftp://ftp.tuebingen.mpg.de/pub/protevo/CLANS/). The multiple sequence alignment files can be viewed with aliview (Larsson, 2014a). The phylogenetic tree files can be viewed using Figtree (http://tree.bio.ed.ac.uk/software/figtree/) or TreeGraph2 (Stöver and Müller, 2010a).

https://doi.org/10.7554/eLife.46113.013

Download elife-46113-fig2-data3-v2.zip

Figure 2 - source data 4

CCAP/CCAP-receptor proteins and associated tree files.

Compressed. zip file containing the 3D-cluster map of the CCAP ligands in. rtf format, the CCAP receptor proteins in fasta format, the multiple sequence alignment of the receptor (trimmed and untrimmed), and the tree files genereted by RAxML, PhyML and mrbayes programs. The 3D cluster peptide map can be visualised and manipulated using the program clans (Frickey and Lupas, 2004; see ftp://ftp.tuebingen.mpg.de/pub/protevo/CLANS/). The multiple sequence alignment files can be viewed with aliview (Larsson, 2014a). The phylogenetic tree files can be viewed using Figtree (http://tree.bio.ed.ac.uk/software/figtree/) or TreeGraph2 (Stöver and Müller, 2010a).

https://doi.org/10.7554/eLife.46113.014

Download elife-46113-fig4-v2.zip

Figure 2—source data 5

Bursicon/rickets protein and tree associated files.

Compressed. zip file containing the 3D-cluster map of the bursicon ligands in. rtf format, the rickets receptor proteins in fasta format, the multiple sequence alignment of the receptor (trimmed and untrimmed), and the tree files genereted by RAxML, PhyML and mrbayes programs. The 3D cluster peptide map can be visualised and manipulated using the program clans (Frickey and Lupas, 2004a; see ftp://ftp.tuebingen.mpg.de/pub/protevo/CLANS/). The multiple sequence alignment files can be viewed with aliview (Larsson, 2014). The phylogenetic tree files can be viewed using Figtree (http://tree.bio.ed.ac.uk/software/figtree/) or TreeGraph2 (Stöver and Müller, 2010).

https://doi.org/10.7554/eLife.46113.015

Download elife-46113-fig2-data5-v2.zip

Figure 3

Download asset Open asset

Figure 3—source data 1

Ctenophore trunk cluster peptide map.

Compressed. zip file containing the 3D-cluster map of ptth, trunk and noggin orthologs in. rtf format. he 3D cluster peptide map can be visualised and manipulated using the program clans (Frickey and Lupas, 2004a; see ftp://ftp.tuebingen.mpg.de/pub/protevo/CLANS/).

https://doi.org/10.7554/eLife.46113.017

Download elife-46113-fig3-data1-v2.zip

PTTH and trunk share a common receptor, the tyrosine kinase torso (Rewitz et al., 2009). Similar to its ligands, torso (Rewitz et al., 2009) proved also to be much more ancient than commonly assumed. We identified torso sequences in deuterostomes, lophotrochozoans, cnidarians and ecdysozoans (Figure 2—figure supplement 2), indicating that the trunk-torso neuropeptide signalling pathway dates back at least as far as the last common ancestor of Cnidaria, Ctenophora and Bilateria and is thus not restricted to Bilateria as suggested previously (e.g., Jékely, 2013) (Figures 2A,B and 4A).

Figure 4

Download asset Open asset

In insects, the first hormone released in response to decreasing ecdysone levels is usually ETH (Zitnan et al., 1996; Zitnan et al., 1999) although in the lepidopteran Manduca sexta the neuropeptide corozanin acts as the trigger for the release of ETH from the epitracheal glands (Kim et al., 2004). Knockdown of the eth gene in Drosophila (Park et al., 2002) and of eth and its receptors in Tribolium and Schistocerca (Arakane et al., 2008; Lenaerts et al., 2017) lead to lethality at the expected onset of ecdysis, demonstrating the essential role of the ETH peptidergic signalling system in moulting (Park et al., 2002; Arakane et al., 2008; Lenaerts et al., 2017; Shi et al., 2017). Our screening and phylogenetic analyses confirmed the presence of ETH and its receptor in tardigrades and arthropods, thus corroborating previous studies (Figure 2B, Figure 2—figure supplement 3, Figure 2—source data 2) (Zitnan et al., 1996; Zitnan et al., 1999; Park et al., 2002; Arakane et al., 2008; Veenstra et al., 2012; Lenaerts et al., 2017; Koziol, 2018; Zhu et al., 2019). For Arthropoda, the ETH ligand was only found in insects (Drosophila and Tribolium), but was lacking in the crustacean Parhyale hawaiensis and the arachnid Parasteatoda tepidariorum. However, studies on the two mites Panonychus citri and Tetranychus urticae as well as several decapods have shown the presence of the ETH ligand in chelicerates and crustaceans (in which the homology was reconfirmed by our clustering analysis) (Veenstra et al., 2012; Veenstra, 2016; Zhu et al., 2019). Surprisingly, we did not find the entire ETH signalling pathway in the two onychophoran genomes analysed herein (Figures 2B and 4B, Figure 2—figure supplement 3, Figure 2—source data 2). Due to the fragmented nature of the onychophoran genomes a final statement whether this signalling system was indeed lost in this lineage cannot be made at present.

No eth ortholog was identified outside the panarthropods, including the nematode C. elegans, suggesting that this gene originated in the last common ancestor of Panarthropoda (Figure 2B). Our findings on the distribution of the ETH receptor are in agreement with the results of previous studies and demonstrate the presence of this receptor in arthropods (insects, crustaceans and arachnids), mollusks, nemerteans, brachiopods, echinoderms, cephalochordates (in which we found a substantial expansion of eth-receptor homologs in the genomes of Branchiostoma floridae and B. belcheri), vertebrates and acoels (Park et al., 2003; Roller et al., 2010; Veenstra et al., 2012; Mirabeau and Joly, 2013; Lenaerts et al., 2017; Thiel et al., 2018; Zhu et al., 2019) (Figures 2B and 4A, Figure 2—figure supplement 3, Figure 2—source data 2). This provides evidence for the presence of individual components of the ETH signalling system already at the base of Bilateria (Figures 2A and 4A).

