Intersexuality in aquatic invertebrates: Prevalence and causes

This review is the first assembling information on intersexuality in aquatic invertebrates, from freshwater to estuarine and marine environments. Intersex is a condition whereby an individual of a gonochorist (separate sexes) species has oocytes or distinct stages of spermatogonia, at varying degrees of development, within the normal gonad of the opposite gender (i.e. spermatocytes in the ovary or oocytes in the testis), often involving alterations in the gonadal structure, reproductive tract or external genitalia. By the end of 2016 we found approximately 340 records of aquatic invertebrate species evidencing signs of intersexuality (or imposex), all comprised within the Phyla Mollusca and Arthropoda. Gastropod molluscs are by far the group with more examples documented (256 species), followed by crustaceans, i.e., decapods, copepods and amphipods. To our knowledge no further cases of intersexuality were known concerning other invertebrate taxa. Despite some reports suggesting that a baseline level of intersexuality may occur naturally in some populations, the causes are multifaceted and mostly linked with environmental contamination by estrogenic and organotin endocrine disrupting chemicals (EDCs), parasitism, and genetic/environmental sex determination abnormalities. A more comprehensive discussion about the origin of intersexuality, prevalence and causes, knowledge gaps and future research directions in the light of new omics scientific advances (genomics, proteomics and transcriptomics) is also provided. The lack of studies linking molecular responses of invertebrate intersex individuals to multiple stressors represents a true challenge to be further investigated in the future.