Molecular evolution of the crustacean hyperglycemic hormone family in ecdysozoans
© Montagné et al; licensee BioMed Central Ltd. 2010
Received: 25 September 2009
Accepted: 25 February 2010
Published: 25 February 2010
Crustacean Hyperglycemic Hormone (CHH) family peptides are neurohormones known to regulate several important functions in decapod crustaceans such as ionic and energetic metabolism, molting and reproduction. The structural conservation of these peptides, together with the variety of functions they display, led us to investigate their evolutionary history. CHH family peptides exist in insects (Ion Transport Peptides) and may be present in all ecdysozoans as well. In order to extend the evolutionary study to the entire family, CHH family peptides were thus searched in taxa outside decapods, where they have been, to date, poorly investigated.
CHH family peptides were characterized by molecular cloning in a branchiopod crustacean, Daphnia magna, and in a collembolan, Folsomia candida. Genes encoding such peptides were also rebuilt in silico from genomic sequences of another branchiopod, a chelicerate and two nematodes. These sequences were included in updated datasets to build phylogenies of the CHH family in pancrustaceans. These phylogenies suggest that peptides found in Branchiopoda and Collembola are more closely related to insect ITPs than to crustacean CHHs. Datasets were also used to support a phylogenetic hypothesis about pancrustacean relationships, which, in addition to gene structures, allowed us to propose two evolutionary scenarios of this multigenic family in ecdysozoans.
Evolutionary scenarios suggest that CHH family genes of ecdysozoans originate from an ancestral two-exon gene, and genes of arthropods from a three-exon one. In malacostracans, the evolution of the CHH family has involved several duplication, insertion or deletion events, leading to neuropeptides with a wide variety of functions, as observed in decapods. This family could thus constitute a promising model to investigate the links between gene duplications and functional divergence.
The study of the evolutionary history of arthropods is a challenging field of research, as they constitute the large majority of known metazoan species and exhibit an extreme diversity of body plans and physiology. Nowadays, evo-devo approaches largely contribute to this research area [reviewed in ], but the evolution of peptide hormone families directly involved in physiological adaptations remains poorly investigated in arthropods, especially when compared to vertebrates. The Crustacean Hyperglycemic Hormone (CHH) family could constitute a model of choice to address this question, as CHH family peptides are well known in decapod crustaceans, where they do play major roles in many physiological processes. Since decapods were the first invertebrates where a neuroendocrine mechanism was discovered, they have been extensively used in comparative endocrinology studies, and CHH has become the archetype of a neuropeptide family including around 150 members to date [reviewed in [2–4]]. CHH family peptides are 72 to 78 amino acids long and are, based on structural features, divided into two sub-families . Type I peptides, the CHHs sensu stricto, are pleiotropic hormones involved in the regulation of energetic and ionic metabolism and, in addition, can also exert an inhibitory effect on molting and reproduction [reviewed in ]. By a tissue-specific alternative splicing mechanism, CHH genes produce a second peptide, devoid of hyperglycemic activity, named CHH-L (for CHH long isoform), which may be involved in osmoregulation [7–9]. Type II peptides, namely the molt-inhibiting hormones (MIHs), the vitellogenesis-inhibiting hormones (VIHs) and the mandibular organ-inhibiting hormones (MOIHs), are functionally more specialized than CHHs. Characterized through their inhibitory actions on molting and reproduction, they never elicit hyperglycemia [reviewed in [2, 10]].
Newly characterized sequences were included in CHH family sequence datasets, which were then used to build phylogenies of this family and to investigate its evolutionary history. Because of the reduced size of these datasets, a test was conducted to assess which of the two phylogenetic hypotheses presented Figure 1 was more strongly supported by our data, and could be further used as a basis to elaborate evolutionary scenarios of the CHH family genes.
CHH family peptides characterized in Daphnia magna and Folsomia candida
The two complete cDNA sequences obtained from the collembolan Folsomia candida led to similar results: two transcripts of different lengths (1307 and 2018 bp) encoded prepro-peptides which only differed after the fortieth residue of the mature peptide. The 72 residue amidated peptide, translated from the short cDNA, was named ITP and the 82 residue non-amidated peptide, translated from the longest cDNA, was named ITP-L (Figure 2A and 2B).
Sequences characterized in silico
For the insects Anopheles gambiae, Apis mellifera, Culex pipiens, Nasonia vitripennis and Pediculus humanus, nucleotide sequences encoding for ITP or ITP-L, which have not been recovered by automatic annotation programs were deduced from the gene sequence following alternative splicing rules. A gene encoding putative ITP and ITP-L isoforms was also found in the genome of another water flea, Daphnia pulex. At the present time, both ITP (72 or 73 residue amidated peptides) and ITP-L (79 to 90 residue non-amidated peptides) sequences are available from 12 insect and two branchiopod species (Figure 2A and 2B).
