Protandric Simultaneous Hermaphroditism Is a Conserved Trait in Lysmata (Caridea: Lysmatidae): Implications for the Evolution of Hermaphroditism in the Genus J. Antonio Baeza ABSTRACT. Shrimps from the genus Lysmata are unusual because of their peculiar sexual system. Individuals in a population first reproduce as males, to change later in life to functional simultaneous hermaphrodites. The evolutionary origin of this sexual sys- tem ,called protandric simultaneous hermaphroditism (PSH) ,is a longstanding question overdue for consideration. A previously proposed “historical contingency” hypothesis suggested that PSH evolved in the tropics from an ancestral protandric species of Lys- mata that became socially monogamous and symbiotic with sea anemones .The restricted probability of encountering mating partners by shrimps because of their association with their hosts would have favored PSH. Here, I first provide evidence that PSH is a fixed trait within the genus. Second, I examine whether the historical contingency hypothesis appropriately explains the origin of PSH in the genus. Using anatomical observations and laboratory experiments combined, I demonstrate that two shrimps from the genus Lysmata ,L .galapagensis and L .boggessi ,feature PSH .Study of museum specimens sug- gests that nine other species of Lysmata are protandric simultaneous hermaphrodites. The foregoing information indicates that PSH represents a fixed trait in the genus Lys- mata .Ancestra lcharacter state reconstruction using Bayesian inference allowed testing whether the ancestra lLysmata featured a symbiotic lifestyle and a socially monogamous mating system ,as proposed by the historica lcontingency hypothesis .In agreement with this hypothesis ,analysis indicated that the most common recent ancestor of Lysmata was most likely socially monogamous. However, the ancestral lifestyle was equally likely to be free-living or symbiotic. Thus, the present study provides partial support for the his- torica lcontingency hypothesis .Studies on the sexua lsystem and lifestyle of more species and development of a more robust phylogeny are needed to revea lthe evolutionary origin of PSH in the genus Lysmata. INTRODUCTION In decapod crustaceans, the greatest diversity of sexual systems is found in the infraorder Caridea. Most caridean shrimps are gonochoric, with individuals in a population producing only male or female gametes during their entire life. AJ.nton iBoaez aS,mithsonia Tnropic aRlesearch Well-studied examples include Rhynchocinetes typus (Correa et al., 2000), Hip- Institut eP,anam a,n Sdmithsonia Mn arin Seta- polyte obliquimanus (Terossi et al., 2008), Pontonia margarita (Baeza, 2008a), tio na Ft or Pt ierce 7, 0 1Seawa yDrive F, or Pt ierce, and Hippolyte williamsi (Espinoza-Fuenzalida et al., 2008). The second most Florid 3a494 9U,S A(baezaa@si.edu R).eceive 9d common sexual system is protandry. In at least 31 species of shrimps, individu- Jun e2008 a; ccepte d2 0Apr i2l 009. als in a population reproduce first as males and change to females later in life 96 e* SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES (Bauer, 2000). Although several variants of protandry some species are socially monogamous (pair-living; e.g., have been reported (e.g., protandry with primary females L. grabhami (Gordon, 1935)) (Wirtz, 1997). Several spe- in Crangon crangon; Schatte and Saborowski, 2006), no cies with an inconspicuous coloration dwell freely among study has reported protogyny (changing sex from female to rocks in temperate zones, while other more colorful spe- male) among shrimps. Most recently, a particular variant cies inhabit tropical sponges (L. pederseni Rhyne and Lin, of simultaneous hermaphroditism, that is, adolescent pro- 2006) (Rhyne and Lin, 2006). Other strikingly brilliant tandry sensu Ghiselin (1974), protandric cosexuality sensu species clean fishes (L. amboinensis (De Man, 1888)) Policansky (1982), or protandric simultaneous hermaph- (Limbaugh et al., 1961). Species from this genus represent roditism (PSH) sensu Bauer (2000), has been described for ideal candidates to explore the role of ecological condi- shrimps from the genera Lysmata (Baeza et al., 2008) and tions in explaining evolutionary innovations in the marine Exhippolysmata (Kagwade, 1982; Braga et al., 2009). It environment (see Baeza and Thiel, 2007). must be noticed that a recently developed molecular phy- Recent studies have examined various aspects of the logeny for Lysmata and other related genera demonstrated biology of various Lysmata and Exhippolysmata shrimps that the genus Exhippolysmata represents a derived group (Baeza, 2008b; Baeza and Anker, 2008; Baeza et al., 2008; of shrimps within the genus Lysmata (Baeza et al., 2009). Lopez-Greco et al., 2009). Furthermore, shrimps from the Thus, species of Exhippolysmata are treated here as mem- genera Lysmata and Exhippolysmata are currently being bers of the genus Lysmata. used as models in evolutionary biology and behavioral In protandric simultaneous hermaphroditic shrimps, ecology because of their peculiar sexual system (Baeza and juveniles consistently mature as functional male individu- Bauer, 2004; Baeza, 2006, 2007a, 2007b, 2007c). In spite als (also called male-phase [MP] shrimps; Bauer and Holt, of the increasing knowledge regarding the behavior and 1998) bearing typical caridean male characters (1.e., cou- ecology of several species of Lysmata, the evolutionary pling hoods and appendix masculina on the first and sec- origins of PSH in the genus remain uncertain. Although ond pleopods, respectively) (Bauer and Holt, 1998; Baeza, recent studies have shown that the variety of lifestyles 2008b; Baeza and Anker, 2008; Baeza et al., 2008). These of Lysmata is greater than originally recognized (Baeza, functional males later attain female sexual function and 2008b; Baeza and Anker, 2008; Baeza et al., 2008), an develop into functional simultaneous hermaphrodites emerging dichotomy in social organization and ecology (hereafter, hermaphrodites; but also called female-phase was noted in initial studies. One group of species (named [FP] shrimps; Bauer and Holt, 1998). Resembling females “Crowd” species by Bauer, 2000) was described as inhab- of caridean gonochoric species, hermaphrodites mate as iting warm subtropical environments, occurring as dense females shortly after molting, spawn oocytes to an abdom- aggregations in their refuges, and exhibiting no specialized inal chamber where fertilization takes place, and brood fish-cleaning behavior (i.e., L. californica: Bauer and New- their embryos for relatively long periods of time (e.g., man, 2004; L. wurdemanni: Baeza, 2006). A second group 10-15 days in Lysmata wurdemanni; Baeza, 2006). These (named “Pair” species by Bauer, 