Abstract

Most multicellular organisms reproduce sexually. Where male and female functions are in separate individuals, as in nearly all vertebrates, male and female anatomies diverge at some point during development. In species with parental care of eggs or young, sex-typical anatomy sometimes includes special structures for egg brooding or provisioning of young, as is the case for pregnancy pouches of male seahorses or crop milk in pigeons. Finding the mechanisms responsible for the development of sex differences in sexual and parental anatomy is a classic problem in reproductive endocrinology. Much research points to an important distinction between sextypical characters that are established early in development, well before sexual maturity, such as the scrotum of many male mammals, and those that arise at sexual maturity, such as human female breasts. Combinations are also possible, in which the structure undergoes sexual differentiation early and then later on is enlarged by the hormonal changes of sexual maturity, such as the uterus of female mammals. Invertebrates, especially arthropods, have been a source of some interesting discoveries about the endocrinology of sex differences. Invertebrate gonads do not always serve dual gamete and endocrine functions like vertebrate gonads do, and instead, hormones involved in sexual differentiation are often extragonadal. In several kinds of crustaceans, including some shrimp and crayfish, insulin-like peptide hormones from the androgenic glands (separate glands from the testes) have been shown to be responsible for male morphology and to suppress female characters (1). This has been taken to indicate that the female phenotype is the “default,” for which no feminizing hormone is required. In nature, Armadillidium (isopod “pillbugs” or woodlice) infested with parasitic Wolbachia bacteria that destroy the androgenic gland undergo complete sex reversal, gonads and all, from male to female, but normal males can tell the difference and prefer to mate with “real” females (2). In insects such as Drosophila, sexual differentiation is not hormonal at all and instead is based on cell-autonomous molecular pathways. Yet some of the most familiar arthropods are poorly understood with respect to the development of sex-typical characters, nor are parental characters adequately represented. Enter the blue crab (Callinectes sapidus), the subject of a new paper by Zmora and Chung (3). Blue crabs live along the entire Atlantic coast and around the Gulf of Mexico and throughout their range are a highly sought after food item. (Their scientific name means “beautiful savory swimmer.”) There are millions in the Chesapeake Bay, where they are an iconic species in the ecology, history, economy, and culture of the region and where the authors’ research facility is located. Female blue crabs have a fascinating reproductive strategy. They mate only once, at the time of the pubertalterminal molt, but thanks to prolonged sperm storage, they can produce multiple batches of fertilized eggs over their lifespan of up to 3 years. Each batch of up to 2 million fertilized eggs and embryos is carried for about 2 weeks underneath an abdominal cover (see Ref. 3 and figure 5 therein). Carrying and brooding is a fitness-enhancing but probably relatively low-cost form of parental care seen in a variety of crustaceans and other arthropods. Female blue crabs have an external anatomy specialized for brooding. Their semicircular abdominal cover is shaped differently than the males’ long and narrow cover, allowing the sexes to be easily distinguished. In local lore, the male’s “apron” is the Washington Monument, and the female’s is the Capitol dome (4). Inside the mature female’s abdominal cover is the egg attachment system, consisting of a large number of hair-like ovigerous setae, plus a pair of gonopores for

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