In the genome of the deer tick Ixodes scapularis (Chelicerata), a gene was found that encoded only one mature ITP-like peptide. In addition, cDNA and peptide sequences of another ITP-like peptide were found, during database mining, in the American dog tick Dermacentor variabilis. These peptides are 74 and 75 residue long, respectively, and are not amidated on their C-terminal end (Figure 2A).
Phylogeny of CHH family peptides in Pancrustacea
A clade supported by a bootstrap value of 76% (pp of 0.99 in BI) was positioned at the base of the type I and type II clades and contained all ITPs from insects, together with the peptides characterized in the collembolan Folsomia candida and the branchiopods Daphnia magna and Daphnia pulex, which were located at the base. The type III sub-family was thus created to designate peptides contained in this clade.
Since the topology of this clade was only weakly supported (notably with insects appearing paraphyletic), amino acid and DNA datasets containing less taxa but more characters were used for phylogenetic inference. When an outgroup (DNA or amino acid sequences from Ixodes scapularis) was included in these datasets, a structure of two monophyletic groups was found within the ingroup: a "type I" clade (supported by a bootstrap value of 100% in the ML analysis based on the amino acid dataset and by posterior probabilities of 1.00 in BI analyses using either amino acid or DNA dataset) and a "type III" clade (bootstrap value of 48% in the ML analysis of the amino acid dataset, posterior probabilities of 0.79 and 0.98 in BI analyses based on the amino acid and the DNA datasets, respectively). Since the four exons used in these datasets exist only in the ingroup species, the inclusion of the outgroup resulted in a loss of phylogenetic signal. Then, the outgroup was removed for subsequent analyses and the resulting trees were rooted using the structure in two clades previously found.
Evolutionary scenarios of the CHH family genes
Because of the weak support, in the ML phylogeny (Figure 5), at the node indicating the duplication which led to the two paralogous CHH genes found in Dendrobranchiata (with three or four exons), an alternative topology was considered for pancrustacean CHH family genes, where the CHH gene duplication would have occurred only in the Dendrobranchiata phylum (Figure 7B). In that case, the most parsimonious scenario implied eight intron or exon insertion/deletion events, and the exon duplication leading to the four-exon gene structure would have occurred only once.
Regardless of the evolutionary scenario considered, the putative ancestral gene was likely composed of two exons and a phase 2 intron interrupting the codon of the amino acid residue following the fourth cysteine of the mature peptide. Such an intron was found in every known CHH family gene, except the ITP2 genes in Caenorhabditis species and the ITP gene of Trichinella spiralis (Figure 4).
Dibasic processing sites used for precursor maturation by prohormone convertase then likely appeared independently twice, in the common ancestor to arthropods on one hand and in the common ancestor to the Caenorhabditis genus on the other hand, leading to the occurrence in these lineages of precursor related peptides (blue boxes in Figures 4 and 7), such as the CHH-precursor related peptides (CPRPs) of decapods.
Evolution of the CHH family in decapods and functional implications
Since the discovery of neuroendocrine factors within the eyestalks of decapods seventy years ago [24–26], structural and functional data about CHH family peptides in these crustaceans have been accumulated. While our knowledge increased, it became more and more difficult to propose a model of endocrine regulation applying to all decapods. Indeed, CHH family peptides are not identical in all decapod groups, and their function varies with the species. This diversity prompted us to investigate the evolutionary history of these peptides.
In decapods, many gene duplications have occurred, leading to two main paralogous lineages (type I and type II peptides) and to a large polymorphism of CHH family peptides inside these lineages (Figure 7). For example, two clusters containing each at least 7 different CHH genes were identified in the shrimp Metapenaeus ensis . A paradigm in evolutionary biology is that gene duplication represents the major mechanism for emergence of new functions, as one of the two copies is potentially freed from selective pressure and will accumulate more mutations during evolution [28, 29]. In the CHH family, the functional divergence observed between the two paralogous lineages could result from a subfunctionalization [30, 31], rather than from a neofunctionalization. In fact, the ancestral gene may have encoded a pleiotropic hormone, like current CHHs, and after duplication of this gene the type II paralogous lineage may have evolved faster to peptides with a CHH-like structure, but devoid of hyperglycemic activity and conversely exhibiting more specialized activities, such as inhibition of molting or vitellogenesis (for MIHs and VIHs, respectively). The faster evolution rate of type II peptide genes may explain the loss of phylogenetic signal observed in MIHs, VIHs and MOIHs sequences. Indeed, the topology of the "type II" clade (Figure 5) is not congruent with the phylogeny of decapods, whereas it is for the "type I" clade, as shown in earlier work . This clearly impedes the elucidation of evolutionary relationships between type II peptides. The only paralogous lineages clearly identified so far are the MIHs and MOIHs of Cancer crabs, as the MOIH genes seem to have appeared from a duplicated MIH gene only in this genus . In lobsters, there is no MIH identified so far but a VIH instead, whose gene may have evolved from a MIH gene subjected to a reduced selective pressure, as molt inhibition is exerted in this taxa by a CHH isoform .