2000) was described as hermaphrodites retain testicular tissue, male ducts, and mostly tropical, occurring at low densities in the subtidal, gonopores and thus have the ability to reproduce as both and dwelling as socially monogamous pairs on sea anemo- male and female (Bauer and Holt, 1998). After becoming nes used as spots for fish-cleaning activities (i.e., L. grab- hermaphrodites, individuals do not revert to males (Baeza, ham: Wirtz, 1997; L. amboinensis: Fiedler, 1998). Based 2007a), and no self-fertilization has been demonstrated on this initial dichotomy, Bauer (2000) proposed that PSH (Bauer and Holt, 1998; Baeza, 2008b; Baeza and Anker, evolved in the tropics from an ancestral symbiotic pro- 2008; Baeza et al., 2008). tandric species of Lysmata that became a specialized fish So far, the various studies on the sexual biology of cleaner. Restricted mobility of individuals resulting from shrimps from the genus Lysmata suggest that all species their association with the host and, hence, reduced prob- exhibit PSH. Protandric simultaneous hermaphroditism ability of encountering mating partners would have fa- is suspected to be a fixed trait in the genus. Nonetheless, vored PSH (also see Bauer, 2006). Under such a scenario, additional information from more species is needed to the “Crowd” warm temperate species that do not exhibit confirm this notion. In turn, other life history traits differ specialized cleaning behaviors would have evolved from within these two genera. Shrimps have been reported to tropical species with specialized cleaning behaviors and inhabit the shallow subtidal and intertidal of subtropical more complex mating systems (Bauer, 2006). A recent and tropical rocky and coral reefs around the world. Some phylogeny developed for the genus found no support for species of Lysmata live in groups, others are solitary, while Bauer’s hypothesis because socially monogamous species NUMBER 38 ¢ 97 presented a more derived position than gregarious species DISSECTIONS (Baeza et al., 2009). However, no formal testing of Bauer’s ideas was conducted. Current advances in ancestral char- Observations on reproductive anatomy were con- acter state reconstruction using Bayesian inference (Pagel ducted as in Baeza (2008b) in a total of six specimens of et al., 2004) make it possible to test whether the ancestral each species, three presumptive males (3.6-3.8 and 4.0-4.6 Lysmata featured a symbiotic lifestyle and a socially mo- mm carapace length [CL] in Lysmata galapagensis and L. nogamous mating system, as proposed by Bauer (2000). boggessi, respectively) and three presumptive hermaphro- Here, I provide evidence that PSH is a fixed trait dites that were brooding embryos (4.4—5.1 and 6.5—5.6 mm within the genus Lysmata (including Exhippolysmata), CL in Lysmata galapagensis and L. boggessi, respectively). as suspected by previous studies (see Bauer, 2000; Baeza, First, the presence or absence of male gonopores on the 2008b; Baeza and Anker, 2008; Baeza et al., 2008). coxae of the fifth pereiopods was recorded for each indi- For this purpose, I examined the sexual system of two vidual. Individuals with male gonopores (all) had sperm shrimps from the genus, L. galapagensis Schmitt, 1924 collected from the ejaculatory ducts using short electric and L. boggessi Rhyne and Lin, 2006, using anatomi- shocks that results in the ejection of a spermatophore (as cal observations and laboratory experiments. I also ex- noted in Baeza, 2006, 2007c). Each individual was then amined specimens from another nine species deposited dissected to extract the gonad for examination under the at the National Museum of Natural History (NMNH), stereomicroscope. Finally, the first and second pleopods Washington, D.C. The information altogether strongly were dissected and the presence or absence of appendi- suggests that PSH is a conserved trait within the genus ces internae and masculinae, respectively, were recorded. Lysmata. My second goal was to examine Bauer’s (2000) Specimens were defined as males or hermaphrodites by the hypothesis regarding the evolution of PSH in Lysmata. presence (males) or absence (hermaphrodites) of coupling I tested whether the ancestral Lysmata was socially mo- hooks (cincinnuli) and appendices masculinae on the en- nogamous (1) and strictly symbiotic with, for example, dopods of the first and second pleopods, respectively (see sea anemones (2), as proposed by this author. To accom- Baeza, 2007c, 2008b). plish this second goal, a review of the literature on the socioecology of Lysmata was conducted. Next, the life- EXPERIMENTS style of shrimps was mapped onto the phylogeny of the genus, and the likelihood of specific traits to occur at Three experiments, as described in Baeza et al. particular ancestral nodes in the phylogeny was tested. (2008) and Baeza (2008b), were conducted to determine the sexual system of the three species under study. In summary, the different experiments determined whether METHODS (1) brooding shrimps (reproducing as females) were capa- COLLECTION AND MAINTENANCE OF SHRIMPS ble of mating as males, (2) brooding shrimps were capable of self-fertilization, and (3) males were capable of becoming Individuals from the two studied species were collected hermaphrodites with time (see Results). In the first experi- between February and August, 2006, at different localities ment (7 = 5), pairs of brooding shrimps were maintained in Panama and Florida, USA. Individuals from L. boggessi in 21 L aquaria. In the second experiment, five brooding were collected at night during low tides from seagrass beds shrimp were each maintained alone. In the third experi- at Madelaine Key (27°38'51.87”N, 82°42'56.50” W), Fort ment (n = 5), pairs of males (small nonbrooding shrimp De Soto National Park, Florida. Specimens from L. gala- with no externally visible female gonads and visible cin- pagensis were collected from Islas Secas (7°58'37.54’N, cinnuli and appendices masculinae) were maintained 82°02'18.02”W), Gulf of Chiriqui, Panama. Immedi- separately in 21 L aquaria for at least 50 days. Individu- ately after collection, specimens were transported to the als were examined daily for hatching of the embryos, the R/V Urraca and then to the Naos Marine Laboratories, presence of exuvia from molting, development of mature Panama (L. galapaguensis) or directly to the Smithsonian oocytes in the gonad (visible through the carapace), and Marine Research Station at Fort Pierce, Florida (L. bog- spawning of a new batch of eggs. The development of any gessi). Individuals were maintained in 15—70 L aquaria at newly spawned embryos was examined in detail after four a water temperature of 22°-33°C and 34-36 ppt salinity days of spawning. and were fed every other day with shrimp pellets before