Eclosion hormone (EH) was first identified as a blood-borne factor (Truman and Riddiford, 1970) in three lepidopteran species, Hyalophora cecropia, Antheraea polyphemus and Antheraea pernyi. A positive feedback loop between EH and ETH was found in Manduca and suggested in Tribolium (Ewer et al., 1997; Arakane et al., 2008), whereas in Drosophila, EH has been described either acting downstream of ETH (Kim et al., 2006a; Kim et al., 2006b) or in a positive endocrine feedback loop with ETH (Krüger et al., 2015). Despite EH being a key regulator of ecdysis in insects, eh knockout in Drosophila melanogaster did not abolish ecdysis, but instead produced flies with discrete behavioural deficits such as slow and uncoordinated eclosion. This shows that EH is involved, but does not play an essential role, in moulting in these insects (McNabb et al., 1997). This result, however, has been contested in a more recent study using eh null mutants in Drosophila (Krüger et al., 2015), showing that the lack of eh function is lethal during larval fruit fly ecdysis.

Traditionally considered to be confined to arthropods, recent studies showed the presence of EH and its receptor, a guanylyl cyclase, in echinoderms and tardigrades (Zandawala et al., 2017; Koziol, 2018). Our study corroborates these findings but considerably expands the presence of the EH ligand to cnidarians, acoels, hemichordates, lophotrochozoans (mollusks, annelids, nemerteans and phoronids) and onychophorans (Figure 2B, Figure 2—figure supplement 1B, Figure 2—source data 3). All EH ligand orthologs harbour the six cysteine conserved residues (Zitnan et al., 2007) except for Cnidaria, in which only five are present. The identification of the EH receptor in ambulacrarians, mollusks, annelids, nemerteans and phoronids suggests co-evolution of this ligand-receptor pair throughout Metazoa (Figure 2B, Figure 2—figure supplement 4, Figure 2—source data 3). Although the eh-receptor gene was not found in Cnidaria, Xenacoelomorpha and Onychophora, its distribution includes the Brachiopoda, Ectoprocta and Cephalochordata lineages. Consequently, our findings shift the ancestry of this peptidergic pathway back to the cnidarian-bilaterian split (Figures 2A and 4A).

First isolated from the shore crab Carcinus maenas, crustacean cardioactive peptide (CCAP) is a highly conserved amidated neuropeptide that increases heart rate in crustaceans and insects (Stangier et al., 1987; Cheung et al., 1992; Lehman et al., 1993; Suggs et al., 2016). CCAP has multiple functions in addition to its cardioacceleratory activity, such as accelerating the frequency and amplitude of oviduct contractions in the locust Locusta migratoria (Donini et al., 2001) and regulating the release of digestive enzymes in the cockroach Periplaneta americana (Sakai et al., 2006). CCAP is important for ecdysis in crustaceans and insects where it initiates the stereotyped sequence of behaviours that mark the end of the pre-ecdysis stage (Gammie and Truman, 1997a; Gammie and Truman, 1997b; Phlippen et al., 2000; Arakane et al., 2008; Lee et al., 2013). However, transgenic Drosophila larvae lacking CCAP neurons moult normally and only exhibit a prolonged pre-ecdysis behaviour (Clark et al., 2004).

Only three studies focusing on the CCAP signalling pathway components are available outside of Arthropoda. In the snail Lymnaea stagnalis (Vehovszky et al., 2005), immunostaining revealed a dense network of CCAP-positive fibres that likely function to regulate parts of the feeding behaviour. In the oyster Saccostrea glomerata (In et al., 2016) and in the cuttlefish Sepia officinalis (Endress et al., 2018), in vivo bioassays using synthesised neuropeptides and immunohistochemistry suggested that the CCAP signalling pathway is involved in reproduction (e.g., spawning, oocyte transport, egg-laying). Additionally, Sepia CCAP has been shown to increase the tonus of the vena cava, demonstrating its role in the regulation of hemolymph circulation (Endress et al., 2018). These results indicate that in both, mollusks and arthropods, CCAP functions in feeding, reproduction and regulation of hemolymph circulation, suggesting that these may have been its ancestral roles. In arthropods, co-option of CCAP into the ecdysis pathway expanded this set of functions to include moulting.

The CCAP receptor is a G protein-coupled receptor (GPCR) that was first described from the Drosophila genome and subsequently identified in many other insects (Cazzamali et al., 2003; Arakane et al., 2008; Vogel et al., 2013). We confirm here the presence of a CCAP ligand in mollusks, annelids, arthropods and tardigrades, as stated earlier (Veenstra, 2010; Jékely, 2013; Mirabeau and Joly, 2013; Conzelmann et al., 2013; Stewart et al., 2014; Ahn et al., 2017; Zhang et al., 2018; Koziol, 2018), and extend the distribution of the CCAP ligand to three additional lophotrochozoan phyla (Nemertea, Platyhelminthes and Rotifera) as well as to the remaining panarthropod phylum Onychophora (Figures 2B and 4B, Figure 2—figure supplement 1C, Figure 2—source data 4). Interestingly, the CCAP ligand is absent from all investigated deuterostome genomes analysed (Figure 2—figure supplement 1C, Figure 2B, Figure 2—source data 4). The ccap-receptor ortholog was found in acoels, lophotrochozoans and panarthropods except Onychophora (Figure 2—figure supplement 5). Surprisingly, we found the receptor also in all deuterostome phyla (Echinodermata, Hemichordata, Vertebrata, Cephalochordata) except Tunicata (Figure 2—figure supplement 5, Figure 2—source data 4). These results reinforce the suggested origin of the ligand-receptor pair at the base of Bilateria and points towards a possible loss of the CCAP ligand in the Deuterostomia lineage (Figures 2B and 4A, Figure 2—figure supplement 5, Figure 2—source data 4).