Evolutionary history "outside decapods"
A high number of gene duplications were observed in decapods only. So far, the only paralogous lineages identified outside decapods are the "ITP1" and "ITP2" genes found in Caenorhabditis species (Figure 7), and only one CHH family peptide gene could be found in genomes of the other nematodes, the insects and the deer tick. In the water flea Daphnia pulex, one ITP gene was also rebuilt from whole genome shotgun (WGS) sequences but other WGS sequences sharing sequence identity with the ITP gene have been found. However, it is unclear whether these sequences correspond to another CHH family peptide coding gene or to a pseudo-gene: this gene would have a peculiar structure, with exon III lacking, and the prepro-peptide putatively encoded would lack the dibasic processing site found in every CHH or ITP precursors and the 6 following residues of the mature peptide as well. Yet, although only one ITP and one ITP-L cDNA have been cloned in Daphnia magna, recently published EST data suggest that both genes may be expressed in Daphnia pulex , but EST and genomic sequences do not match (only 85% identity between deduced amino acid sequences). To include these data in an evolutionary scenario, genomic and mRNA sequences should be characterized by molecular cloning.
This apparent lack of paralogous lineages outside decapods raises the question of a possible conservation of function between the ITPs of insects and the related peptides found in branchiopods, chelicerates and nematodes. Yet, functional studies are too scarce to address this question. In insects, the effect of ITP on ionic and water balance was only demonstrated in locusts [35, 36] and nothing is known about the function of ITP-like peptides in chelicerates or nematodes. In branchiopods, only one gene expression study on sex determination in Daphnia magna has indicated that CHH family peptides may inhibit methyl farnesoate synthesis by the mandibular organ . It is noteworthy that several CHH family peptides are known to play such a role in decapods [38–40]. It will be informative to determine whether Daphnia peptides exhibit other typical "decapod" functions such as hyperglycemia or ecdysteroid synthesis inhibition, or if they also possess an anti-diuretic activity, as shown for insect ITPs. A similar question about another neuropeptide family, the RPCH/AKH family, has recently found a partial answer. Like for the CHH family, the putative RPCH (red pigment-concentrating hormone) of Daphnia magna shares more sequence similarity with AKHs (adipo-kinetic hormones) of insects than with RPCH of decapod crustaceans . In a heterologous bioassay, this peptide was able to trigger a mobilization of lipid reserves when injected into the green shield bug Nezara viridula whereas it did not provoke pigment migration when injected into the shrimp Palaemon pacificus . Although heterologous bioassays must be considered cautiously, such results suggest that this peptide could have an adipokinetic function in water fleas (like in insects) rather than a pigment-concentration function (like in decapods).
Emergence of the four-exon genes
One important step in the evolution of the CHH family is the emergence of the four-exon genes found in decapods, branchiopods and insects. In these genes, exons III and IV encode peptide sequences of similar lengths, with two cystein residues in the same positions, thus suggesting that the supplementary exon has appeared by tandem duplication of another exon. At first glance, it seems more likely that this duplication has occurred only once, in a common ancestor of Pancrustacea (Figure 7B). In all these taxa, two peptides are produced by alternative splicing; one peptide (CHH or ITP) is 72 or 73 amino acids long and is always amidated on its C-terminal end, and the other peptide (CHH-L or ITP-L) is slightly longer and is never amidated. Moreover, the expression of these two isoforms seems to be similar in decapods and insects; in the crab Carcinus maenas and the caridean shrimp Macrobrachium rosenbergii, CHH transcripts were mainly found in neurons of the central nervous system (more precisely in the X-organ located in the eyestalk) whereas CHH-L transcripts were found in neurons of the peripheral nervous system [7, 8]; in the moths Manduca sexta and Bombyx mori and the locust Schistocerca americana, ITP-immunoreactive neurons were only found in the brain, whereas ITP-L-immunoreactive ones were found along the ventral nervous chain. ITP-L immunoreactivity was also detected in the brain, but was weak and restricted to cell bodies, thus suggesting that ITP-L was not secreted from this tissue .
Yet, even if the hypothesis of an independent emergence of the fourth exon (Figure 7A) appears unlikely, it should not be rejected, as a similar exon duplication also occurred in a Drosophila ancestor, leading to the five-exon gene found in Drosophila melanogaster .
