Nonspecific expression of fertilization genes in the crown‐of‐thorns Acanthaster cf. solaris: Unexpected evidence of hermaphroditism in a coral reef predator

Abstract

The characterization of gene expression in gametes has advanced our understanding of the molecular basis for ecological variation in reproductive success and the evolution of reproductive isolation. These advances are especially significant for ecologically important keystone predators such as the coral‐eating crown‐of‐thorns sea stars (COTS, Acanthaster) which are the most influential predator species in Indo‐Pacific coral reef ecosystems and the focus of intensive management efforts. We used RNA‐seq and transcriptome assemblies to characterize the expression of genes in mature COTS gonads. We described the sequence and domain organization of eight genes with sex‐specific expression and well known functions in fertilization in other echinoderms. We found unexpected expression of genes in one ovary transcriptome that are characteristic of males and sperm, including genes that encode the sperm‐specific guanylate cyclase receptor for an egg pheromone, and the sperm acrosomal protein bindin. In a reassembly of previously published RNA‐seq data from COTS testes, we found a complementary pattern: strong expression of four genes that are otherwise well known to encode egg‐specific fertilization proteins, including the egg receptor for bindin (EBR1) and the acrosome reaction‐inducing substance in the egg coat (ARIS1, ARIS2, ARIS3). We also found histological evidence of both eggs and sperm developing in the same gonad in several COTS individuals from a parallel study. These results suggest the occurrence of hermaphrodites, and the potential for reproductive assurance via self‐fertilization. Our findings have implications for management of COTS populations, especially in consideration of the large size and massive fecundity of these sea stars.

Selection on genes associated with the evolution of divergent life histories: Gamete recognition or something else?

“…The PCA confirmed that each individual clustered with its corresponding group, either the hermaphroditic C. hystera , or the gonochoric C. pentagona males or C. pentagona females (Figure 2). The expression of GRGs (Table ) was consistent with that result and with the gonad types of each individual: hermaphroditic gonads of C. hystera showed expression of GRGs that are characteristic of both sperm and eggs; and the gonochoric testes or ovaries of C. pentagona showed expression of either sperm‐ or egg‐specific GRGs but not both (for a counterexample see Guerra et al, 2020). Information on the differential expression analysis and polymorphism is found in the supplement (Tables and and Figure ).…”

“…It remains possible that new GRGs not previously described and not analyzed in this study, including GRGs created through the process of neofunctionalization, may have participated in that speciation event. In particular, the binding region of REJ1 is expected to interact with the ARIS protein complex in the egg coat, but ARIS1 , ARIS2 , and ARIS3 (which are abundantly expressed in other sea star oocytes; Guerra et al, 2020; Hart & Foster, 2013) are not expressed in Cryptasterina ovaries. This gap in evidence suggests that ARIS genes in Cryptasterina have diverged so strongly from those of other sea stars that they cannot be recognized by sequence‐similarity searches using BLAST, or that the function of the ARIS proteins in the egg coat has been replaced by neofunctionalization of other genes.…”

The hidden army: corallivorous crown-of-thorns seastars can spend years as herbivorous juveniles

“…The resilience of the herbivorous juvenile COTS to coral scarcity adds to the suite of remarkable traits that may contribute to its boom-bust dynamics. Larval plasticity is seen in cloning and body form and potential nutritive augmentation from a phototropic microbiome to dissolved organic matter [29][30][31][32], and some adults may be hermaphrodites [33]. That the herbivorous phase has the potential to accumulate in the reef infrastructure for years to seed an outbreak should be considered alongside the current larva-centric model of COTS outbreaks.…”

Integrated Population Genomic Analysis and Numerical Simulation to Estimate Larval Dispersal of Acanthaster cf. solaris Between Ogasawara and Other Japanese Regions

“…In the present study, we found three pairs of individuals in Ogasawara population were possible clonal or genetically very close individual (Table 1 and Supplementary Figure 2). It is also notable that we also found one pair of possible clonemates in Tatsukushi population where previous study found hermaphrodites (Guerra et al, 2020). Although we need more precise analysis to identify true clonemates, it is possible that inbreeding including self-fertilization or larval cloning also partly facilitated the initiation of population outbreak in the oceanographically isolated Ogasawara populations.…”

“…Recently, self-fertilization and/or clonal propagation hypothesis has been proposed by Guerra et al (2020) to explain the cause of primary outbreak as evidenced by the existence of hermaphrodites and the finding of possible larval cloning of A. cf. solaris (Allen et al, 2019).…”