Bursicon was identified as a neurohormone responsible for cuticle sclerotization and melanisation (tanning) during post-ecdysis (Cottrell, 1962a; Cottrell, 1962b; Fraenkel and Hsiao, 1965). Recent studies have shown that bursicon also has a mild effect on the regulation of pre-ecdysis and is important for the proper execution of post-ecdysis in Manduca, Drosophila and Tribolium as well as for the development of wings and other integumentary structures (Baker and Truman, 2002; Dewey et al., 2004; Arakane et al., 2008; Bai and Palli, 2010). Together with the ecdydis-triggering hormone signalling system, bursicon is an indispensable component of the moulting behaviour in insects (Arakane et al., 2008). Previous studies show that bursicon is present outside Ecdysozoa, for example in the anthozoan Nematostella vectensis, the echinoderm Strongylocentrotus purpuratus as well as in annelids and mollusks (Jékely, 2013; Conzelmann et al., 2013; Stewart et al., 2014; Ahn et al., 2017; Zhang et al., 2018). Our work confirms the presence of the complete bursicon signalling system in all arthropod genomes analysed here and extends its distribution (receptor and/or ligand) to the hemichordate, nemertean, phoronid, rotifer and onychophoran phyla (Figure 2B, Figure 2—figure supplement 1D, Figure 2—source data 5). Interestingly, bursicon and its receptor rickets are absent in tardigrades, suggesting the loss of the bursicon peptidergic signalling in this lineage (Figures 2B and 4B, Figure 2—figure supplement 6, Figure 2—source data 5). The latter findings are corroborated by independent proneuropeptide and peptide prohormone surveys in the tardigrade genomic and EST data that also failed to detect this ligand-receptor pair in different tardigrade species (Christie et al., 2011; Koziol, 2018). We did not identify the receptor in any deuterostome or non-arthropod ecdysozoan lineage (Figure 2B).

The PTTH, ETH, EH, CCAP and bursicon peptide signalling systems are lacking in the nematode Caenorhabditis elegans (cf. our study and, e.g., Page et al., 2014; Lažetić and Fay, 2017; Figure 2B, Figure 2—figure supplement 1). Additionally, other key moulting components, such as the ecdysteroid ecdysone (E), 20-hydroxyecdysone (20E), and various halloween gene products have also been reported absent from the C. elegans genome (Frand et al., 2005; Schumann et al., 2018). An extensive body of research on moulting in C. elegans suggests an entirely different molecular machinery controlling this behaviour in this free-living nematode (Russel et al., 2011; for review Lažetić and Fay, 2017).

Interestingly, however, E and 20E were identified in parasitic nematodes (Cleator et al., 1987; Shea et al., 2004) and, outside Ecdysozoa, in the platyhelminth Monieza expansa, the gastropod mollusks Lymnaea stagnalis and Helix pomatia as well as in the hirudinean annelid Hirudo medicinalis (Mendis et al., 1984; Nolte et al., 1986; Garcia et al., 1989; Barker et al., 1990).

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have also been provided. The molecular databases analysed in this study are publicly available and novel annotated sequences are included in the Source data 1-5. The list of investigated species and their respective links to a direct download are presented in the Supplementary File 1 (Table S1). The 3D proneuropeptide/prohormone maps as well as all the multiple sequence alignments and the phylogenetic trees generated in this study are available in the Source Data 1-5 enclosed in the original submission. The 3D maps in .rtf format can be visualised and inspected with the software clans (ftp://ftp.tuebingen.mpg.de/pub/protevo/CLANS/). The multiple sequence alignments used in the phylogenetic inferences can be graphically visualised using aliview (http://www.ormbunkar.se/aliview/#DOWNLOAD). The phylogenetic tree files can be viewed using an appropriate phylogetic tree viewer such as Figtree (http://tree.bio.ed.ac.uk/software/figtree/).

1. 1. Aguinaldo AM
   2. Turbeville JM
   3. Linford LS
   4. Rivera MC
   5. Garey JR
   6. Raff RA
   7. Lake JA

   (1997) Evidence for a clade of Nematodes, arthropods and other moulting animals

   Nature 387:489–493.

   https://doi.org/10.1038/387489a0

   • PubMed
   • Google Scholar
2. 1. Ahn SJ
   2. Martin R
   3. Rao S
   4. Choi MY

   (2017) Neuropeptides predicted from the transcriptome analysis of the gray garden slug Deroceras reticulatum

   Peptides 93:51–65.

   https://doi.org/10.1016/j.peptides.2017.05.005

   • PubMed
   • Google Scholar
3. 1. Arakane Y
   2. Li B
   3. Muthukrishnan S
   4. Beeman RW
   5. Kramer KJ
   6. Park Y

   (2008) Functional analysis of four neuropeptides, EH, ETH, CCAP and Bursicon, and their receptors in adult ecdysis behavior of the red flour beetle, Tribolium castaneum

   Mechanisms of Development 125:984–995.

   https://doi.org/10.1016/j.mod.2008.09.002

   • PubMed
   • Google Scholar
4. 1. Bai H
   2. Palli SR

   (2010) Functional characterization of bursicon receptor and genome-wide analysis for identification of genes affected by bursicon receptor RNAi

   Developmental Biology 344:248–258.

   https://doi.org/10.1016/j.ydbio.2010.05.003

   • PubMed
   • Google Scholar
5. 1. Baker JD
   2. Truman JW

   (2002)

   Mutations in the Drosophila glycoprotein hormone receptor, rickets, eliminate neuropeptide-induced tanning and selectively block a stereotyped behavioral program

   The Journal of Experimental Biology 205:2555–2565.