Controversy about pancrustacean phylogeny
Given the relative short length of the sequences used, the objective of this study was not to build a phylogeny of pancrustaceans using CHH family peptides, but to choose the appropriate phylogeny to infer evolutionary scenarios of the CHH family. The KH test carried out with our datasets indicated a congruence of the data with recent molecular phylogenies of pancrustaceans based on nuclear gene sequences [21–23] and not with those based on mitochondrial genes [18–20]. Moreover, the robustness and quality of the signal contained in mitochondrial gene sequences for arthropod phylogenetics have recently been questioned [45, 46]. Supplementary taxa will have to be represented within CHH family datasets to confirm this result, but studying the evolutionary history of this family may help to select synapomorphies to support concurrent phylogenetic hypotheses about pancrustacean relationships. For example, the presence of paralogous type I and type II peptides could constitute a trait shared by malacostracans and their sister-groups.
The evolutionary scenarios proposed in this study suggest that genes encoding Crustacean Hyperglycemic Hormone family peptides of Ecdysozoa evolved from an ancestral two-exon gene. In the malacostracan lineage (including decapods), the evolution of the CHH family has involved numerous duplications, insertions and deletions of exons or entire genes, leading to the wide variety of functions displayed by the encoded neurohormones in decapods. This neuropeptide family could thus constitute a promising model to investigate the evolutionary forces at the root of the functional divergence of duplicated genes. Outside malacostracans, the number of gene duplications seems to have been lower, which may reflect different evolutionary pathways. At present, CHH family peptides characterized outside decapods are still scarce, and this work constitutes a first step in a wider quest. In the future, the evolutionary scenarios elaborated here will be completed and amended, as CHH family peptides will probably be characterized in new taxa. The 38 genome sequencing projects currently under way in ecdysozoan species will be of valuable help as soon as they are completed, to enlarge our view on the evolution of this multigenic family.
Biological material and RNA extraction
Daphnia magna and Folsomia candida (strain TO) specimens were supplied by the BIOEMCO laboratory and the Ecology & Evolution laboratory, respectively, both located at the Ecole Normale Supérieure (Paris, France). Total RNA was extracted from 10 mg of whole animals, using SV Total RNA Isolation System (Promega, Madison, WI). cDNA was synthesized from 300 ng of total RNA using 200 U of M-MLV Reverse Transcriptase (Promega), 20 pmoles of each dNTP and 30 pmoles of an Oligo(dT) primer. This synthesis was performed at 42°C for 1 hour, followed by an inactivation step at 70°C for 15 min.
PCR amplification and cloning
First, a central region of putative ITP precursor cDNAs was amplified using degenerate primers DgnITP-Up (5'-CTTCGAYATCMAKTGYAARGG-3') and DgnITP-Down (5'-RAGRCAWCCTTTGAAGWATG-3') designed from the alignment of known insect ITP cDNAs. The reaction mixture contained 1.5 U of GoTaq® DNA Polymerase (Promega), 5 pmoles of each dNTP and 10 pmoles of each degenerate primer. Amplifications were conducted with a denaturation step at 94°C for 3 min, followed by 40 cycles of 94°C for 30 sec, 55°C for 30 sec and 72°C for 30 sec, and a final extension step at 72°C for 10 min. After their purification with the Wizard® SV Gel and PCR Clean-Up System (Promega), products were cloned using pGEM®-T Easy Vector and JM109 Competent Cells (Promega). Plasmids were purified using the Wizard® Plus SV Minipreps DNA Purification System (Promega), and their sequencing was performed by Cogenics - Genome Express (Meylan, France).
3' and 5'RACE
Primers used for 3' and 5'RACE.
Sequence (5' to 3')
A search for CHH family peptide sequences from arthropods and nematodes was performed with the BLAST program at the NCBI website http://blast.ncbi.nlm.nih.gov/Blast.cgi. The non-redundant protein sequences (nr) database was mined by blastp algorithm using Schistocerca gregaria ITP or the putative peptide ZC168.2 of Caenorhabditis elegans as query sequences for arthropods and for nematodes, respectively. Corresponding mRNA sequences were also collected, and aligned with genome sequences to determine the exon-intron structure of the genes. Sequences of genes encoding putative CHH family peptides of Daphnia pulex (Branchiopoda), Ixodes scapularis (Chelicerata), Caenorhabditis remanei and Brugia malayi (Nematoda) were assembled from whole genome shotgun (WGS) sequences available in the NCBI Trace Archives database, by assembling trace reads with CLC Genomics Workbench software (CLCbio, Aarhus, Denmark).
Amino acid sequences used for phylogenetic inference.
