Sex-specific expression of pheromones and other signals in gravid starfish

Abstract

Background Many echinoderms form seasonal aggregations prior to spawning. In some fecund species, a spawning event can lead to population outbreaks with detrimental ecosystem impacts. For instance, outbreaks of crown-of-thorns starfish (COTS), a corallivore, can destroy coral reefs. Here, we examine the gene expression in gravid male and female COTS prior to spawning in the wild, to identify genome-encoded factors that may regulate aggregation and spawning. This study is informed by a previously identified exoproteome that attracts conspecifics. To capture the natural gene expression profiles, we isolated RNAs from gravid female and male COTS immediately after they were removed from the Great Barrier Reef. Results Sexually dimorphic gene expression is present in all seven somatic tissues and organs that we surveyed and in the gonads. Approximately 40% of the exoproteome transcripts are differentially expressed between sexes. Males uniquely upregulate an additional 68 secreted factors in their testes. A suite of neuropeptides in sensory organs, coelomocytes and gonads is differentially expressed between sexes, including the relaxin-like gonad-stimulating peptide and gonadotropin-releasing hormones. Female sensory tentacles—chemosensory organs at the distal tips of the starfish arms—uniquely upregulate diverse receptors and signalling molecules, including chemosensory G-protein-coupled receptors and several neuropeptides, including kisspeptin, SALMFamide and orexin. Conclusions Analysis of 103 tissue/organ transcriptomes from 13 wild COTS has revealed genes that are consistently differentially expressed between gravid females and males and that all tissues surveyed are sexually dimorphic at the molecular level. This finding is consistent with female and male COTS using sex-specific pheromones to regulate reproductive aggregations and synchronised spawning events. These pheromones appear to be received primarily by the sensory tentacles, which express a range of receptors and signalling molecules in a sex-specific manner. Furthermore, coelomocytes and gonads differentially express signalling and regulatory factors that control gametogenesis and spawning in other echinoderms.

Neuropeptide expression and action in the reproductive system of the starfish Asterias rubens

“…Furthermore, given the large number of neuropeptides (>40) that have been identified in A. rubens (Semmens et al, 2016), it is likely that other neuropeptides that remain to be investigated are also expressed in the gonoducts and/or gonads. Consistent with this hypothesis, transcriptomic and mass spectroscopic analysis of the starfish Acanthaster planci has revealed a variety of neuropeptides that are expressed in the gonads, including orthologs of neuropeptides analyzed in this study (SS1-type, PPLN1-type, PPLN2-type, and GnRH-type), and others (e.g., kisspeptin-type, luqin-type, orexin-type, SALMFamide-type, and NGFFYamide) (Jonsson et al, 2022;Smith et al, 2017).…”

Captivity induces a sweeping and sustained genomic response in a starfish

“…or in small (5000 litre) closed aquarium in artificial seawater (coelomocytes)-or (iii) type of RNA-Seq method, whether stranded RNA-Seq (Hall et al, 2017) or CEL-Seq2 (this study). Using the same tissue, and sampling and sequencing methods as described here, we found that these wild-captive differences are more than four times greater than gene expression differences observed between seasons (unpublished) and 173 times greater than between sexes (Jönsson et al, 2022). Only metamorphosis appears to have a similar magnitude of transcriptional change in echinoderms (Wygoda et al, 2014).…”

“…For captive and wild coelomocyte samples (13 and eight biological replicates, respectively), CDS were considered expressed if the average count per condition was ≥0.25 (Jönsson et al, 2022). Using Wald Test statistics in the DESeq2 package (v1.28.1; Love et al, 2014), CDS with an adjusted p ‐value <.05 between treatments were identified as being significantly differentially expressed.…”

“…For captive and wild coelomocyte samples (13 and eight biological replicates, respectively), CDS were considered expressed if the average count per condition was ≥0.25 (Jönsson et al, 2022).…”

Seasonal tissue-specific gene expression reveals reproductive and stress-related transcriptional systems in wild crown-of-thorns starfish

“…Samples with mapped transcripts < 0.5 million were discarded as low-quality [60]. GBR v1.1 gene models and transcriptomes can be visualised at https://apolloportal.genome.edu.au/degnan/cots [28,29].…”