   • PubMed
   • Google Scholar
6. 1. Barker GC
   2. Chitwood DJ
   3. Rees HH

   (1990) Ecdysteroids in helminths and annelids

   Invertebrate Reproduction & Development 18:1–11.

   https://doi.org/10.1080/07924259.1990.9672124

   • Google Scholar
7. 1. Camacho C
   2. Coulouris G
   3. Avagyan V
   4. Ma N
   5. Papadopoulos J
   6. Bealer K
   7. Madden TL

   (2009) BLAST+: architecture and applications

   BMC Bioinformatics 10:421.

   https://doi.org/10.1186/1471-2105-10-421

   • PubMed
   • Google Scholar
8. 1. Cazzamali G
   2. Hauser F
   3. Kobberup S
   4. Williamson M
   5. Grimmelikhuijzen CJ

   (2003) Molecular identification of a Drosophila G protein-coupled receptor specific for crustacean cardioactive peptide

   Biochemical and Biophysical Research Communications 303:146–152.

   https://doi.org/10.1016/S0006-291X(03)00302-4

   • PubMed
   • Google Scholar
9. 1. Cheung CC
   2. Loi PK
   3. Sylwester AW
   4. Lee TD
   5. Tublitz NJ

   (1992) Primary structure of a cardioactive neuropeptide from the tobacco hawkmoth, Manduca sexta

   FEBS Letters 313:165–168.

   https://doi.org/10.1016/0014-5793(92)81436-P

   • PubMed
   • Google Scholar
10. 1. Christie AE
    2. Nolan DH
    3. Garcia ZA
    4. McCoole MD
    5. Harmon SM
    6. Congdon-Jones B
    7. Ohno P
    8. Hartline N
    9. Congdon CB
    10. Baer KN
    11. Lenz PH

    (2011) Bioinformatic prediction of arthropod/nematode-like peptides in non-arthropod, non-nematode members of the ecdysozoa

    General and Comparative Endocrinology 170:480–486.

    https://doi.org/10.1016/j.ygcen.2010.11.002

    • Google Scholar
11. 1. Clark AC
    2. del Campo ML
    3. Ewer J

    (2004) Neuroendocrine control of larval ecdysis behavior in Drosophila: complex regulation by partially redundant neuropeptides

    Journal of Neuroscience 24:4283–4292.

    https://doi.org/10.1523/JNEUROSCI.4938-03.2004

    • PubMed
    • Google Scholar
12. 1. Cleator M
    2. Delves CJ
    3. Howells RE
    4. Rees HH

    (1987) Identity and tissue localization of free and conjugated ecdysteroids in adults of Dirofilaria immitis and Ascaris suum

    Molecular and Biochemical Parasitology 25:93–105.

    https://doi.org/10.1016/0166-6851(87)90022-3

    • PubMed
    • Google Scholar
13. 1. Conzelmann M
    2. Williams EA
    3. Krug K
    4. Franz-Wachtel M
    5. Macek B
    6. Jékely G

    (2013) The neuropeptide complement of the marine annelid Platynereis dumerilii

    BMC Genomics 14:906.

    https://doi.org/10.1186/1471-2164-14-906

    • PubMed
    • Google Scholar
14. 1. Cottrell CB

    (1962a)

    The imaginal ecdysis of blowflies. The control of cuticuar hardening and darkening

    The Journal of Experimental Biology 39:395–412.

    • Google Scholar
15. 1. Cottrell CB

    (1962b)

    The imaginal ecdysis of blowflies. Detection of the blood-borne darkening factor and determination of some of its properties

    The Journal of Experimental Biology 39:413–430.

    • Google Scholar
16. 1. Criscuolo A
    2. Gribaldo S

    (2010) BMGE (Block mapping and gathering with entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments

    BMC Evolutionary Biology 10:210.

    https://doi.org/10.1186/1471-2148-10-210

    • PubMed
    • Google Scholar
17. 1. De Oliveira AL
    2. Calcino A
    3. Wanninger A

    (2019) Extensive conservation of the proneuropeptide and peptide prohormone complement in mollusks

    Scientific Reports 9:4846.

    https://doi.org/10.1038/s41598-019-40949-0

    • PubMed
    • Google Scholar
18. 1. de Rosa R
    2. Grenier JK
    3. Andreeva T
    4. Cook CE
    5. Adoutte A
    6. Akam M
    7. Carroll SB
    8. Balavoine G

    (1999) Hox genes in brachiopods and priapulids and protostome evolution

    Nature 399:772–776.

    https://doi.org/10.1038/21631

    • PubMed
    • Google Scholar
19. 1. Dewey EM
    2. McNabb SL
    3. Ewer J
    4. Kuo GR
    5. Takanishi CL
    6. Truman JW
    7. Honegger HW

    (2004) Identification of the gene encoding Bursicon, an insect neuropeptide responsible for cuticle sclerotization and wing spreading

    Current Biology 14:1208–1213.

    https://doi.org/10.1016/j.cub.2004.06.051

    • PubMed
    • Google Scholar
20. 1. Donini A
    2. Agricola H
    3. Lange AB

    (2001) Crustacean cardioactive peptide is a modulator of oviduct contractions in Locusta migratoria

    Journal of Insect Physiology 47:277–285.

    https://doi.org/10.1016/S0022-1910(00)00112-8

    • PubMed
    • Google Scholar
21. 1. Dunn CW
    2. Hejnol A
    3. Matus DQ
    4. Pang K
    5. Browne WE
    6. Smith SA
    7. Seaver E
    8. Rouse GW
    9. Obst M
    10. Edgecombe GD
    11. Sørensen MV
    12. Haddock SH
    13. Schmidt-Rhaesa A
    14. Okusu A
    15. Kristensen RM
    16. Wheeler WC
    17. Martindale MQ
    18. Giribet G

    (2008) Broad phylogenomic sampling improves resolution of the animal tree of life

    Nature 452:745–749.

    https://doi.org/10.1038/nature06614

    • PubMed
    • Google Scholar
22. 1. Dunn CW
    2. Giribet G
    3. Edgecombe GD
    4. Hejnol A

    (2014) Animal phylogeny and its evolutionary implications

    Annual Review of Ecology, Evolution, and Systematics 45:371–395.

    https://doi.org/10.1146/annurev-ecolsys-120213-091627

    • Google Scholar
23. 1. Endress M
    2. Zatylny-Gaudin C
    3. Corre E
    4. Le Corguillé G
    5. Benoist L
    6. Leprince J
    7. Lefranc B
    8. Bernay B
    9. Leduc A
    10. Rangama J
    11. Lafont AG
    12. Bondon A
    13. Henry J

    (2018) Crustacean cardioactive peptides: expression, localization, structure, and a possible involvement in regulation of egg-laying in the cuttlefish Sepia officinalis

    General and Comparative Endocrinology 260:67–79.

    https://doi.org/10.1016/j.ygcen.2017.12.009

    • PubMed
    • Google Scholar
24. 1. Ewer J
    2. Gammie SC
    3. Truman JW

    (1997)

    Control of insect ecdysis by a positive-feedback endocrine system: roles of eclosion hormone and ecdysis triggering hormone

    The Journal of Experimental Biology 200:869–881.