Following the rationale developed by Baeza et al. being selected for dissections or experiments. (2008), if in the first experiment ovigerous shrimps that 98 © SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES paired together produced normally developing broods, using BayesTraits (Pagel and Meade, 2006; available at then it was inferred that either the other ovigerous shrimp www.evolution.rdg.ac.uk). in the aquarium acted as a male to inseminate its partner, A pruned set of sequences (from the 16S mitochondrial or that the shrimp was capable of self-fertilization. If in the gene) recently published by Baeza et al. (2009) was used to second experiment shrimps in isolation failed to success- generate a phylogenetic hypothesis for the group on which fully produce and brood developing eggs, then the possibil- to reconstruct the evolution of lifestyles in shrimps. The ity of self-fertilization was eliminated. If in the third experi- sequences pertained to 20 species of Lysmata and Exhip- ment individuals identified as males at the beginning of the polysmata plus 3 other species (Merguia rhizophorae, Hip- experiment developed the ovarian portion of the ovotestis polyte williamsi, and H. inermis) used to root the trees and produced eggs, then I inferred that male shrimps ma- during the initial phylogenetic analysis. The set of aligned ture as hermaphrodites (see Baeza et al., 2008). sequences was first imported to BayesPhylogenies (Pagel et al., 2004) to obtain a Bayesian posterior distribution POPULATION STRUCTURE ,SEX RATIO ,AND ABUNDANCE of phylogenetic trees. Metropolis coupled—Markov chain— Monte Carlo analyses were conducted using a GIR + I Information on the abundance, population structure, (invariant) + G (gamma) model of nucleotide substitu- and sex ratio (males to hermaphrodites) of each species tion. The analysis was run on two different simultaneous was collected from the field. The carapace length (CL) and chains. A total of 6,000,000 iterations were conducted, number of shrimps of each sexual phase and each species and sampling was performed every 100th tree. The last captured during the different samplings were recorded. 1,000 posterior probability trees generated by BayesPhy- The sampling effort (total number of hours spent collect- logenies were then imported to BayesTraits. The submod- ing shrimps) was calculated for each sampling event. Rela- ule MultiState in BayesTraits uses Markov chain Monte tive abundance of shrimps was estimated by dividing the Carlo (MCMC) methods to infer values of traits (that sample abundance (number of shrimps captured) by the adopt a finite number of discrete states) at ancestral nodes sampling effort. of phylogenies. Additionally, this method permits testing for particular ancestral characters at specific nodes taking MUSEU MSPECIMENS phylogenetic uncertainty into account (Pagel et al., 2004). The two traits here analyzed have three states each. Specimens from nine different species of Lysmata de- For group size, the states were (1) aggregations (includ- posited at the Collection of Crustaceans, National Mu- ing swarms), (2) small groups, and (3) pair-living (social seum of Natural History (NMNH; Smithsonian Institu- monogamy). The three character states used for describ- tion, Washington, D.C.) were examined. Dissection of ing the symbiotic propensity of different shrimp species specimens pertaining to the collection was not possible be- were (1) free-living, (2) facultative associate (with differ- cause only a few individuals were available from several of ent moray eel species, such as L. californica and L. seti- the examined species and many of the specimens were part caudata; with sea anemones, such as L. ankeri), and (3) of the type series used to describe the species. Therefore, strictly symbiotic with either sponges (e.g., L. pederseni) the identification of males and hermaphrodites was mostly or sea anemones (L. amboinensis, L. grabhami). Informa- based on external morphological characters (see forego- tion on the lifestyle of each species was obtained by direct ing). When identifying sexual phases, particular attention observation of shrimps in nature (personal observations), was given to the presence of male gonopores at the base from the literature (see literature review), or from both of the coxae of the fifth pair of pereiopods in brooding sources. shrimps as a likely indicator of simultaneous hermaphro- During the analysis, a reversible-jump MCMC search ditism (see Results). was used with two independent chains that were run for 6,000,000 iterations with a burn-in of 50,000. I choose TESTING THE HISTORICAL CONTINGENCY HYPOTHESIS the prior distribution of the parameters in the model with the option Hyperprior (see Pagel et al., 2004), seeding an To examine whether the historical contingency hy- exponential distribution from uniform on the interval 0.0 pothesis proposed by Bauer (2000) appropriately explains to 30 and a rate deviation of 18. These values were se- the origins of PSH in shrimps from the genus Lysmata, the lected considering preliminary runs and were used to keep lifestyle (in terms of the propensity to develop symbiotic the acceptance rate at approximately 0.3, as recommended partnerships and natural group size) was reconstructed by Pagel et al. (2004). Character states at internal nodes NUMBER 38 °° 99 were reconstructed using the most recent common ances- minor differences between the two species were noticed tor method. I tested hypotheses about particular character regarding the relative length and number of spines borne states at specific nodes when comparing the MCMC run- by the appendix masculinae; in L. boggessi, the spines in which the node was “fossilized” (constrained) to one were more numerous and longer than those of L. gala- state versus an alternative. The command Fossil allows pagensis (Figure 1G,H). Overall, all the anatomical dif- testing whether a particular state is “significantly” more ferences observed between brooding and nonbrooding likely at a specific node than an alternative state. For each shrimps indicate that the populations of all the Lysmata tested character, the same set of conditions (prior distri- species studied herein are indeed composed of males and bution, burn-in) as used in the ancestral character state hermaphrodites. reconstructions already described were used. However, the MCMC was run 5 times for each trait state tested, and EXPERIMENTS a total of 100,000,000 iterations were conducted. Bayes factors were calculated as the difference between the high- When two brooding individuals (presumed her- est harmonic mean of the marginal likelihood from the maphrodites) were paired, all individuals in the two five MCMC runs for each state (Pagel et al., 2004). The species