DNA and amino acid datasets including CHH-L and ITP-L sequences were also created. For the 23 taxa in which such peptides are known, the amino acid sequence of the mature CHH-L or ITP-L (encoded by exons II and III of the gene) was concatenated with the C-terminal sequence of CHH or ITP (encoded by exon IV of the gene). Alignments were performed manually and 109 unambiguously aligned residues were conserved in the dataset. The DNA dataset contained 327 characters.
At first, DNA and translated amino acid sequences of Ixodes scapularis ITP-like were included in these datasets, to be used as an outgroup in order to determine the global branching order in the ingroup. Since the gene encoding this peptide lacks exon III in the outgroup taxon, corresponding characters were replaced with "?" symbols in the alignments. Because of the loss of phylogenetic signal brought by the inclusion of the outgroup, it was removed from datasets for subsequent phylogenetic analyses, but the global structure previously found was kept.
Phylogenetic reconstructions were carried out using Bayesian inference and maximum likelihood. Bayesian analyses were performed with MrBayes 3.1.2 with four chains of 106 generations, trees sampled every 100 generations and burn-in value set to 20% of the sampled trees. We checked that standard deviation of the split frequencies fell below 0.01 to insure convergence in tree search. Protein sequences were analyzed with a mixed amino acid model , and DNA sequences were considered with an evolutionary model designed for coding sequences and taking the genetic code into account [48–50].
Maximum likelihood reconstructions were carried out only on amino acid sequences. For both datasets, the WAG+I+G substitution model  was determined as the best-fit model of protein evolution by ProtTest 1.3 http://darwin.uvigo.es/software/prottest_server.html, following Akaike Information Criterion. Rate heterogeneity was set at four categories. The gamma distribution parameter and the proportion of invariable sites were estimated from the datasets. Tree reconstructions were performed using PhyML 3.0 http://www.atgc-montpellier.fr/phyml/ and validated with 100 bootstrap replicates.
The two phylogenetic trees shown in Figure 1 were used as competing hypotheses to assess if one was more strongly supported by the 23-taxa sequence datasets. This was done via a KH test using a maximum likelihood criterion . This allowed us to choose a "species tree" on which the "gene tree" could be super-imposed.
The evolution of CHH family gene structures was analyzed using Mesquite 2.6 , under a parsimony framework. For this analysis, two alternate topologies depicting the evolution of the CHH family genes were created. All the known intron locations within CHH family genes were considered as characters and the presence/absence of intron in each location was coded 0 (absence) or 1 (presence) to create a character matrix.
The authors are grateful to Drs Gérard Lacroix, Michaël Danger and Thomas Tully (Ecole Normale Supérieure, Paris) for supplying water fleas and springtails, and to Drs Laurence Dinan and Stéphane Hourdez for critical reading of the manuscript.
- Angelini DR, Kaufman TC: Comparative developmental genetics and the evolution of arthropod body plans. Annu Rev Genet. 2005, 39: 95-119. 10.1146/annurev.genet.39.073003.112310.View ArticlePubMedGoogle Scholar
- Böcking D, Dircksen H, Keller R: The crustacean neuropeptides of the CHH/MIH/GIH family: structures and biological activities. The Crustacean Nervous System. Edited by: Wiese K. 2002, Berlin, Heidelberg, New York: Springer, 84-97.View ArticleGoogle Scholar
- Chen SH, Lin CY, Kuo CM: In silico analysis of crustacean hyperglycemic hormone family. Mar Biotechnol (NY). 2005, 7 (3): 193-206. 10.1007/s10126-004-0020-5.View ArticleGoogle Scholar
- Soyez D: Recent data on the crustacean hyperglycemic hormone family. Recent Advances in Marine Biotechnology. Edited by: Fingerman M, Nagabhushanam R. 2003, Plymouth, U.K.: Science Publishers, 10: 279-301.Google Scholar