    • PubMed
    • Google Scholar
25. 1. Fraenkel G
    2. Hsiao C

    (1965) Bursicon, a hormone which mediates tanning of the cuticle in the adult fly and other insects

    Journal of Insect Physiology 11:513–556.

    https://doi.org/10.1016/0022-1910(65)90137-X

    • Google Scholar
26. 1. Frand AR
    2. Russel S
    3. Ruvkun G

    (2005) Functional genomic analysis of C. elegans molting

    PLOS Biology 3:e312.

    https://doi.org/10.1371/journal.pbio.0030312

    • PubMed
    • Google Scholar
27. 1. Frickey T
    2. Lupas A

    (2004) CLANS: a Java application for visualizing protein families based on pairwise similarity

    Bioinformatics 20:3702–3704.

    https://doi.org/10.1093/bioinformatics/bth444

    • PubMed
    • Google Scholar
28. 1. Gammie SC
    2. Truman JW

    (1997a) An endogenous elevation of cGMP increases the excitability of identified insect neurosecretory cells

    Journal of Comparative Physiology A: Sensory, Neural, and Behavioral Physiology 180:329–337.

    https://doi.org/10.1007/s003590050052

    • Google Scholar
29. 1. Gammie SC
    2. Truman JW

    (1997b) Neuropeptide Hierarchies and the Activation of Sequential Motor Behaviors in the Hawkmoth, Manduca sexta

    The Journal of Neuroscience 17:4389–4397.

    https://doi.org/10.1523/JNEUROSCI.17-11-04389.1997

    • Google Scholar
30. 1. Garcia M
    2. Gharbi J
    3. Girault JP
    4. Hetru C
    5. Lafont R

    (1989) Ecdysteroid metabolism in leeches

    Invertebrate Reproduction & Development 15:57–68.

    https://doi.org/10.1080/07924259.1989.9672022

    • Google Scholar
31. 1. Guindon S
    2. Dufayard JF
    3. Lefort V
    4. Anisimova M
    5. Hordijk W
    6. Gascuel O

    (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0

    Systematic Biology 59:307–321.

    https://doi.org/10.1093/sysbio/syq010

    • PubMed
    • Google Scholar
32. 1. Guittard E
    2. Blais C
    3. Maria A
    4. Parvy JP
    5. Pasricha S
    6. Lumb C
    7. Lafont R
    8. Daborn PJ
    9. Dauphin-Villemant C

    (2011) CYP18A1, a key enzyme of Drosophila steroid hormone inactivation, is essential for metamorphosis

    Developmental Biology 349:35–45.

    https://doi.org/10.1016/j.ydbio.2010.09.023

    • PubMed
    • Google Scholar
33. 1. Halanych KM

    (2004) The new view of animal phylogeny

    Annual Review of Ecology, Evolution, and Systematics 35:229–256.

    https://doi.org/10.1146/annurev.ecolsys.35.112202.130124

    • Google Scholar
34. 1. In VV
    2. Ntalamagka N
    3. O'Connor W
    4. Wang T
    5. Powell D
    6. Cummins SF
    7. Elizur A

    (2016) Reproductive neuropeptides that stimulate spawning in the Sydney rock oyster (Saccostrea glomerata)

    Peptides 82:109–119.

    https://doi.org/10.1016/j.peptides.2016.06.007

    • PubMed
    • Google Scholar
35. 1. Jékely G

    (2013) Global view of the evolution and diversity of metazoan neuropeptide signaling

    PNAS 110:8702–8707.

    https://doi.org/10.1073/pnas.1221833110

    • PubMed
    • Google Scholar
36. 1. Jékely G
    2. Paps J
    3. Nielsen C

    (2015) The phylogenetic position of ctenophores and the origin(s) of nervous systems

    EvoDevo 6:1.

    https://doi.org/10.1186/2041-9139-6-1

    • Google Scholar
37. 1. Johnson LS
    2. Eddy SR
    3. Portugaly E

    (2010) Hidden markov model speed heuristic and iterative HMM search procedure

    BMC Bioinformatics 11:431.

    https://doi.org/10.1186/1471-2105-11-431

    • PubMed
    • Google Scholar
38. 1. Katoh K
    2. Standley DM

    (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability

    Molecular Biology and Evolution 30:772–780.

    https://doi.org/10.1093/molbev/mst010

    • PubMed
    • Google Scholar
39. 1. Kim YJ
    2. Spalovská-Valachová I
    3. Cho KH
    4. Zitnanova I
    5. Park Y
    6. Adams ME
    7. Zitnan D

    (2004) Corazonin receptor signaling in ecdysis initiation

    PNAS 101:6704–6709.

    https://doi.org/10.1073/pnas.0305291101

    • PubMed
    • Google Scholar
40. 1. Kim YJ
    2. Zitnan D
    3. Galizia CG
    4. Cho KH
    5. Adams ME

    (2006a) A command chemical triggers an innate behavior by sequential activation of multiple peptidergic ensembles

    Current Biology 16:1395–1407.

    https://doi.org/10.1016/j.cub.2006.06.027

    • PubMed
    • Google Scholar
41. 1. Kim YJ
    2. Zitnan D
    3. Cho KH
    4. Schooley DA
    5. Mizoguchi A
    6. Adams ME

    (2006b) Central peptidergic ensembles associated with organization of an innate behavior

    PNAS 103:14211–14216.

    https://doi.org/10.1073/pnas.0603459103

    • PubMed
    • Google Scholar
42. 1. Koziol U

    (2018) Precursors of neuropeptides and peptide hormones in the genomes of tardigrades

    General and Comparative Endocrinology 267:116–127.

    https://doi.org/10.1016/j.ygcen.2018.06.012

    • PubMed
    • Google Scholar
43. 1. Krüger E
    2. Mena W
    3. Lahr EC
    4. Johnson EC
    5. Ewer J

    (2015) Genetic analysis of eclosion hormone action during Drosophila larval ecdysis

    Development 142:4279–4287.

    https://doi.org/10.1242/dev.126995

    • PubMed
    • Google Scholar
44. 1. Larsson A

    (2014) AliView: a fast and lightweight alignment viewer and editor for large datasets

    Bioinformatics 30:3276–3278.

    https://doi.org/10.1093/bioinformatics/btu531

    • PubMed
    • Google Scholar
45. 1. Lažetić V
    2. Fay DS

    (2017)

    Worm

    Molting in C. elegans, Worm, 6, Taylor & Francis.

