J. Antonio Baeza

SEX ALLOCATION IN A SIMULTANEOUSLY HERMAPHRODITIC MARINE SHRIMP

Abstract Two fundamental questions dealing with simultaneous hermaphrodites are how resources are optimally allocated to the male and female function and what conditions determine shifts in optimal sex allocation with age or size. In this study, I explored multiple factors that theoretically affect fitness gain curves (that depict the relationship between sex-specific investment and fitness gains) to predict and test the overall and size-dependent sex allocation in a simultaneously hermaphroditic brooding shrimp with an early male phase. In Lysmata wurdemanni, sperm competition is absent as hermaphrodites reproducing in the female role invariably mated only once with a single other shrimp. Shrimps acting as females preferred small over large shrimps as male mating partners, male mating ability was greater for small compared to large hermaphrodites, and adolescent males were predominant in the population during the breeding season. In addition, brooding constraints were not severe and varied linearly with body size whereas the ability to acquire resources increased markedly with body size. Using sex allocation theory as a framework, the findings above permitted to infer the shape of the male and female fitness gain curves for the hermaphrodites. The absence of sperm competition and the almost unconstrained brooding capacity imply that both curves saturate, however the male curve levels off much more quickly than the female curve with increasing level of investment. In turn, the predominance of adolescent males in the population implies that the absolute gain of the female curve is greater than that of the male curve. Last, the size-dependent female preference and male mating ability of hermaphrodites determines that the absolute gain of the male curve is greater for small than for large hermaphrodites. Taking into consideration the inferred shape of the fitness gain curves, two predictions with respect to the optimal sex allocation were formulated. First, overall sex allocation should be female biased; it permits hermaphrodites to profit from the female function that provides a greater fitness return than the male function. Second, sex allocation should be size-dependent with smaller hermaphrodites allocating more than proportionally resources to male reproduction than larger ones. This size-dependent sex allocation permits hermaphrodites to profit from male mating opportunities that are the greatest at small body sizes. Size-dependent sex allocation is also expected because the male fitness gain curve decelerates more quickly than the female gain curve and experiments indicated that resources are greater for large than small hermaphrodites. These two predictions were tested when determining the sex allocation of hermaphrodites by dissecting their gonad and quantifying ovaries versus testes mass. Supporting the predictions above, hermaphrodites allocated, on average, 118 times more to the female than to the male gonad and the proportion of resources devoted to male function was higher in small than in large hermaphrodites. A trade-off between male and female allocation is assumed by theory but no negative correlation between male and female reproductive investment was observed. In L. wurdemanni, the relationship between sex-specific investment and fitness changes during ontogeny in a way that is consistent with an adjustment of sex allocation to improve size-specific reproductive success.

The symbiotic lifestyle and its evolutionary consequences: Social monogamy and sex allocation in the hermaphroditic shrimp Lysmata pederseni

Sex allocation theory predicts female-biased sex allocation for simultaneous hermaphrodites with a monogamous mating system. Mating systems theory predicts that monogamy is advantageous in environments where refuges are discrete, scarce, relatively small, and when predation risk is high outside of these refuges. These predictions were tested with the Caribbean shrimp Lysmata pederseni, a simultaneous hermaphrodite which has an early male phase and lives inside tubes of the sponge Callyspongia vaginalis. This host sponge is a scarce resource that, together with the high predation risk typical of tropical environments, should favor monogamy in the shrimp. Field observations demonstrated that shrimps were frequently encountered as pairs within these tube sponges. Pairs were equally likely to comprise two hermaphrodites or one hermaphrodite and one male. Several of these pairs were observed for long periods of time in the field. Experiments demonstrated that hermaphrodites tolerated other hermaphrodites but not males in their host sponge. These results suggest that pairs of hermaphroditic L. pederseni are socially monogamous; they share the same host individual and might reproduce exclusively with their host partners for long periods of time. Nevertheless, males appeared less likely to establish long-term associations with hermaphrodites as indicated by the rate of their disappearance from their hosts (greater than that of hermaphrodites). Sex allocation was female biased in monogamous hermaphrodites. On average, hermaphrodites invested 34 times more to female than to male reproductive structures. Monogamy and female-biased sex allocation seem to be evolutionary consequences of adopting a symbiotic lifestyle in simultaneous hermaphrodites.

LYSMATA HOCHI N. SP., A NEW HERMAPHRODITIC SHRIMP FROM THE SOUTHWESTERN CARIBBEAN SEA (CARIDEA: HIPPOLYTIDAE).