- Lacombe C, Grève P, Martin G: Overview on the sub-grouping of the crustacean hyperglycemic hormone family. Neuropeptides. 1999, 33 (1): 71-80. 10.1054/npep.1999.0016.View ArticlePubMedGoogle Scholar
- Fanjul-Moles ML: Biochemical and functional aspects of crustacean hyperglycemic hormone in decapod crustaceans: review and update. Comp Biochem Physiol C Toxicol Pharmacol. 2006, 142 (3-4): 390-400. 10.1016/j.cbpc.2005.11.021.View ArticlePubMedGoogle Scholar
- Chen SH, Lin CY, Kuo CM: Cloning of two crustacean hyperglycemic hormone isoforms in freshwater giant prawn (Macrobrachium rosenbergii): evidence of alternative splicing. Mar Biotechnol (NY). 2004, 6 (1): 83-94. 10.1007/s10126-003-0014-8.View ArticleGoogle Scholar
- Dircksen H, Böcking D, Heyn U, Mandel C, Chung JS, Baggerman G, Verhaert P, Daufeldt S, Plosch T, Jaros PP, et al: Crustacean hyperglycaemic hormone (CHH)-like peptides and CHH-precursor-related peptides from pericardial organ neurosecretory cells in the shore crab, Carcinus maenas, are putatively spliced and modified products of multiple genes. Biochem J. 2001, 356 (1): 159-170. 10.1042/0264-6021:3560159.PubMed CentralView ArticlePubMedGoogle Scholar
- Tiu SH, He JG, Chan SM: The LvCHH-ITP gene of the shrimp (Litopenaeus vannamei) produces a widely expressed putative ion transport peptide (LvITP) for osmo-regulation. Gene. 2007, 396 (2): 226-235. 10.1016/j.gene.2007.02.027.View ArticlePubMedGoogle Scholar
- Webster SG: Neuropeptides inhibiting growth and reproduction in crustaceans. Recent Advances in Arthropod Endocrinology. Edited by: Coast GM, Webster SG. 1998, Cambridge, U.K.: Cambridge University Press, 33-52.Google Scholar
- Montagné N, Soyez D, Gallois D, Ollivaux C, Toullec JY: New insights into evolution of crustacean hyperglycaemic hormone in decapods - first characterization in Anomura. FEBS J. 2008, 275 (5): 1039-1052. 10.1111/j.1742-4658.2007.06245.x.View ArticlePubMedGoogle Scholar
- Grève P, Sorokine O, Berges T, Lacombe C, Van Dorsselaer A, Martin G: Isolation and amino acid sequence of a peptide with vitellogenesis inhibiting activity from the terrestrial isopod Armadillidium vulgare (Crustacea). Gen Comp Endocrinol. 1999, 115 (3): 406-414. 10.1006/gcen.1999.7330.View ArticlePubMedGoogle Scholar
- Martin G, Sorokine O, Van Dorsselaer A: Isolation and molecular characterization of a hyperglycemic neuropeptide from the sinus gland of the terrestrial isopod Armadillidium vulgare (Crustacea). Eur J Biochem. 1993, 211 (3): 601-607. 10.1111/j.1432-1033.1993.tb17587.x.View ArticlePubMedGoogle Scholar
- Dircksen H: Insect ion transport peptides are derived from alternatively spliced genes and differentially expressed in the central and peripheral nervous system. J Exp Biol. 2009, 212 (3): 401-412. 10.1242/jeb.026112.View ArticlePubMedGoogle Scholar
- Zhang Q, Keller R, Dircksen H: Crustacean hyperglycaemic hormone in the nervous system of the primitive crustacean species Daphnia magna and Artemia salina (Crustacea: Branchiopoda). Cell Tiss Res. 1997, 287 (3): 565-576. 10.1007/s004410050779.View ArticleGoogle Scholar
- Laverdure AM, Carette-Desmoucelles C, Breuzet M, Descamps M: Neuropeptides and related nucleic acid sequences detected in peneid shrimps by immunohistochemistry and molecular hybridizations. Neuroscience. 1994, 60 (2): 569-579. 10.1016/0306-4522(94)90265-8.View ArticlePubMedGoogle Scholar
- Stockmann R, Laverdure AM, Breuzet M: Localization of a crustacean hyperglycemic hormone-like immunoreactivity in the neuroendocrine system of Euscorpius carpathicus (L.) (Scorpionida, Chactidae). Gen Comp Endocrinol. 1997, 106 (3): 320-326. 10.1006/gcen.1997.6874.View ArticlePubMedGoogle Scholar
- Carapelli A, Liò P, Nardi F, Wath van der E, Frati F: Phylogenetic analysis of mitochondrial protein coding genes confirms the reciprocal paraphyly of Hexapoda and Crustacea. BMC Evol Biol. 2007, 7 (suppl2 S8): 2-13.Google Scholar
- Cook CE, Yue Q, Akam M: Mitochondrial genomes suggest that hexapods and crustaceans are mutually paraphyletic. Proc R Soc B. 2005, 272: 1295-1304. 10.1098/rspb.2004.3042.PubMed CentralView ArticlePubMedGoogle Scholar
