Protandric simultaneous hermaphroditism in the shrimps Lysmata bahia and Lysmata intermedia

The sexual system of two peppermint shrimps, Lysmata bahia and Lysmata intermedia, inhabiting intertidal fossil coral terraces at Bocas del Toro, on the Caribbean coast of Panama, was examined. Dissections suggested that the population of each species consisted of functional males and functional simultaneous hermaphrodites. Males have cincinulli and appendices masculinae on the first and second pair of pleopods, respectively, gonopores located at the coxae of the third pair of walking legs, and ovotestes with a well-developed male portion full of sperm, but an undeveloped female portion. Hermaphrodites lacked appendices masculinae and cincinulli. However, they have male gonopores and ovotestes with well-developed ovaries full of mature oocytes and testes with sperm. When hermaphrodites were maintained in pairs, both molted and spawned eggs (to beneath abdomen) that continued developing after 3 d, demonstrating that hermaphrodites can reproduce as males and inseminate other hermaphrodites acting as females. The possibility of self-fertilization or parthenogenetic reproduction was tested and disregarded, because hermaphrodites reared in isolation spawned oocytes that failed to develop, disappearing from the abdomen after 2 d. Males reared in pairs mature as hermaphrodites in o50 d, showing the ability of males to mature as hermaphrodites. These results demonstrate that L. bahia and L. intermedia are protandric simultaneous hermaphrodites, as reported for all species of this genus whose sexual system has been examined. However, the studied species featured a lifestyle, termed ‘‘tropical-low abundance,’’ here not recognized previously for the genus; they occur in low abundances in tropical environments, they do not develop symbiotic associations with sessile invertebrates, and they are not conspicuously colored. Information on the sexual systems and lifestyles of more species needs to be examined before these observations can be placed into a comparative context within the genus. Additional key words: hermaphrodite, protandry, sex allocation, Crustacea, Hippolytidae Sexual systems vary considerably among caridean shrimps. Most species appear to be gonochoric, with individuals in a population reproducing either as a male or as a female during their entire life (e.g., many shrimps from the diverse family Alpheidae: Correa & Thiel 2003; Bauer 2004). Other species are sequential protandric hermaphrodites, with individuals consistently maturing and reproducing first as males to then, later in life, change sex to females (e.g., various species of Pandalus: Butler 1964, 1980). Although several variants of protandry have been described (see reviews by Bauer 2000; Correa & Thiel 2003), no study has reported protogyny (female first) among caridean shrimps. Lastly, a particular form of simultaneous hermaphroditism (adolescent protandry sensu Ghiselin 1974, protandric cosexuality sensu Policansky 1982, or protandric simultaneous hermaphroditism sensu Bauer 2000) has been described recently for shrimps from the genus Lysmata (Wirtz 1997; Fiedler 1998; Bauer & Holt 1998; d’Acoz 2003; Bauer & Newman 2004). In protandric simultaneous hermaphrodites, juvenile shrimps invariably mature and reproduce as males. These males have typical caridean male external characters, including gonopores located at the coxae of the third pair of walking legs (pereiopods), cincinulli (coupling hooks) on the endopod of the first pair of pleopods (abdominal swimming Invertebrate Biology 127(2): 181–188. r 2008, The Authors Journal compilation r 2008, The American Microscopical Society, Inc. DOI: 10.1111/j.1744-7410.2007.00122.x Author for correspondence. E-mail: [email protected] appendages), and appendices masculinae on the endopods of the second pair of pleopods (Bauer & Holt 1998). Males are capable of reproducing only as males, although their gonads are ovotestes with an undeveloped ovarian portion (Bauer & Holt 1998). Later in life, males attain the female sexual function, developing into functional simultaneous hermaphrodites (Baeza 2007). Externally, these hermaphrodites resemble females of gonochoric shrimp species, having female gonopores on the coxae of the third pair of walking legs, expanded flanges on the basipod of the pleopods, and well-developed lateral abdominal plates that form an abdominal chamber in which embryos are brooded (Höglund 1943). Although simultaneous hermaphrodites lose the appendices masculinae and cincinulli, they retain testicular tissue, male ducts, and gonopores, and thus have the ability to reproduce as both males and females (Bauer & Holt 1998). After becoming hermaphrodites, individuals do not revert to their initial sexual condition (Baeza 2007) and no self-fertilization has been observed (Bauer & Holt 1998; Baeza & Anker 2008). So far, the various studies on the sexual biology of shrimps from the genus Lysmata suggest that all the species are simultaneous hermaphrodites with an early male phase (Lysmata grabhami GORDON 1935 (Wirtz 1997): Lysmata amboinensis DE MANN 1888 (Fiedler 1998); Lysmata wurdemanni GIBBES 1850 (Bauer & Holt 1998); Lysmata seticaudata RISSO 1816 and Lysmata nitida DOHRN & HOLTHUIS 1950 (d’Acoz 2003); Lysmata californica STIMPSON 1866 (Bauer & Newman 2004); and Lysmata hochi BAEZA & ANKER 2008 (Baeza & Anker 2008). While this sexual system does not vary within the genus, other life-history features do differ. For instance, two distinct lifestyles have been recognized (‘‘crowd’’ and ‘‘pair’’ species sensu Bauer 2000). ‘‘Crowd’’ species mostly occur in warm temperate environments, inhabit refuges (e.g., rocky crevices and caves) as dense aggregations, and do not exhibit any specialized fishcleaning behavior (i.e., L. californica: Bauer & Newman 2004; and L. wurdemanni: Baeza 2006). ‘‘Pair’’ species are mostly tropical, occur at low densities in the subtidal, and dwell as socially monogamous pairs on hosts, usually sea anemones, which are used as vantage points for cleaning fish clients attracted by colorful displays and specialized behaviors (i.e., L. grabhami: Wirtz 1997; L. amboinensis: Fiedler 1998; see Bauer 2000). Taking this diversity of lifestyles into consideration, Bauer (2000) proposed a historical contingency hypothesis to explain the evolution of protandric simultaneous hermaphroditism in Lysmata. According to this author, protandric simultaneous hermaphroditism evolved in a strictly protandric tropical species of Lysmata that became a specialized fish cleaner. Restricted mobility of individuals due to their association with the host, and hence, reduced probability of encountering mating partners, would have favored simultaneous hermaphroditism over protandry or gonochorism (Bauer 2000). In this scenario, the ‘‘crowd’’ warm-temperate species that do not exhibit specialized cleaning behaviors would have evolved from tropical species with specialized cleaning behaviors andmore complex mating systems. The evolution of these simple characters from more complex ones appeared unlikely to Bauer (2000). Overall, studies on the reproductive biology, life history, and ecology of several other species of Lysmata should improve our understanding of the conditions that in the past favored protandric simultaneous hermaphroditism in the genus. In this study, I demonstrate, through a series of anatomical observations and experiments, that two tropical shrimps, Lysmata intermedia KINGSLEY 1878 and Lysmata bahia RHYNE & LIN 2006, are protandric simultaneous hermaphrodites. Information on their general ecology and life history is provided.