examined successfully hatched their embryos as strength of support for one model over another was mea- larvae, molted, and spawned a new batch of oocytes sured using the scale from Kass and Raftery (1995). below the abdomen. The oocytes remained attached to the pleopods and showed embryonic development as em- bryos (i.e., early blastulae formation) after three days. RESULTS This embryological development suggests the ability of DISSECTIONS the other hermaphrodites in the same aquarium to re- produce as males or, alternatively, the possibility of self- Dissections demonstrated that all shrimps (brooding ing by the hermaphrodites acting as females. However, or nonbrooding) from the two species had male gonopores none of the 10 hermaphrodites (5 of each species) main- at the coxae of the fifth pair of pereiopods (Figure 1A). tained in isolation from conspecifics successfully reared Female gonopores at the coxae of the third pair of pe- their embryos to larvae. These solitary shrimps molted reiopods were more difficult to reliably observe. From all and spawned oocytes to beneath the abdomen. However, shrimps (brooding or nonbrooding), sperm cells shaped in the oocytes invariably disappeared from the pleopods the form of an inverted umbrella were retrieved from the within a few days after spawning. Overall, the observa- male gonopores by electroshocks (Figure 1A,B). Dissec- tions from these first two experiments strongly suggest tions of the gonads from small shrimps not brooding em- that brooding hermaphrodites do not have the capability bryos (presumptive males) demonstrated the presence of of self-fertilization. Therefore, brooding shrimps (her- an ovotestes (Figure 1C) with an undeveloped anterior fe- maphrodites) maintained in pairs indeed acted as males male portion full of immature oocytes (lacking coloration) and fertilized eggs when their partners molted and repro- (Figure 1D) and a posterior male gonad containing sperm duced as females. cells with the same morphology as the sperm retrieved In the experiment conducted to determine whether from the gonopores (see Figure 1B). Gonads dissected from males mature as hermaphrodites later in life, all six males brooding (presumptive hermaphrodites) shrimps also had of L. galapagensis turned into simultaneous hermaphro- ovotestes, but with a large ovarian portion full of mature dites within four months. Males showed signs of ovarian oocytes and a relatively small posterior testicular portion maturation during intermolt periods. When the gonad was with sperm (Figure 1E). In both brooding and nonbrood- full of large green (vitellogenic) oocytes, the male shrimps ing shrimps, vas deferentia and oviducts extended later- molted into hermaphrodites. Most probably, these shrimps ally from the testicular and ovarian portions, respectively mated as females shortly after molting for the first time in (Figure 1C,E). their lifetime because the spawned embryos beneath the Shrimps brooding embryos invariably lacked cincin- abdomen were observed developing normally several days nuli and appendices masculinae in the endopod of the first afte rspawning. and second pereiopods, respectively. In contrast, appendi- In contrast to L. galapagensis, all six male shrimps ces masculinae bearing relatively long spines and numerous from L. boggessi died of unknown reasons within the cincinnuli were observed in the second and first pleopods, first month of the experiment. However, observations on respectively, of nonbrooding shrimps (Figure 1F—H). Some three males of L. boggessi in the maintenance aquaria NUMBER 38 e¢ 101 indicated that they turn into hermaphrodites before four majority of them above average size) invariably lacked months. This change of sexual phase was accomplished cincinnuli and appendices masculinae in the endopod of after a single month, as observed in L galapagensis. Thus, the first and second pereiopods, respectively. This last ob- it may be concluded that L. galapagensis and L. boggessi servation suggests they were hermaphrodites. It was not are protandric simultaneous hermaphrodites, incapable of possible to detect transitional individuals in these species self-fertilization. because no dissections were possible and gonad condi- tion was not easily observed. The carapace of formalde- POPULATION STRUCTURE ,SEX RATIO ,AND ABUNDANCE hyde- and alcohol-fixed specimens is not translucent as it is in living or recently preserved specimens. Also, shrimps Abundances of L. galapagensis and L. boggessi at less than 3.0 mm CL were not sexed because of the risk the different sampling locations were high and low, with of inflicting damage. For all species examined except L. a mean of 2.79 and 0.317 individuals collected per min- anchisteus, L. argentopunctata, and L. philippinensis, ute per sampling period, respectively. In the two species, a relatively large sample of specimens was available. population was biased toward males. The ratio of males The size-frequency distribution of the different species to total shrimps collected during the sampling period was strongly resembled that of the two species studied above, 0.024 and 0.16 for L. galapagensis and L. boggessi, re- with small shrimps resembling males and large shrimps spectively. The range of body size registered for males resembling hermaphrodites (Figure 3). Observations of varied from 1.9 to 3.8 and from 3.13 to 5.75 mm CL in the coxae of the fifth pair of pereiopods of the largest L. galapagensis and L. boggessi, respectively. Hermaph- brooding shrimps in each species demonstrated the pres- rodites ranged in size between 4.1 and 5.1 and 5.63 and ence of male gonopores. Overall, the distribution of the 6.5 mm CL in L. galapagensis and L. boggessi, respec- sexes across size classes and the limited observations on tively (Figure 2). the external male and female anatomy suggest that all these other Lysmata shrimps are protandric simultaneous MUSEU SMPECIMENS hermaphrodites. A variable number of specimens from L. anchisteus, L. LITERATU REVIEW argentopunctata, L. chica, L. kuekenthali, L. moorei, L. philippinensis, L. rathbunae, L. trisetacea, and L. vittata The literature review of the 41 species of Lysmata (in- were available at the NMNH. Small shrimps in each spe- cluding Exhippolysmata) described to date revealed that cies appear to be males as they have cincinnuli and ap- the geographic and bathymetric distribution, coloration, pendices masculinae in the second and first pleopod, re- and habitat of these species are relatively well known. spectively. In turn, shrimps brooding embryos (the great Shrimps from the genus Lysmata occur in tropical, sub- tropical, and temperate waters around the world and can be found among rocks or fossilized coral, live coral, sea- grass blades, on muddy and shell bottoms, or associated FIGURE 1 .