Abstract Lysmata hochi n. sp., a new peppermint shrimp, is described from Bocas del Toro, Caribbean coast of Panama. All individuals were collected on near-shore fossil coral terraces with deep channels and caves, sparsely covered with seagrass. Besides the type locality, L. hochi n. sp. also occurs in Cahuita, Costa Rica, in a similar type of habitat. The new species can be distinguished from other species of Lysmata by the presence of an unguis-shaped accessory branch on the lateral antennular flagellum; the rostrum with three dorsal teeth, followed by two mid-dorsal teeth on the carapace posterior to the orbital margin; the number of carpal segments of the second pereiopod ranging from 21 to 24; the presence of two to four ventrolateral spines on the merus of the third pereiopod; the dactylus of the third to fifth pereiopod bearing two spines in addition to a bifurcated inguis; and the conspicuous color pattern, especially the irregular bright red bands on the pleon. Based on morphology and (where known) color patterns, L. hochi n. sp. appears to be most closely related to the Indo-West Pacific L. kuekenthali (De Man) and the eastern Atlantic L. uncicornis Holthuis and Maurin. Anatomical observations, field population studies and laboratory experiments indicate that L. hochi n. sp. is a protandric simultaneous hermaphrodite, with a primary male phase followed by a simultaneous hermaphrodite phase.

Protandric Simultaneous Hermaphroditism in Parhippolyte misticia (Clark, 1989) (Caridea: Hippolytidae): Implications for the Evolution of Mixed Sexual Systems in Shrimp

ABSTRACT The sexual system of the shrimp Parhippolyte misticia (Clark, 1989), inhabiting the rocky subtidal at Okinawa, Japan and Kimbe Bay, Papua New Guinea, was examined. Dissections suggested that the population consisted of male phase (MP) and functional simultaneous euhermaphrodite (EH) individuals. MPs 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 containing sperm, but an undeveloped female portion. EHs lacked appendices masculinae and cincinulli. However, they have male gonopores and ovotestes with well-developed ovaries containing mature oöcytes and testes with sperm. When EHs were maintained in pairs, both shrimp molted and spawned eggs which attached below the pleon and developed as embryos, demonstrating that EHs can reproduce as males and inseminate other EHs acting as females. These results demonstrate that P. misticia is a protandric simultaneous hermaphrodite, as reported before for other shrimp of the genera Lysmata and Exhippolysmata. Also, these results suggest that protandric simultaneous hermaphroditism might have evolved more than once independently in shrimp from the diverse and species-rich Infraorder Caridea. Future research aimed at disentangling the phylogenetic relationship of Parhippolyte, Lysmata, Exhippolysmata and other closely related genera (Calliasmata, Lysmatella, Barbouria) and describing the sociobiology of additional representatives from the genera above is needed to understand the evolutionary history of sexual systems in caridean shrimp.

No effect of group size on sex allocation in a protandric-simultaneous hermaphroditic shrimp

Lysmata wurdemanni is a protandric-simultaneous hermaphroditic shrimp. Individuals reproduce as males first and late in life as simultaneous hermaphrodites. I examined whether sex allocation (resources devoted to ova vs sperm) varies with group size in shrimps that have just matured as hermaphrodites. Focal males were reared with different numbers of hermaphrodites (1, 2, 5 or 10). Sperm stored in the ejaculatory ducts and eggs brooded underneath the abdomen were retrieved and weighted immediately after focal shrimps matured as hermaphrodites. Hermaphrodites should invest more into sperm with increasing group size to cope with more intense sperm competition. The proportion of focal shrimps that lost their first clutch of eggs after maturing as hermaphrodites increased with group size. This suggests male gender preferences by hermaphrodites experiencing large group sizes. No differences in sex allocation among group sizes were recorded for shrimps that did not lose their first clutch of eggs. Thus, group size does not affect sex allocation in terms of ova and sperm mass. This lack of phenotypic plasticity might be explained if sperm competition is not important in L. wurdemanni . It should not pay in terms of fitness for shrimps to produce and inseminate female-role hermaphrodites with large amounts of sperm when full paternity is assured in the absence of multi-male mating. In agreement with this idea, a second experiment demonstrated that female-role hermaphrodites invariably mated only once with a single other shrimp.

Molecular phylogeny of enigmatic Caribbean spider crabs from the Mithrax–Mithraculus species complex (Brachyura: Majidae: Mithracinae): ecological diversity and a formal test of genera monophyly

STRI ; Marine biology ; Understanding and Sustaining a Biodiverse Planet ; forces of Change

Sexual Dimorphism, Allometry, and Size at First Maturity of the Caribbean King Crab, Mithrax spinosissimus, in the Florida Keys

ABSTRACT The Caribbean King crab Mithrax spinosissimus is the largest brachyuran found in the western Atlantic and it supports subsistence and small commercial fisheries throughout the Caribbean and Gulf of Mexico. Because of its short larval duration and rapid growth, M. spinosissimus is considered a good candidate for aquaculture. Our study documents for the first time the size at sexual maturity, sexual dimorphism, and allometric growth relative to carapace width for certain secondary sexual characters in male and female M. spinosissimus from the Florida Keys, Florida. Using principal component analysis, K-means cluster analysis, and discriminant analysis, we identified 2 major growth phases in the postlarval benthic life of this species (juvenile or prepubertal and adult or pubertal). The typical growth pattern for majoid crabs includes a third, intermediate growth phase that appears absent in M. spinosissimus. The major cheliped of males was larger than that of females and exhibited positive allometric growth to maturity, after which the level of allometry decreased. In females, both chelipeds exhibited positive allometry throughout ontogeny. Abdominal width was negatively allometric throughout ontogeny in males, whereas in females the abdomen exhibited positive allometric growth until reproductive maturity, at which point it became isometric. Logistic regression indicated that the carapace width at first maturity was 45.2 mm in males and 69.7 mm in females. This new information should be taken into account when assessing stocks and setting harvest regulations if this fishery is to be managed sustainably.