- Hassanin A: Phylogeny of Arthropoda inferred from mitochondrial sequences: strategies for limiting the misleading effects of multiple changes in pattern and rates of substitution. Mol Phylogenet Evol. 2006, 38: 100-106. 10.1016/j.ympev.2005.09.012.View ArticlePubMedGoogle Scholar
- Mallatt J, Giribet G: Further use of nearly complete 28S and 18S rRNA genes to classify Ecdysozoa: 37 more arthropods and a kinorhynch. Mol Phylogenet Evol. 2006, 40: 772-794. 10.1016/j.ympev.2006.04.021.View ArticlePubMedGoogle Scholar
- Timmermans MJ, Roelofs D, Marien J, van Straalen NM: Revealing pancrustacean relationships: phylogenetic analysis of ribosomal protein genes places Collembola (springtails) in a monophyletic Hexapoda and reinforces the discrepancy between mitochondrial and nuclear DNA markers. BMC Evol Biol. 2008, 8: 83-10.1186/1471-2148-8-83.PubMed CentralView ArticlePubMedGoogle Scholar
- Regier JC, Shultz JW, Kambic RE: Pancrustacean phylogeny: hexapods are terrestrial crustaceans and maxillopods are not monophyletic. Proc R Soc B. 2005, 272: 395-401. 10.1098/rspb.2004.2917.PubMed CentralView ArticlePubMedGoogle Scholar
- Abramowitz RK, Abramowitz AA: Moulting, growth, and survival after eyestalk removal in Uca pugilator. Biol Bull. 1940, 78: 179-188. 10.2307/1537771.View ArticleGoogle Scholar
- Brown FA, Cunningham O: Influence of the sinusgland of crustaceans on normal viability and ecdysis. Biol Bull. 1939, 77: 104-114. 10.2307/1537849.View ArticleGoogle Scholar
- Smith RI: Studies on the effects of eyestalk removal upon young crayfish (Cambarus clarkii, Girard). Biol Bull. 1940, 79: 145-152. 10.2307/1537835.View ArticleGoogle Scholar
- Gu PL, Yu KL, Chan SM: Molecular characterization of an additional shrimp hyperglycemic hormone: cDNA cloning, gene organization, expression and biological assay of recombinant protein. FEBS Lett. 2000, 472: 122-128. 10.1016/S0014-5793(00)01420-4.View ArticlePubMedGoogle Scholar
- Ohno S: Evolution by Gene Duplication. Berlin, Heidelberg. 1970, New York: Springer-VerlagGoogle Scholar
- Zhang J: Evolution by gene duplication: an update. Trends Ecol Evol. 2003, 18 (6): 292-298. 10.1016/S0169-5347(03)00033-8.View ArticleGoogle Scholar
- Hughes AL: The evolution of functionally novel proteins after gene duplication. Proc R Soc B. 1994, 256 (1346): 119-124. 10.1098/rspb.1994.0058.View ArticlePubMedGoogle Scholar
- Lynch M, Force A: The probability of duplicate gene preservation by subfunctionalization. Genetics. 2000, 154 (1): 459-473.PubMed CentralPubMedGoogle Scholar
- Lu W, Wainwright G, Webster SG, Rees HH, Turner PC: Clustering of mandibular organ-inhibiting hormone and moult-inhibiting hormone genes in the crab, Cancer pagurus, and implications for regulation of expression. Gene. 2000, 253 (2): 197-207. 10.1016/S0378-1119(00)00282-1.View ArticlePubMedGoogle Scholar
- Chang ES, Bruce MJ, Newcomb RW: Purification and amino acid composition of a peptide with molt-inhibiting activity from the lobster Homarus americanus. Gen Comp Endocrinol. 1987, 65: 56-64. 10.1016/0016-6480(87)90222-X.View ArticlePubMedGoogle Scholar
- Gard AL, Lenz PH, Shaw JR, Christie AE: Identification of putative peptide paracrines/hormones in the water flea Daphnia pulex (Crustacea; Branchiopoda; Cladocera) using transcriptomics and immunohistochemistry. Gen Comp Endocrinol. 2009, 160 (3): 271-287. 10.1016/j.ygcen.2008.12.014.View ArticlePubMedGoogle Scholar
- King DS, Meredith J, Wang YJ, Phillips JE: Biological actions of synthetic locust ion transport peptide (ITP). Insect Biochem Mol Biol. 1999, 29: 11-18. 10.1016/S0965-1748(98)00098-8.View ArticlePubMedGoogle Scholar
- Phillips JE, Meredith J, Audsley N, Richardson N, Macins A, Ring M: Locust ion transport peptide (ITP): A putative hormone controlling water and ionic balance in terrestrial insects. Amer Zool. 1998, 38 (3): 461-470.View ArticleGoogle Scholar
- Eads BD, Andrews J, Colbourne JK: Ecological genomics in Daphnia: stress responses and environmental sex determination. Heredity. 2008, 100 (2): 184-190. 10.1038/sj.hdy.6800999.View ArticlePubMedGoogle Scholar