    • Google Scholar
46. 1. Lee D
    2. Orchard I
    3. Lange AB

    (2013) Evidence for a conserved CCAP-signaling pathway controlling ecdysis in a hemimetabolous insect, Rhodnius prolixus

    Frontiers in Neuroscience 7:207.

    https://doi.org/10.3389/fnins.2013.00207

    • PubMed
    • Google Scholar
47. 1. Lehman HK
    2. Murgiuc CM
    3. Miller TA
    4. Lee TD
    5. Hildebrand JG

    (1993) Crustacean cardioactive peptide in the sphinx moth, Manduca sexta

    Peptides 14:735–741.

    https://doi.org/10.1016/0196-9781(93)90106-Q

    • Google Scholar
48. 1. Lenaerts C
    2. Cools D
    3. Verdonck R
    4. Verbakel L
    5. Vanden Broeck J
    6. Marchal E

    (2017) The ecdysis triggering hormone system is essential for successful moulting of a major hemimetabolous pest insect, Schistocerca gregaria

    Scientific Reports 7:46502.

    https://doi.org/10.1038/srep46502

    • PubMed
    • Google Scholar
49. 1. McBrayer Z
    2. Ono H
    3. Shimell M
    4. Parvy JP
    5. Beckstead RB
    6. Warren JT
    7. Thummel CS
    8. Dauphin-Villemant C
    9. Gilbert LI
    10. O'Connor MB

    (2007) Prothoracicotropic hormone regulates developmental timing and body size in Drosophila

    Developmental Cell 13:857–871.

    https://doi.org/10.1016/j.devcel.2007.11.003

    • PubMed
    • Google Scholar
50. 1. McNabb SL
    2. Baker JD
    3. Agapite J
    4. Steller H
    5. Riddiford LM
    6. Truman JW

    (1997) Disruption of a behavioral sequence by targeted death of peptidergic neurons in Drosophila

    Neuron 19:813–823.

    https://doi.org/10.1016/S0896-6273(00)80963-0

    • PubMed
    • Google Scholar
51. 1. Mendis AH
    2. Rees HH
    3. Goodwin TW

    (1984) The occurrence of ecdysteroids in the cestode, Moniezia expansa

    Molecular and Biochemical Parasitology 10:123–138.

    https://doi.org/10.1016/0166-6851(84)90001-X

    • PubMed
    • Google Scholar
52. 1. Mirabeau O
    2. Joly JS

    (2013) Molecular evolution of peptidergic signaling systems in bilaterians

    PNAS 110:E2028–E2037.

    https://doi.org/10.1073/pnas.1219956110

    • PubMed
    • Google Scholar
53. 1. Moroz LL
    2. Kocot KM
    3. Citarella MR
    4. Dosung S
    5. Norekian TP
    6. Povolotskaya IS
    7. Grigorenko AP
    8. Dailey C
    9. Berezikov E
    10. Buckley KM
    11. Ptitsyn A
    12. Reshetov D
    13. Mukherjee K
    14. Moroz TP
    15. Bobkova Y
    16. Yu F
    17. Kapitonov VV
    18. Jurka J
    19. Bobkov YV
    20. Swore JJ
    21. Girardo DO
    22. Fodor A
    23. Gusev F
    24. Sanford R
    25. Bruders R
    26. Kittler E
    27. Mills CE
    28. Rast JP
    29. Derelle R
    30. Solovyev VV
    31. Kondrashov FA
    32. Swalla BJ
    33. Sweedler JV
    34. Rogaev EI
    35. Halanych KM
    36. Kohn AB

    (2014) The ctenophore genome and the evolutionary origins of neural systems

    Nature 510:109–114.

    https://doi.org/10.1038/nature13400

    • PubMed
    • Google Scholar
54. 1. Nolte A
    2. Koolman J
    3. Dorlöchter M
    4. Straub H

    (1986) Ecdysteroids in the dorsal bodies of pulmonates (gastropoda): Synthesis and release of ecdysone

    Comparative Biochemistry and Physiology Part A: Physiology 84:777–782.

    https://doi.org/10.1016/0300-9629(86)90405-6

    • Google Scholar
55. 1. Page AP
    2. Stepek G
    3. Winter AD
    4. Pertab D

    (2014) Enzymology of the nematode cuticle: a potential drug target?

    International Journal for Parasitology: Drugs and Drug Resistance 4:133–141.

    https://doi.org/10.1016/j.ijpddr.2014.05.003

    • Google Scholar
56. 1. Park Y
    2. Filippov V
    3. Gill SS
    4. Adams ME

    (2002)

    Deletion of the ecdysis-triggering hormone gene leads to lethal ecdysis deficiency

    Development 129:493–503.

    • PubMed
    • Google Scholar
57. 1. Park Y
    2. Kim YJ
    3. Dupriez V
    4. Adams ME

    (2003)

    Two subtypes of ecdysis triggering hormone receptor in Drosophila Melanogaster

    The Journal of Biological Chemistry.

    • Google Scholar
58. 1. Phlippen MK
    2. Webster SG
    3. Chung JS
    4. Dircksen H

    (2000)

    Ecdysis of decapod crustaceans is associated with a dramatic release of crustacean cardioactive peptide into the haemolymph

    The Journal of Experimental Biology 203:521–536.