(facing page) Lysmata galapagensis and Lysmata bog- with sponges or sea anemones in the intertidal or subtidal gess ia: natomica al n dmorphologica dl ifference sbetwee nmale sand to 360 m depth. Most species have an inconspicuous color- hermaphrodites .A ,spermatophore (arrow )retrieved from gono- ation (red striped, translucent reddish with reddish flagella pores o fhermaphrodite (L .boggessi) ;B ,sperm from male (L .gala- on both pairs of antenna). Only 4 species are reported as pagensis) ;C o, voteste sfrom male (anterio rfemale and male portions featuring a striking color pattern (contrasting body colors, on top and bottom ,respectively ;arrow points a tlef tvas deferentia) bright white flagella on both antenna). This dichotomy in (L .galapagensis) ;D ,close-up o ffemale gonad portion in male (arrow coloration was previously noticed by Bauer (2000). Lys- point sa timmature oocyte )(L .boggessi) ;E o, voteste sfrom dissected mata splendida, one of the 4 species with a brilliant color- hermaphrodite (anterior female and male portions on the top and bottom ,respectively ;top and bottom arrows poin ta trigh toviduct ation, most probably is a cleaner shrimp. However, noth- and lef tva sdeferentia ,respectively )(L .galapagensis) ;F ,endopod of ing is known about its reaction to fish and its propensity first pleopod in male (arrow points at cincinulli) (L .galapagensis); to clean them. Similarly, information regarding the degree G ,endopod of second pleopod in male (arrow points at appendix of specialization of the cleaning behavior is unknown for masculina )(L .galapagensis) ;H ,endopod o fsecond pleopod in male most of the species (Table 1). (arrow point sa tappendi xmasculina )(L b. oggessi). Information on the socioecology and sexual system is, in general, poorly known. Information on lifestyle 102 e SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES TESTING THE HISTORICAL CONTINGENCY HYPOTHESIS oO Male i Transitional |_| Hermaphrodite 90 The 50% majority-rule consensus tree obtained dur- L. galapagensis ing the initial phylogenetic analysis confirms the existence of the three natural clades (tropical-American, cosmopoli- 60 tan, and cleaner) noticed previously by Baeza et al. (2009). However, one important difference between the present consensus tree and that previously published is that L. olavoi is not supported as the most basal species within the genus. This difference between trees might (1) be an ef- fect of the different set of species used for the phylogenetic analysis or (2) perhaps have occurred because the differ- shrimN opufsmber ent software programs used for phylogenetic inference function with different algorithms. On the other hand, the monophyly of Lysmata is well supported in this new tree, with a 100% posterior probability (Figure 4; Baeza et al., 2009: fig. 1). The lifestyle of shrimps mapped onto the consensus tree indicated that the most recent common ancestor of the species pertaining to the neotropical and cosmopoli- tan clades was gregarious. In contrast, the ancestor of the species comprising the cleaner clade most probably 1 (2 3 4 5 6 u 8 was socially monogamous (see Figure 4). On average, the node of the most common recent ancestor of all Lys- Size (CL, mm) mata species is reconstructed to be in state 2 (social mo- nogamy) with 80% of certainty. The degree of certainty FIGURE 2 .Lysmata galapagensis and L .boggess ipopulation struc- varied from tree to tree but was generally high, as indi- ture (7 = 178 and 22 shrimps ,respectively ,from L .galapagensis and cated by the low standard deviation of this value (SD L .boggessi ;CL = carapace length). = 0.03, calculated from 2,000,000 iterations using 1 of 1,000 randomly sampled posterior probability distribu- tion trees at each iteration). The largest harmonic log- likelihood obtained from five independent runs when the (socioecological attributes) is available only for 18 of the node was fossilized to state 0 and 2 was -—22.309507 41 described species. Of these, 7 species live in crowds and —20.865237, respectively. The almost three log-unit (aggregations), 7 species live in small groups, 3 species improvement in likelihood (Bayes factor = 2.89) of the live in pairs (i.e., they are socially monogamous), and 1 model when the node was fossilized to state 2 represents species is reported as living in extremely large aggrega- evidence that the ancestral lifestyle of Lysmata was so- tions (in swarms; Exhippolysmata oplophoroides). Dem- cial monogamy. onstration of PSH using a combination of experimental, With regard to the propensity for developing symbi- morphological, and anatomical findings and population Otic interrelationships, the reconstructions suggest that structure is available for 12 species. A strong indication the ancestor of the neotropical and cosmopolitan clades of PSH exists for another 10 species. Although the in- most probably had a free-living lifestyle and did not de- formation is incomplete (PSH has been reported for a velop any symbiotic partnership with other macroinver- total of 22 species, or 54% of the described species), this tebrates. It should be noticed that the degree of certainty review clearly demonstrates that the lifestyle and socio- of these two inferences is relatively low, as indicated by ecology of shrimps from this genus are more complex the large standard deviations of the distribution of the than originally thought and further confirms the idea character (see Figure 4). Also, the reconstructions indi- that PSH is a fixed trait in the genus Lysmata (including cate that, with a probability of 0.46 + 0.20 or 0.41 + Exhippolysmata). 0.18, either facultative partnerships or strict symbiosis, NUMBER 38 e¢ 103 [1 Male MB Hermaphrodite L. trisetacea L. moorei 12 L. rathbunae shriNm oupfms ber L. vittata L. kuekenthali 0 0 4 8 IZ 4 8 12 size (CL, mm) FIGURE 3 .Lysmata spp .Population structure o fselected species from the Nationa lMuseum o fNatura lHis- tory (7 = 71, 56, 22, 31, 70, and 57 shrimps from L. trisetacea, L. mooret, L. chica, L. rathbunae, L. vittata, an dL k.uekenthal ir,espectively). respectively, was the ancestral state of the genus Lys- cantly more likely than a free-living lifestyle in the an- mata. The improvement in the likelihood of the model cestral Lysmata. (Bayes factor = 1.51) when the node was fossilized to Overall, the present ancestral character state recon- state 2 (strict symbiosis) was low compared to when the struction provides partial support for Bauer’s (2000) hy- node was fossilized to state 0 (free-living). Therefore, pothesis about the evolution of PSH in shrimps from the there is no evidence indicating that symbiosis is signifi- genus Lysmata. 