- Keller R, Kegel G, Reichwein B, Sedlmeier D, Soyez D: Biological effects of neurohormones of the CHH/MIH/GIH peptide family in crustaceans. Recent Developments in Comparative Endocrinology and Neurobiology. Edited by: Roubos EW, Wendelaar Bonga SE, Vaudry H, De Loof A. 1999, Nijmegen: Shaker, 209-212.Google Scholar
- Laufer H, Johnson M, Demir N, Twidy K, Chang E, Soyez D, Van Herp F, Bagshaw J: Identification of lobster hyperglycemic hormones (CHHs) with mandibular organ inhibiting activity. SICB Annual Meeting: 2003; Toronto, Canada. 2003Google Scholar
- Wainwright G, Webster SG, Wilkinson MC, Chung JS, Rees HH: Structure and significance of mandibular organ-inhibiting hormone in the crab, Cancer pagurus - Involvement in multihormonal regulation of growth and reproduction. J Biol Chem. 1996, 271 (22): 12749-12754. 10.1074/jbc.271.22.12749.View ArticlePubMedGoogle Scholar
- Christie AE, Cashman CR, Brennan HR, Ma M, Sousa GL, Li L, Stemmler EA, Dickinson PS: Identification of putative crustacean neuropeptides using in silico analyses of publicly accessible expressed sequence tags. Gen Comp Endocrinol. 2008, 156 (2): 246-264. 10.1016/j.ygcen.2008.01.018.View ArticlePubMedGoogle Scholar
- Marco HG, Gäde G: Biological activity of the predicted red pigment-concentrating hormone of Daphnia pulex in a crustacean and an insect. Gen Comp Endocrinol. 2010, 166 (1): 104-110. 10.1016/j.ygcen.2009.08.002.View ArticlePubMedGoogle Scholar
- Dai L, Zitnan D, Adams ME: Strategic expression of ion transport peptide gene products in central and peripheral neurons of insects. J Comp Neurol. 2007, 500: 353-367. 10.1002/cne.21192.View ArticlePubMedGoogle Scholar
- Dircksen H, Tesfai LK, Albus C, Nassel DR: Ion transport peptide splice forms in central and peripheral neurons throughout postembryogenesis of Drosophila melanogaster. J Comp Neurol. 2008, 509 (1): 23-41. 10.1002/cne.21715.View ArticlePubMedGoogle Scholar
- Cameron SL, Miller KB, D'Haese CA, Whiting MF, Barker SC: Mitochondrial genome data alone are not enough to unambiguously resolve the relationships of Entognatha, Insecta and Crustacea sensu lato (Arthropoda). Cladistics. 2004, 20: 534-557. 10.1111/j.1096-0031.2004.00040.x.View ArticleGoogle Scholar
- Delsuc F, Phillips MJ, Penny D: Comment on "Hexapod origins: monophyletic or paraphyletic?". Science. 2003, 301: 1482-10.1126/science.1086558.View ArticlePubMedGoogle Scholar
- Ronquist F, Huelsenbeck JP: MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003, 19: 1572-1574. 10.1093/bioinformatics/btg180.View ArticlePubMedGoogle Scholar
- Goldman N, Yang Z: A codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol Biol Evol. 1994, 11: 725-736.PubMedGoogle Scholar
- Muse SV, Gaut BS: A likelihood approach for comparing synonymous and nonsynonymous nucleotide substitution rates, with application to the chloroplast genome. Mol Biol Evol. 1994, 11: 715-724.PubMedGoogle Scholar
- Shapiro B, Rambaut A, Drummond AJ: Choosing appropriate substitution models for the phylogenetic analysis of protein-coding sequences. Mol Biol Evol. 2006, 23 (1): 7-9. 10.1093/molbev/msj021.View ArticlePubMedGoogle Scholar
- Whelan S, Goldman N: A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol. 2001, 18 (5): 691-699.View ArticlePubMedGoogle Scholar
- Abascal F, Zardoya R, Posada D: ProtTest: Selection of best-fit models of protein evolution. Bioinformatics. 2005, 21: 2104-2105. 10.1093/bioinformatics/bti263.View ArticlePubMedGoogle Scholar
- Guindon S, Gascuel O: A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Syst Biol. 2003, 52 (5): 696-704. 10.1080/10635150390235520.View ArticlePubMedGoogle Scholar
- Kishino H, Hasegawa M: Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in hominoidea. J Mol Evol. 1989, 29 (2): 170-179. 10.1007/BF02100115.View ArticlePubMedGoogle Scholar
- Maddison WP, Maddison DR: Mesquite: a modular system for evolutionary analysis. 2009, Version 2.6, [http://mesquiteproject.org]Google Scholar
- Tsutsui N, Ohira T, Kawazoe I, Takahashi A, Wilder MN: Purification of sinus gland peptides having vitellogenesis-inhibiting activity from the whiteleg shrimp Litopenaeus vannamei. Mar Biotechnol (NY). 2007, 9 (3): 360-369. 10.1007/s10126-006-6151-0.View ArticleGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.