    • PubMed
    • Google Scholar
59. 1. Pisani D
    2. Pett W
    3. Dohrmann M
    4. Feuda R
    5. Rota-Stabelli O
    6. Philippe H
    7. Lartillot N
    8. Wörheide G

    (2015) Genomic data do not support comb jellies as the sister group to all other animals

    PNAS 112:15402–15407.

    https://doi.org/10.1073/pnas.1518127112

    • PubMed
    • Google Scholar
60. 1. Rewitz KF
    2. Yamanaka N
    3. Gilbert LI
    4. O'Connor MB

    (2009) The insect neuropeptide PTTH activates receptor tyrosine kinase torso to initiate metamorphosis

    Science 326:1403–1405.

    https://doi.org/10.1126/science.1176450

    • PubMed
    • Google Scholar
61. 1. Rewitz KF
    2. Yamanaka N
    3. O'Connor MB

    (2013) Developmental checkpoints and feedback circuits time insect maturation

    Current Topics in Developmental Biology 103:1–33.

    https://doi.org/10.1016/B978-0-12-385979-2.00001-0

    • PubMed
    • Google Scholar
62. 1. Roller L
    2. Zitnanová I
    3. Dai L
    4. Simo L
    5. Park Y
    6. Satake H
    7. Tanaka Y
    8. Adams ME
    9. Zitnan D

    (2010) Ecdysis triggering hormone signaling in arthropods

    Peptides 31:429–441.

    https://doi.org/10.1016/j.peptides.2009.11.022

    • PubMed
    • Google Scholar
63. 1. Ronquist F
    2. Teslenko M
    3. van der Mark P
    4. Ayres DL
    5. Darling A
    6. Höhna S
    7. Larget B
    8. Liu L
    9. Suchard MA
    10. Huelsenbeck JP

    (2012) MrBayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space

    Systematic Biology 61:539–542.

    https://doi.org/10.1093/sysbio/sys029

    • PubMed
    • Google Scholar
64. 1. Russel S
    2. Frand AR
    3. Ruvkun G

    (2011) Regulation of the C. elegans molt by pqn-47

    Developmental Biology 360:297–309.

    https://doi.org/10.1016/j.ydbio.2011.09.025

    • PubMed
    • Google Scholar
65. 1. Sakai T
    2. Satake H
    3. Takeda M

    (2006) Nutrient-induced alpha-amylase and protease activity is regulated by crustacean cardioactive peptide (CCAP) in the cockroach midgut

    Peptides 27:2157–2164.

    https://doi.org/10.1016/j.peptides.2006.04.009

    • PubMed
    • Google Scholar
66. 1. Schmidt-Rhaesa A
    2. Bartolomaeus T
    3. Lemburg C
    4. Ehlers U
    5. Garey JR

    (1998) The position of the arthropoda in the phylogenetic system

    Journal of Morphology 238:263–285.

    https://doi.org/10.1002/(SICI)1097-4687(199812)238:3<263::AID-JMOR1>3.0.CO;2-L

    • PubMed
    • Google Scholar
67. 1. Schumann I
    2. Kenny N
    3. Hui J
    4. Hering L
    5. Mayer G

    (2018) Halloween genes in Panarthropods and the evolution of the early moulting pathway in ecdysozoa

    Royal Society Open Science 5:180888.

    https://doi.org/10.1098/rsos.180888

    • Google Scholar
68. 1. Shea C
    2. Hough D
    3. Xiao J
    4. Tzertzinis G
    5. Maina CV

    (2004) An rxr/usp homolog from the parasitic nematode, Dirofilaria immitis

    Gene 324:171–182.

    https://doi.org/10.1016/j.gene.2003.09.032

    • PubMed
    • Google Scholar
69. 1. Shi Y
    2. Jiang HB
    3. Gui SH
    4. Liu XQ
    5. Pei YX
    6. Xu L
    7. Smagghe G
    8. Wang JJ

    (2017) Ecdysis triggering hormone signaling (ETH/ETHR-A) Is required for the Larva-Larva ecdysis in Bactrocera dorsalis (Diptera: Tephritidae)

    Frontiers in Physiology 8:587.

    https://doi.org/10.3389/fphys.2017.00587

    • PubMed
    • Google Scholar
70. 1. Stamatakis A

    (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies

    Bioinformatics 30:1312–1313.

    https://doi.org/10.1093/bioinformatics/btu033

    • PubMed
    • Google Scholar
71. 1. Stangier J
    2. Hilbich C
    3. Beyreuther K
    4. Keller R

    (1987) Unusual cardioactive peptide (CCAP) from pericardial organs of the shore crab Carcinus maenas

    PNAS 84:575–579.

    https://doi.org/10.1073/pnas.84.2.575

    • PubMed
    • Google Scholar
72. 1. Stewart MJ
    2. Favrel P
    3. Rotgans BA
    4. Wang T
    5. Zhao M
    6. Sohail M
    7. O'Connor WA
    8. Elizur A
    9. Henry J
    10. Cummins SF

    (2014) Neuropeptides encoded by the genomes of the akoya pearl oyster Pinctata fucata and Pacific oyster Crassostrea gigas: a bioinformatic and peptidomic survey

    BMC Genomics 15:840.

    https://doi.org/10.1186/1471-2164-15-840

    • PubMed
    • Google Scholar
73. 1. Stöver BC
    2. Müller KF

    (2010) TreeGraph 2: combining and visualizing evidence from different phylogenetic analyses

    BMC Bioinformatics 11:7.

    https://doi.org/10.1186/1471-2105-11-7

    • PubMed
    • Google Scholar
74. 1. Suggs JM
    2. Jones TH
    3. Murphree SC
    4. Hillyer JF

    (2016) CCAP and FMRFamide-like peptides accelerate the contraction rate of the antennal accessory pulsatile organs (auxiliary hearts) of mosquitoes

    The Journal of Experimental Biology 219:2388–2395.

    https://doi.org/10.1242/jeb.141655

    • PubMed
    • Google Scholar
75. 1. Telford MJ
    2. Bourlat SJ
    3. Economou A
    4. Papillon D
    5. Rota-Stabelli O

    (2008) The evolution of the ecdysozoa

    Philosophical Transactions of the Royal Society B: Biological Sciences 363:1529–1537.

    https://doi.org/10.1098/rstb.2007.2243

    • Google Scholar
76. 1. Thiel D
    2. Franz-Wachtel M
    3. Aguilera F
    4. Hejnol A

    (2018) Xenacoelomorph neuropeptidomes reveal a major expansion of neuropeptide systems during early bilaterian evolution

    Molecular Biology and Evolution 35:2528–2543.

    https://doi.org/10.1093/molbev/msy160

    • Google Scholar
77. 1. Truman JW

    (2005)

    Hormonal control of insect ecdysis: endocrine cascades for coordinating behavior with physiology

    Vitamins & Hormones 73:1–30.