104 SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES panuiquoo sw1Oyd TseNu1IlsuI0yv s0yaI5eypd)n)DxUesDPIAT uO (TUNt)q spw , I}gaJI yIeOjga y1-e S(qOiSsI9SosR AeILUapSk tpI yBéaqd ds)g uOépAYog] NSpIDO a a S SéU a“epyqp AS9I“ P ,Is=Sn—oJ=F Fn OCTsaqUji¢ TyJeénuSogL-[ uFHTDgWsOaeeOje otU ySdD laHUYdST A ‘vA YSps TyAOd u UDAp u JsWY VOIs u{m*SUI a.joyIleNL “ToI qfJstey IUOAd }epsK AOse(zTodI[uy¢T1sdyeIQNie)D GagspIJeOpbujxI]u]syUISs eTsAu K—e ms é-aSy fs“eeUp gAGooi R ouVé ité Ld1dv€ lY Hoao- W u0qqanS erq“qS yW Iiys Nonani ,SOTédea jrasajAdu dqQnySaa oe ,s o*I7UrnITt 9 iT-SHdOnoL0TI oDSq 'P A“ Sdrq"IM T ydUujdiTe,ai O veWD iqsT7 oy“eaHdIL -TUt} —Dq 0 2TSndU qq1 do yusp vd i S erHiW“e 8jiey dUeq}T “nPSS d, s [ aWin T HRA8q“8My euovt g 6gT7I SyLlu“8djSpoyIP3 e7 OIe -YST“0desoti a nOU gM0 o LS saJd o>nT éuq‘yINs ageSqV1iUuHIrpDAd f Wteias NOTdriHsS qdenIy7 vuOdSysti TW a nI o-eagS“d ujotW]j T,Ha D “0 fejgYJd}TsMrd8qorIe asTgysSyUTd€q rov AUat,dE ,U-y Ir“i6 disT-p Teédy,DgUA0Tydo ) ,oB "pqnYIaJSredL Qsaro “yO“ o ayt9i¢ i7Daue7nt,A TnOHdA}7vyN oa-SSUW 0 “Iqxda IVLTvyVqdE i,dipG iyeWSaeDw “s éI" TyBtsPI“d-OaT oa 0qHoéqgyVrSuj Euyéd,a y LT“aT67nOCy jeo é8t drP - oéOTjea1 L s“ yéItA,aTdNp Yo8él ron B y-qgéCOevn Ts ¢L yéYs “t Ié$ sdoIJFa vN¢ onéYy “€1Gri!qjsq-ya “0-eI,svJ gniév]ja uénd é fe ~ u snéT©tao daS s éaoIverud yée, 2y é“1eT4yGT9 us IdvM a njiH e"qIo s}SjA qi et1nd i éoqia“Weo r 62Tée dr1L0 ywoée4 ,é ri1ényd g,éu t 7 “iv afps]juoey jdu“ e vusj é naer1a9Ié tyIlo ndsoaq .e My 9 1tidéo i Sqp d énE) a¢IDuqnr 7iu Noié4iHy UsiSe Jva rl0,“é e“q SS)Wy jLyéT0soUdI,,T UtiI sé sBé dS6 é“OéL uUIoT“ A Ysa u éynlPLJyIdpe. MN gIeé“sj m lsI eyTLAq odSUO tdeés é 9ddnIv u “OHDLwIt‘Us I T0aT oq smYr“dHéDNtW9éIS 7 pdDTdaUYeo ¢é ESdéas7Iéud TérIoasUHsTp-[a dUytvrSyWr 1T duSld,s y aé‘yE,oT9é0 zd irros,qtTs Iz“'0aySdu-Tn 8uyq v jpd0Yénmae7qai]ues0onuae d s t1*ési Si dud a6 nK 1TujdpHosdeteTO 4vWéoa snIoiST07ya-Gy,{rd€ 4a i qé, id“sqGuaé hL4IqJdJod ve0s1 inUa$oiX4deo qyI aruév“d¢ ,i qMt nfTWHuDo igd“eOSaE4Ty)WdCyTI,DETs “7a ojeytroeddugiay snoewAWeg yin‘osyBlo OWeYgND-OUpeuN]Y g-Opu]oytoe “AsueyIU INDYeOgUP IGIDeT OUR SEALS“s] NUMBER 38 105 “ u— PvMys eUSooi PtI1iyIdI Oos Dau NinIepDq} PnH aNdsS y*WPvd]ITaNId TI[ A"Tp dS enWH qeGN S axjS Ee EodC©HMoTYnNiGEdS) WEI)orwye, e ‘puo 0mvr€da o1-mqo0 dl{qmMa ifiqeu nHl)psSim dA ad“pTL JéTWnITnET e eeee $q '‘ f‘A7=sp 9a {s 2{ “PZpYa] RV[‘O“‘ J(jFqp91A s0EIeeUjpUYS SDOe M[B ¢0 q0TeAaUmS I‘Te[Me OlSp‘ EV0P12gnU Ssu s“ ePIg‘{‘1 =JvI“‘{BLaT7=1ssIp1Of)a“ES4wUq/op P0 8 Zys zMu SeS9290pEo“Hp =‘UueO9R SDII“‘i)EoN eG‘sU$y"p}uT9R ‘ufvOee6 LJ“ rd rYTZ‘ IWpYI£JeO =‘Vga d“o7T¢en ZAr‘eRI80r6 A1O“s“JTI yweLIU ‘l2Mv OZu9AIY‘0“ezN psTaEs6S0 IZn USTdPOs8g“‘ Y Az0W 6MTaDrdO pIoE]J“07n“}y Zu*ieA1p‘6 9o“PZUNO0*n1f6Xrp17= 9EJyZuyI£epHs9 A61aUVuSg r71s[0 Du“y0ZTS‘Y8FgT0UaN‘“u.P re9T0IAqp Yy‘PO6ru0g*o0rT69y qseP7o0O“z]Tao1I0L/nsSIHZoA0eSNyd7 H6eI71ZY.UqDPTY9 n“Yydeun jeo SétLdT oé ¢- oua Osd yp jiSées,sTodp éj qraéeida uj O s " SégOo eét Yqpu eédr “lmPéj dpyLua eCoT‘Eé,S aiy sr9ypSéé ,snytOe>) udé ,j osé“e éSa oé C|rqoT Ms T PdrSL uniév1 -yS“Ads MiOo E S07ql:p ,P‘V-1IqoéTmN —pL OoéIuv rNIYy S)yqédN0 tS ,onOCé ETéeslEI g1é 9-“éOU' WTSéPpNTITuCD,yr 9 Yé 1é eé q€ é- Oé ép Néu 7L]IS S ‘usoueUo O“tu 6T ‘ | ‘g7NIpueBzUaAy sI O‘IsWU7AtIS7yR{SO“iiaqIADyndOpdnuans 5‘a ‘ms u‘C‘mAso j8jqun o uy s gn=o0yuasjnsto y=ies ys= i=dpnixdoeowd “a Pq‘onuepYy IONSOIXSIN EABOS PISQUpuOrPyUes]7 “faellOpPe rE“sANn‘oynUETTY sJa i p o‘jy [so0qeiI dr}‘au p yu|a¢jieonlappwsu ao=lqnusI [‘*s S Ya ‘ [= rYS JUJ‘JOjPp Uaj =oMAOanIlDI\uI At=RD P‘wisi IYpSogry dsne uo= smspuusrariniyouidrs 5‘p ‘ap z¢ei yz4ei)ei s=isa a=ddssun 106 e SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES DISCUSSION time because this strategy increases reproductive success through both sperm donation to the partner and female The present study suggests that the sexual system in reproduction. Thus, an early male phase in these socially shrimps from the genus Lysmata (including Exhippolys- monogamous species should not be adaptive. On the other mata) represents a fixed trait. Anatomical observations, hand, differing costs between the sex functions might ex- behavioral experiments, and field samples demonstrated plain the existence of an early male phase before the si- that the 2 species studied here are protandric simultane- multaneously hermaphroditic phase in these monogamous ous hermaphrodites, as reported for all other Lysmata spe- species. The relatively large energetic and temporal costs cies (Table 1). Size-frequency distributions and additional of producing ova might delay maturation of the female but limited anatomical observations of museum specimens function, resulting in a functional adolescent male phase further suggest that at least 9 other species are protandric previous to the simultaneously hermaphroditic phase (see simultaneous hermaphrodites. Including the information Baeza, 2006). Additional studies in gregarious and socially generated in the present study, PSH has been reported for monogamous cleaner shrimp species should improve our a total of 22 species, or 54% of the 41 species described understanding about the conditions favoring PSH under a worldwide. social monogamous mating system in Lysmata. The well-conserved sexual system in Lysmata con- The literature review conducted herein indicates that trasts with that reported for other genera from the closely the diversity of lifestyles in the genus is greater than pre- related family Hippolytidae. For instance, two different viously recognized. Initial studies reported a distribution genera of Hippolytidae shrimps, Thor and Hippolyte, are for the genus restricted to tropical-subtropical waters. known to contain both gonochoric and strict sequentially The present review suggests that shrimps also inhabit cold hermaphroditic species (Espinosa-Fuenzalida et al., 2008, temperate environments. Lysmata porteri is reported from and references therein). The reasons for PSH to be fixed southern Chile, and L. morelandi inhabits New Zealand in Lysmata are not clear, especially when considering (see Table 1). Because Exhippolysmata spp. represents a the diversity of environments inhabited by these species derived group of Lysmata, the deep water environment (see Table 1). Different habitats with varying degrees of represents another environment colonized by the species structural complexity, seasonality, and predation regimes in this group (see Baeza et al., 2009). Also, the dichotomy should favor different sexual systems. For instance, the in social organization (“Crowd” versus “Pair” species) rather heterogeneous environment (i.e., seagrass beds, sea- noted in initial studies (Bauer, 2000) is not supported. In weed meadows) in which the gregarious L. boggessi and addition to tropical pair-living and temperate gregarious