The sexual and mating system of the shrimp Odontonia katoi (Palaemonidae, Pontoniinae), a symbiotic guest of the ascidian Polycarpa aurata in the Coral Triangle.

Theory predicts that monogamy is adaptive in symbiotic crustaceans inhabiting relatively small and morphologically simple hosts in tropical environments where predation risk away from hosts is high. We tested this prediction in the shrimp Odontonia katoi, which inhabits the atrial chamber of the ascidian Polycarpa aurata in the Coral Triangle. Preliminary observations in O. katoi indicated that males were smaller than females, which is suggestive of sex change (protandry) in some symbiotic organisms. Thus, we first investigated the sexual system of O. katoi to determine if this shrimp was sequentially hermaphroditic. Morphological identification and size frequency distributions indicated that the population comprised males that, on average, were smaller than females. Gonad dissections demonstrated the absence of transitional individuals. Thus, O. katoi is a gonochoric species with reverse sexual dimorphism. The population distribution of O. katoi in its ascidian host did not differ significantly from a random distribution and shrimps inhabiting the same host individual as pairs were found with a frequency similar to that expected by chance alone. This is in contrast to that reported for other socially monogamous crustaceans in which pairs of heterosexual conspecifics are found in host individuals more frequently than expected by chance alone. Thus, the available information argues against monogamy in O. katoi. Furthermore, that a high frequency of solitary females were found brooding embryos and that the sex ratio was skewed toward females suggests that males might be roaming among hosts in search of receptive females in O. katoi. Symbiotic crustaceans can be used as a model system to understand the adaptive value of sexual and mating systems in marine invertebrates.

Territoriality and Conflict Avoidance Explain Asociality (Solitariness) of the Endosymbiotic Pea Crab Tunicotheres moseri.

Host monopolization theory predicts symbiotic organisms inhabiting morphologically simple, relatively small and scarce hosts to live solitarily as a result of territorial behaviors. We tested this prediction with Tunicotheres moseri, an endosymbiotic crab dwelling in the atrial chamber of the morphologically simple, small, and relatively scarce ascidian Styela plicata. As predicted, natural populations of T. moseri inhabit ascidian hosts solitarily with greater frequency than expected by chance alone. Furthermore, laboratory experiments demonstrated that intruder crabs take significantly longer to colonize previously infected compared to uninfected hosts, indicating as expected, that resident crabs exhibit monopolization behaviors. While territoriality does occur, agonistic behaviors employed by T. moseri do not mirror the overt behaviors commonly reported for other territorial crustaceans. Documented double and triple cohabitations in the field coupled with laboratory observations demonstrating the almost invariable success of intruder crabs colonizing occupied hosts, suggest that territoriality is ineffective in completely explaining the solitary social habit of this species. Additional experiments showed that T. moseri juveniles and adults, when searching for ascidians use chemical cues to avoid hosts occupied by conspecifics. This conspecific avoidance behavior reported herein is a novel strategy most likely employed to preemptively resolve costly territorial conflicts. In general, this study supports predictions central to host monopolization theory, but also implies that alternative behavioral strategies (i.e., conflict avoidance) may be more important than originally thought in explaining the host use pattern of symbiotic organisms.

A test of large-scale reproductive migration in females of the amphidromous shrimp Macrobrachium acanthurus (Caridea : Palaemonidae) from south-eastern Brazil

Macrobrachium acanthurus inhabits estuaries and rivers in the western Atlantic. It is not clear whether females migrate towards estuaries to hatch larvae, as reported for other congeneric shrimps. We tested whether females of M. acanthurus exhibit reproductive migrations. The population dynamics of this shrimp was studied in the Ribeira de Iguape River, Brazil. Four sites that differ in position with respect to the coast were sampled monthly during 2007. In M. acanthurus, reproduction was seasonal and reproductive intensity did not vary among study sites. Females brooding early and late embryos were found at all study sites during the reproductive season. No disappearance of reproductive females was observed at the study site located furthest away (~150 km) from the coast. Thus, reproductive females of M. acanthurus do not exhibit reproductive migrations towards estuaries to hatch larvae. Maturity in females was reached at smaller body sizes during the austral summer and spring compared with winter and autumn. Growth rate and body size was sex-specific; males grew slower but attained larger average and final body sizes than females. This information needs to be considered in assessing stocks and establishing sustainable management plans for M. acanthurus in Brazil.