    • Google Scholar
78. 1. Truman JW
    2. Riddiford LM

    (1970) Neuroendocrine control of ecdysis in silkmoths

    Science 167:1624–1626.

    https://doi.org/10.1126/science.167.3925.1624

    • PubMed
    • Google Scholar
79. 1. Veenstra JA

    (2010) Neurohormones and neuropeptides encoded by the genome of Lottia gigantea, with reference to other mollusks and insects

    General and Comparative Endocrinology 167:86–103.

    https://doi.org/10.1016/j.ygcen.2010.02.010

    • PubMed
    • Google Scholar
80. 1. Veenstra JA
    2. Rombauts S
    3. Grbić M

    (2012) In silico cloning of genes encoding neuropeptides, neurohormones and their putative G-protein coupled receptors in a spider mite

    Insect Biochemistry and Molecular Biology 42:277–295.

    https://doi.org/10.1016/j.ibmb.2011.12.009

    • PubMed
    • Google Scholar
81. 1. Veenstra JA

    (2016) Similarities between decapod and insect neuropeptidomes

    PeerJ 4:e2043.

    https://doi.org/10.7717/peerj.2043

    • PubMed
    • Google Scholar
82. 1. Vehovszky A
    2. Agricola HJ
    3. Elliott CJ
    4. Ohtani M
    5. Kárpáti L
    6. Hernádi L

    (2005) Crustacean cardioactive peptide (CCAP)-related molluscan peptides (M-CCAPs) are potential extrinsic modulators of the buccal feeding network in the pond snail Lymnaea stagnalis

    Neuroscience Letters 373:200–205.

    https://doi.org/10.1016/j.neulet.2004.10.020

    • PubMed
    • Google Scholar
83. 1. Vogel KJ
    2. Brown MR
    3. Strand MR

    (2013) Phylogenetic investigation of peptide hormone and growth factor receptors in five dipteran genomes

    Frontiers in Endocrinology 4:193.

    https://doi.org/10.3389/fendo.2013.00193

    • PubMed
    • Google Scholar
84. 1. Waterhouse AM
    2. Procter JB
    3. Martin DM
    4. Clamp M
    5. Barton GJ

    (2009) Jalview version 2--a multiple sequence alignment editor and analysis workbench

    Bioinformatics 25:1189–1191.

    https://doi.org/10.1093/bioinformatics/btp033

    • PubMed
    • Google Scholar
85. 1. Zandawala M
    2. Moghul I
    3. Yañez Guerra LA
    4. Delroisse J
    5. Abylkassimova N
    6. Hugall AF
    7. O'Hara TD
    8. Elphick MR

    (2017) Discovery of novel representatives of bilaterian neuropeptide families and reconstruction of neuropeptide precursor evolution in ophiuroid echinoderms

    Open Biology 7:170129.

    https://doi.org/10.1098/rsob.170129

    • PubMed
    • Google Scholar
86. 1. Zhang M
    2. Wang Y
    3. Li Y
    4. Li W
    5. Li R
    6. Xie X
    7. Wang S
    8. Hu X
    9. Zhang L
    10. Bao Z

    (2018) Identification and characterization of neuropeptides by transcriptome and proteome analyses in a bivalve mollusc Patinopecten yessoensis

    Frontiers in Genetics 9:.

    https://doi.org/10.3389/fgene.2018.00197

    • Google Scholar
87. 1. Zhu L
    2. Zhang W
    3. Li G
    4. Sun Q-Z
    5. Wang J-J
    6. Smagghe G
    7. Jiang H-B

    (2019) Molecular characterization of ecdysis triggering hormone and its receptor in Citrus red mite (Panonychus citri)

    Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 230:100–105.

    https://doi.org/10.1016/j.cbpa.2019.01.003

    • Google Scholar
88. 1. Zitnan D
    2. Kingan TG
    3. Hermesman JL
    4. Adams ME

    (1996) Identification of ecdysis-triggering hormone from an epitracheal endocrine system

    Science 271:88–91.

    https://doi.org/10.1126/science.271.5245.88

    • PubMed
    • Google Scholar
89. 1. Zitnan D
    2. Ross LS
    3. Zitnanova I
    4. Hermesman JL
    5. Gill SS
    6. Adams ME

    (1999) Steroid induction of a peptide hormone gene leads to orchestration of a defined behavioral sequence

    Neuron 23:523–535.

    https://doi.org/10.1016/S0896-6273(00)80805-3

    • PubMed
    • Google Scholar
90. 1. Zitnan D
    2. Kim YJ
    3. Zitnanová I
    4. Roller L
    5. Adams ME

    (2007) Complex steroid-peptide-receptor cascade controls insect ecdysis

    General and Comparative Endocrinology 153:88–96.

    https://doi.org/10.1016/j.ygcen.2007.04.002

    • PubMed
    • Google Scholar
91. 1. Žitňan D
    2. Adams ME

    (2012)

    Insect Endocrinology

    253–309, Neuroendocrine regulation of ecdysis, Insect Endocrinology, Academic Press.

    • Google Scholar

Author details

1. André Luiz de Oliveira

   Department of Integrative Zoology, Faculty of Life Sciences, University of Vienna, Vienna, Austria

   Contribution

   Conceptualization, Resources, Data curation, Software, Formal analysis, Funding acquisition, Validation, Investigation, Visualization, Methodology, Writing—original draft, Writing—review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-3542-4439

2. Andrew Calcino

   Department of Integrative Zoology, Faculty of Life Sciences, University of Vienna, Vienna, Austria

   Contribution

   Conceptualization, Methodology, Writing—review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-3956-1273

3. Andreas Wanninger

   Department of Integrative Zoology, Faculty of Life Sciences, University of Vienna, Vienna, Austria

   Contribution

   Conceptualization, Resources, Supervision, Funding acquisition, Investigation, Project administration, Writing—review and editing

   For correspondence

   andreas.wanninger@univie.ac.at

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-3266-5838

• 5,185

  views

• 630

  downloads

• 37

  citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.