L. wurdemanni occur is expected to favor sequential her- species, the present review indicates other species forming maphroditism over PSH. In these complex environments, swarms (extremely large aggregations) in temperate deep male mating success most likely decreases with increasing water soft-bottom environments (i.e., E. oplophoroides) or body size because small body size is expected to increase living in small groups in the tropical or subtropical intertidal searching ability and, ultimately, male mating success that might or not associate with sea anemones (L. ankeri; when encounter rate among conspecifics is high (Baeza Table 1). The possibility of an adaptive radiation in this and Thiel, 2007). This small-male advantage together group of shrimps is currently being explored. The rather with the well-reported exponential relationship between unusual sex allocation pattern of this shrimps might repre- fecundity and body size in female shrimps is expected to sent the key innovation allowing species in these two gen- favor strict protandry over simultaneous hermaphroditism era to colonize and persist in environments where species in these species (Charnov, 1982). with conventional sexual systems might fail. On the other hand, hermaphroditic shrimps are known The ancestral character state reconstruction analysis to experience brooding constraints (e.g., L. wurdemanni; conducted in this study provides partial support for Bau- Baeza, 2007c), a condition that theoretically favors simul- er’s (2000) hypothesis about the evolution of PSH in Lys- taneous hermaphroditism (see Charnov, 1982, and refer- mata. The analysis suggested that the ancestral Lysmata ences therein). Similarly, in socially monogamous Lysmata shrimp lived as socially monogamous pairs either faculta- (e.g., L. grabhami; Wirtz, 1997), infrequent encounter tively associated to other macroinvertebrates or featuring rates among conspecifics should be favoring strict simulta- a strictly symbiotic lifestyle (with sea anemones, for exam- neous hermaphroditism over PSH. It should pay (in term ple). The free-living condition of several species pertaining of fitness) for each individual in a pair to reproduce both to the cosmopolitan and neotropical clades is likely to be as male and female as soon as possible during their life- derived according to the present analysis. PSH might have NUMBER 38 107 O0 +O-vF 20lOfe:QPrL O L F0b L:FBZP9OL0b2:'0 sn oA Ai(qyZou)IiNksS Gsiusoi ne[i(Jqja0-uen) wef(j1y1A4n)soey O LFb6 OSZ'LF0L 6:Z'0 OFS 0E-00:b8zLOLFee Z4e80zF0SFrZ0E:O0: O F08ZEeS'0Z:'OF9EO:b b0O -F Z60F8L8:Q7hL'0 0FZp'0 O: 04Fb8ELEVO: O =FzZ98}'0 OFE8'0-091 04b20£'0'F0ZFEZ'E00:: :90°0F96v'L0OFL8 O0 0:FF6 P:0PLS2P0'0 OFLG0:ZL O F0:Q8:LE6'0-0 O :F€ZL80 OF820:SL P :OrF'L0 - 0 Oo QOQOOSMOOBOBBBOOOOOOO0O8BO00 p(awisueaw °)1epinm JuueW °(wXALa) pINM ein S s uIpnIMoay uO sT jaJso aiUoYsydu Naols p Pad urUirPyusj Ona qs(S3JaLAu 9Ure9“Io uWU9I}[sy *obzT SosNdJi4pJOsyIdaeoUNS s}IayU }s-NA I-YpeO q)AoaTNeVRsOys]oO WyagD SId.J1 u)QJqd % IyY U0J‘pe uOonS }e~ap49 OqeU1aOpLo zso1dreO oI1u SiI rYa(AsUYuTyS9d M3oaI(SeTjA3s9r) I}0pIoi9gq).ud19ou)rIeAs *lua *sssua jp*ssoaisd *uoBeajsu6ee u*sisuauloquie *°sap °lsoissuoeydoydoOILUOYIED bedeeBb ° BaIjPA Bj oaadjyAyaajdOelld-o}sdyiuld}u4oIaSzuiWylsIENIIIM *isseb6og °im *esyngieja °EeUyeLpIan}eUa!ijas eye: *ueyue *JOABjO 1 ibqy9g0ayp *JaJOeOy ©WyjIiwSuINYJOY OOBGoOa Ge QOOBSEEBOOB OBOBOA 80'0 OF :SF068Z'S0L':0 2 6O0F°0EF'206- '0O0 €-FLSO S0F'9°0E:0 L+L80°0F62'0 -0 6400F6' €0-vF'90b'0 0 LOp'O0'FO8FEP0E'O: OFSPO:bLL O :FZSv6l'0 OFES'0:0 Zb P6LE0O'0:F 00F OZbEF£ OF:0E:'0 L O 0-bZF3}C80 0 E0FO0ZF-S4Z'bv0 O':0 FO L: LP0FLbQ L4'L0b':O: OFSS'0 :0 Fbp6L670'0: S JJOIUPJ IP SU I OIYT DO[ }FD e9UF7E]9“IBeWIUP1 )J]SMIOWTO WJIJSYUSOII UDITSI OFZS°0-0LL +bLO0FZEO- 0F6S'0:08 dno siu5aozInS [e(JB0)aibby s df(jn1a) Bgtf(iue2nd) Z£0'0 :F08'0 :2LEOF6L'0 108 e SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES evolved in the tropics from an ancestral protandric species species of Lysmata (L. wurdemanni; Baeza, 2006). New of Lysmata that became a specialized fish cleaner, as sug- studies are needed to confirm whether brood constraints gested by Bauer (2000). Restricted mobility of individuals are common in the genus. resulting from their association with the host, and, hence, In the scenarios depicted here, we should expect the reduced probability of encountering mating partners, that, in a phylogeny of the group, “tropical-low abun- would have favored PSH (Bauer, 2000) (see foregoing for dance” species would have a more basal position than further details about this hypothesis). Nonetheless, the in- the “Pair” and “Crowd” species (“Pair” and “Crowd” ferences about ancestral character states from the present sensu Bauer, 2000). The rather complex mating system analysis need to be considered with caution. Indeed, the (social monogamy) and specialized fish-cleaning behav- present analysis did not support an ancestral symbiotic ior of the “Pair” species most probably evolved from condition as significantly more likely than a free-living “tropical-low abundance” species without complex condition. Also, several internal nodes in the phylogenetic cleaning behavior and with rather simple mating systems tree were not well supported by the Bayesian analysis of (i.e., without long-lasting associations between mating phylogenetic inference (see Baeza et al., 2009). This low partners), as appears to be the case for most shrimps support for internal nodes, together with the breadth of from the closely related family Hippolytidae. The unre- the posterior distributions of the character inferred for solved position of the different natural clades with re- these nodes, means that other alternative routes to the spect to each other in the current phylogeny (see also evolution and maintenance of this peculiar sexual system Baeza et al., 2009) constrain testing this last hypothesis in Lysmata cannot be ruled out. against Bauer’s (2000) ideas. Future studies attempt- Among alternative historical scenarios (to that pro- ing to resolve the natural relationships among species posed by Bauer, 2000), PSH might well have evolved of Lysmata, Exhippolysmata, and other related taxa to- from a strict simultaneous hermaphrodite or even from gether with the detailed examination of their sexual sys- a strict gonochoric free-living ancestor inhabiting tropi- tem should allow explaining the origin of simultaneous cal environments. The evolution of PSH from an ances- hermaphroditism in shrimps from the genus Lysmata. tral strictly simultaneous hermaphroditic condition has Last, it is worth mentioning one of the main assump- been reported previously for the worm Ophryotrocha di- tions of the present analysis. PSH was treated as a sin- adema, one of the few other