IntroductionA huge diversity of marine species reproduce by synchronously spawning their gametes into the water column. Although this species-specific event typically occurs in a particular season, the precise time and day of spawning often can not be predicted. There is little understanding of how the environment (e.g. water temperature, day length, tidal and lunar cycle) regulates a population’s reproductive physiology to synchronise a spawning event. The Indo-Pacific tropical abalone, Haliotis asinina, has a highly predictable spawning cycle, where individuals release gametes on the evenings of spring high tides on new and full moons during the warmer half of the year. These calculable spawning events uniquely allow for the analysis of the molecular and cellular processes underlying reproduction. Here we characterise neuropeptides produced in H. asinina ganglia that are known in egg-laying molluscs to control vital aspects of reproduction.ResultsWe demonstrate that genes encoding APGWamide, myomodulin, the putative proctolin homologue whitnin, FMRFamide, a schistosomin-like peptide (SLP), a molluscan insulin-related peptide (MIP) and a haliotid growth-associated peptide (HGAP) all are differentially expressed in the anterior ganglia during the two week spawning cycle in both male and female abalone. Each gene has a unique and sex-specific expression profile. Despite these differences, expression levels in most of the genes peak at or within 12 h of the spawning event. In contrast, lowest levels of transcript abundance typically occurs 36 h before and 24 h after spawning, with differences in peak and low expression levels being most pronounced in genes orthologous to known molluscan reproduction neuromodulators.ConclusionsExploiting the predictable semi-lunar spawning cycle of the gastropod H. asinina, we have identified a suite of evolutionarily-conserved, mollusc-specific and rapidly-evolving neuropeptides that appear to contribute to the regulation of spawning. Dramatic increases and decreases in ganglionic neuropeptide expression levels from 36 h before to 24 h after the broadcast spawning event are consistent with these peptides having a regulatory role in translating environmental signals experienced by a population into a synchronous physiological output, in this case, the release of gametes.
Living in groups is a widespread phenomenon in the animal kingdom. For free-spawning aquatic animals, such as the abalone (Haliotis), being in the close proximity to potential mating partners enhances reproductive success. In this study, we investigated whether chemical cues could be present in abalone mucus that enable species-specific aggregation. A comparative MS analysis of mucus obtained from trailing or fixed stationary Haliotis asinina, and from seawater surrounding aggregations, indicated that water-soluble biomolecules are present and that these can stimulate sensory activity in conspecifics. Purified extracts of trail mucus contain at least three small proteins [termed H. asinina mucus-associated proteins (Has-MAPs)-1-3], which readily diffuse into the surrounding seawater and evoke a robust cephalic tentacle response in conspecifics. Mature Has-MAP-1 is approximately 9.9 kDa in size, and has a glycine-rich N-terminal region. Has-MAP-2 is approximately 6.2 kDa in size, and has similarities to schistosomin, a protein that is known to play a role in mollusc reproduction. The mature Has-MAP-3 is approximately 12.5 kDa in size, and could only be identified within trail mucus of animals outside of the reproductive season. All three Has-MAP genes are expressed at high levels within secretory cells of the juvenile abalone posterior pedal gland, consistent with a role in scent marking. We infer from these results that abalone mucus-associated proteins are candidate chemical cues that could provide informational cues to conspecifics living in close proximity and, given their apparent stability and hydrophilicity, animals further afield.
Prohormone convertase 2 (PC2) belongs to a family of enzymes involved in the proteolytic maturation of neuropeptide precursors into mature peptides that act as neurotransmitters, neuromodulators or neurohormones. Here we show that a gene encoding a PC2-like enzyme (HasPC2) is expressed during larval development and in the adult ganglia of the vetigastropod Haliotis asinina. HasPC2 exhibits high sequence identity to other gastropod PC2s and thus is likely to function in peptide processing. Analysis of HasPC2 expression indicates that it is activated early in nervous system development. During trochophore and early veliger larval stages, HasPC2 is expressed in the vicinity of the forming ganglia of the central nervous system and parts of the putative peripheral nervous system. Later in larval development, at the time the veliger becomes competent to interact with the external environment and initiate metamorphosis, HasPC2 expression largely restricts to cells of the major ganglia and their commissures. Profiling of veliger larvae by bioinformatic approaches suggests the expression of a variety of peptides. Direct MALDI-MS-based peptide profiling of juvenile Haliotis cerebral ganglia (brain) reveals an abundance of neuropeptides, including FMRFamide-related peptides and APGWamide, compatible with PC2 functioning in neuropeptide processing in these regions. These results are consistent with PC2 regulating neuropeptide generation in the earliest functioning of the gastropod nervous system. KEY WORDS: prohormone convertase, abalone, neuropeptide, developmentNeuropeptides are widespread in the animal kingdom and are often involved in the control of critical functions throughout the life cycle. The regulation of development by peptidergic hormones is a common feature of multicellular animals and has been studied in great detail in arthropods and vertebrates. Strikingly, investigations reveal that insects are as well or even better supplied with neuropeptides than mammals. In insects, neuropeptides regulate not only the functioning of endocrine glands, but also a wide range of physiological and developmental processes (Reumer et al., 2008). Although a complete developmental peptidome analysis has not been established for other major invertebrate groups, such as the molluscs, numerous immunolocalization studies suggest that neuropeptides are equally important for their development. For instance, in gastropods FMRFamide and related peptides are amongst the earliest neurotransmitters expressed Int. J. Dev. Biol. 53: 1081-1088 (2009) Abbreviations used in this paper: DIG, digoxigenin; MALDI-MS, matrix-assisted laser desorption/ionization MS; PBS, phosphate-buffered solution; PC, prohormone convertase; RACE, rapid amplification of cDNA ends; WMISH, whole-mount in situ hybridization.within the larval nervous system (Croll and Voronezhskaya, 1996;Dickinson et al., 1999; Dickinson et al., 2000;Haszprunar et al., 2002;Dickinson and Croll, 2003; Croll, 2006). In the adult stages of these same animals, neuropeptides pl...
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