marine invertebrates in which gular innovation only originating in the genus Lysmata PSH has been demonstrated (Dahlgren et al., 2001). Act- (which contains Exhippolysmata), as initially suggested ing together with the conditions favoring simultaneous by Bauer (2000). To the best of my knowledge, shrimps hermaphroditism (i.e., low abundance), sex-dependent from the genus Merguia, apparently the sister group energetic costs might have favored an early maturation to Lysmata, seem to have a gonochoric sexual system. of the male reproductive function compared to that of However, this observation needs experimental confirma- the female function in the ancestral free-living shrimp (re- tion. Most importantly, future studies need to test for gardless of its sexual system), ultimately resulting in the the existence of protandric simultaneous hermaphrodit- evolution of PSH as we observe it today in Lysmata (and ism in members from other closely related genera (t.e., Exhippolysmata). Similarly, brooding constraints experi- Mimocaris, Parahippolyte, Merguia, Merhippolyte). enced by hermaphroditic shrimps might have favored the These studies might reveal that PSH is not a singularity. retention of the male function later in life. If the space Indeed, PSH has independently evolved in the past at for brooding embryos in the abdomen becomes saturated, least four other times outside the Caridea. In addition to allocation of energy to sperm production is expected to Lysmata shrimps, PSH has been confirmed in the poly- maximize fitness. This argument is similar to that of Ghis- chaete worm Ophryotrocha diadema (Premoli and Sella, elin (1987) to explain apparent protogynous simultane- 1995), the land snail Achatina fulica (Tomiyama, 1996), ous hermaphroditism in chitons. In some species of poly- the tunicate Pyura chilensis (Manriquez and Castilla, placophorans, individuals brood eggs along the side of 2005), and the symbiotic barnacle Chelonibia patula the body. Early in life, they reproduce strictly as females (Crisp, 1983). If simultaneous hermaphroditism turns until they reach a size at which the space in which they out not to be a singularity in shrimps from the families brood is saturated. At that point, the same individuals Hippolytidae and Lysmatidae, then it should be possible start producing sperm while they are brooding. Brooding to explore the environmental conditions that favor this constraints have been previously reported for at least one unique sexual system in shrimps. NUMBER 38 e¢ 109 ACKNOWLEDGMENTS Baeza ,J .A. ,J .Reitz ,and R .Collin .2008 .Protandric Simultaneous Her- maphroditism and Se xRatio in th eShrimp Lysmat anayaritensis. Journa ol fNatura Hl istory 4, 1:2843-2850. I appreciate the support from the Smithsonian Tropi- Baeza ,J .A. ,C .D .Schubart ,P .Zillner ,S .Fuentes ,and R .T .Bauer .2009. cal Research Institute (STRI, Panama City and Bocas del Molecula rPhylogen yo fShrimp sfrom the Genu sLysmata (Cari- Toro, Panama) Marine Fellowship and the Smithsonian dea L:ysmatidae )T:h eEvolutionar yOrigin so Pf rotandri cSimulta- Marine Station at Fort Pierce (Fort Pierce, Florida, USA) neou sHermaphroditism an dPair-Living B. iologica Jlourna ol tfheLinnae Saoncie 9ty6,:415—424. Fellowship. I thank Dr. Rachel Collin for inviting me to Baeza, J. A., and M. Thiel. 2007. “The Mating System of Symbiotic join the 2007 Research Cruise to La Coiba Island and Las Crustaceans: A Conceptua lMode lBased on Optimality and Perlas Archipelago, off the Pacific coast of Panama, aboard Ecologica lConstraints.” In Evolutionary Ecology o fSocia landSexual Systems: Crustaceans as Model Organisms, ed. J. E. the R/V Urraca (STRI), during which a portion of this Duffy and M. Thiel, pp. 250-267. Oxford, UK: Oxford Univer- study was conducted. I thank Dr. Klaus Ruetzler (National s iPtyress. Museum of Natural History, Smithsonian Institution), Dr. Baue rR ,T .2.000 S.imultaneou sHermaphroditism i nCaridea nShrimps: Anson (Tuck) Hines (SERC) and Dr. Valerie Paul (SMSFP) A Unique and Puzzling Sexua lSystem in the Decapoda .Journa lofCrustacea nBiolog y2,0(Spe cN. o 2.):116-128. for funding various research visits to Carrie Bow, Belize, 2. 006 S. am eSexua Sl ystem bu Vt ariabl eSociobiology E: volution during which a major portion of this manuscript was com- o Pfrotandr iScimultaneou Hsermaphroditism iLnysma tSahrimps. pleted. I also thank Paula Rodgers and Rafael Lemaitre for Integrativ aen Cdomparativ Beiolog y4,6:430-438.Bauer ,R .T. ,and G .J .Holt .1998 .Simultaneous Hermaphroditism in their support during my visit to the National Museum of th Me arin Sehrim pLysmat wa urdemann (iCaridea H: ippolytidae): Natural History. The comments by two anonymous refer- An Undescribe dSexua Sl ystem in th eDecapo dCrustacea M. arine ees substantially improved this manuscript. This work is Biolo g1y3,2:223-235. contribution number 776 of the Smithsonian Marine Sta- Bauer ,R .T. ,and W .A .Newman .2004 .Protandric Simultaneous Her-maphroditism i nth eMarin eShrim pLysmat acalifornic a(Caridea: tion at Fort Pierce and contribution number 840 of the Ca- Hippolytidae )J.ourna o lCf rustacea nBiology 2,4:131-139. ribbean Coral Reef Ecosystems Program (CCRE), Smithso- Braga ,A .A. ,L .S .Lopez-Greco ,D .C .Santos ,and A .Fransozo .2009. nian Institution, and supported in part by the Hunterdon Morphologic aElvidenc fe oPrrotandr Sicimultaneou Hsermaphro-ditism i nth eCaridea nExhippolysmat aoplophoroides J.ourna ol f Oceanographic Research Fund. This study was partially Crustacea Bniolog 2y9, :34-41. funded by a National Geographic Research Grant from the Bruce ,A .J .1983 .Lysmata debelius ,New Species ,a New Hippolytid National Geographic Society, USA. Shrimp from th ePhilippines R. evu eFrancais ed’Aquariologi eet Herpetolo g4:i1e1, 5-120. 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"Protandric Simultaneous Hermaphroditism Is a conserved trait in Lysmata (Caridea:Lysmatidae): Implications for the Evolution of Hermaphroditism in the Genus." Proceedings of the Smithsonian Marine Science Symposium 38, 95–110. View This Item Online: https://www.biodiversitylibrary.org/item/131385 Permalink: https://www.biodiversitylibrary.org/partpdf/387344 Holding Institution Smithsonian Libraries and Archives Sponsored by Biodiversity Heritage Library Copyright & Reuse Copyright Status: In Copyright. Digitized with the permission of the rights holder License: http://creativecommons.org/licenses/by-nc-sa/3.0/ Rights: https://www.biodiversitylibrary.org/permissions/ This document was created from content at the Biodiversity Heritage Library, the world's largest open access digital library for biodiversity literature and archives. Visit BHL at https://www.biodiversitylibrary.org. This file was generated 31 May 2024 at 05:56 UTC