Male Phase Research Articles

Sex change and reproductive output of the protandric shrimp Merguia rhizophorae (Rathbun, 1900) (Decapoda, Merguiidae)

ABSTRACT The aim of this study was to confirm the type of protandry adopted by M. rhizophorae and to describe the size at which sex change occurs in order to test predictions of sex allocation theory. The reproductive output also was investigated, based on fecundity and embryo volume. Specimens were collected cohabiting burrows built by mud shrimps Upogebia omissa in an estuary region in the northeast of Brazil. The body size (carapace length, CL) and sex of the shrimps were recorded. Observations were made developmental stages of the embryos, fecundity, and embryo volume. A total of 204 M. rhizophorae individuals was sampled, of which 170 (83.3%) male phase (MP) and 34 (16.7%) female phase (FP) individuals. The body size (mean ± SD) of the individuals in the MP was smaller than in the FP: 3.91 ± 0.78 and 6.18 ± 0.52 mm CL, respectively. The size at which 50% of the shrimps changed to FP (CL50) was 5.62 ± 0.01 mm CL. Reproductive output (fecundity and embryo volume) increased linearly with shrimp body size. An increase in embryo size during development and the loss of embryos during final stage of development were recorded. In this study, the behaviour exhibited by M. rhizophorae (share a burrow with another shrimp species) was recorded for the first time, expanding knowledge about the ecology of this semi-terrestrial shrimp. Our results indicate the adoption of strict protandric hermaphroditism by M. rhizophorae. Our study supports the prediction of sex allocation theory that sex ratio is significantly biased towards the first-sex in sequential hermaphrodites. We also found evidence of possible trade-offs between the size in which the sex change occurs and the reproductive strategy exhibited by M. rhizophorae.

Identification of Peptides and Their GPCRs in the Peppermint Shrimp Lysmata vittata, a Protandric Simultaneous Hermaphrodite Species.

Peptide hormones commonly binding with G-protein coupled receptors (GPCRs) achieve their function in reproduction. The peppermint shrimp Lysmata vittata popular in marine ornamental trade and is known to display protandric simultaneous hermaphrodite (PSH). Knowledge on reproductive biology of this commercial species is critical for resources management and aquaculture. This study employed Illumina sequencing and bioinformatics analysis to identify peptides and their candidate GPCRs from male phase (MP) and euhermaphrodite phase (EP) of L. vittata. A total of 61 peptide and 40 peptide GPCR transcripts derive from 44 peptide families and 13 peptide GPCR families were identified, respectively. Among them, insulin-like androgenic gland hormone and crustacean female sex hormone have two unique mature peptides, respectively, and their transcripts showed higher expression levels in MP than EP, which suggest that these sex differentiation hormones might be involved in sexual characters than spermatogenesis or vitellogenesis. Overall, the first study on identification of peptides and their GPCRs in the genus Lysmata extends our knowledge of peptidergic signaling in PSH species, and provides an important basis for development of aquaculture strategies.

Persistence of Reduced Androgenic Glands after Protandric Sex Change Suggests a Basis for Simultaneous Hermaphroditism in a Caridean Shrimp

The caridean shrimp Lysmata wurdemanni is a protandric simultaneous hermaphrodite. These individuals go through a male phase (MP) before changing sex to become female-phase simultaneous hermaphrodites (FPSH). The latter have an externally female phenotype, but retain a reduced male reproductive system and both male and female reproductive function. Previous studies have reported that the androgenic glands (AGs), whose hormones stimulate development of male characteristics in decapod crustaceans, are absent in the female phase of purely protandric species. We tested the hypothesis of androgenic gland persistence in FPSHs of L. wurdemanni by dissection and histology on the ejaculatory ducts. These glands were observed in FPSHs, although in a variably atrophied form. Androgenic glands of L. wurdemanni MPs are compact and replete with well developed cells, with large, deeply stained (hematoxylin-eosin) nuclei, as in males of gonochoric and protandric species. The AGs of simultaneous hermaphrodites were more reticulate in appearance due to the apparent breakdown and loss of cells, resulting in vacuolated areas, or empty spaces in the gland surrounded by connective tissue fibers or cell remnants. However, all FPSHs possessed numerous, or at least some possibly functional cells. The greatest atrophy of AGs was observed in the largest (i.e., oldest) FPSHs. However, the ovotestes of all FPSHs retained a small testicular portion with well developed ejaculatory ducts containing sperm. Our results suggest that the reduced androgenic glands of female-phase simultaneous hermaphrodites of L. wurdemanni allow them to maintain male reproductive function after sex change.

Analysis of life-history traits in a sex-changing marine shrimp (decapoda: caridea: rhynchocinetidae).

The hypothesis of protandrous (male to female) sex change was tested for the first time in a rhynchocinetid shrimp, Rhynchocinetes uritai, with an analysis of life-history traits. Samples were taken monthly for 2 years in Oura Bay, Japan, using a combination of bait and refuge traps. Breeding was seasonal but extended from spring through autumn, with female-phase individuals (FPs) producing broods successively, with their ovaries maturing for a new spawn during incubation of a previous brood. Females incubated numerous (∼500-4000) embryos that suffered insignificant mortality before hatching. Recruitment of juveniles after planktonic larval development began in summer and peaked during the autumn, with negligible recruitment during winter and spring. Cohort analysis confirmed the hypothesis of protandric sex change in this species, with juveniles maturing into the male phase (MP) during their first reproductive season at an age of 6-10 mon, depending on the time of recruitment. Sex change occurred during the following winter when transitional individuals matured into FPs during their second reproductive season at an age of ≥18 mon. Two cohorts were followed from recruitment until the end of the study, indicating a life span of 21-25 mon. Aside from its sexual system, this sex-changing species showed no obvious differences in reproductive and other life-history traits from those of gonochoric species from similar latitudes and habitats.

Protandric simultaneous hermaphroditism in Parhippolyte misticia (Clark, 1989) (Caridea: Hippolytidae): implications for the evolution of mixed sexual systems in shrimp

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 oocytes 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.

Sex-dependent energetic cost of a protandric simultaneous hermaphroditic shrimp Lysmata wurdemanni under different social conditions

We tested a hypothesis (sex-dependent energetic cost) in a protandric simultaneous hermaphroditic (PSH) shrimp Lysmata wurdemanni under different social conditions to explain the adaptive value of PSH. Two components (sex-dependent energetic cost and resource holding power) of the hypothesis were tested. Growth reduction was used to represent the energetic cost in reproduction. This study demonstrated that energetic cost of reproduction of the shrimp is generally sex-dependent, but they are strongly affected by the social environment. When male phase (MP) or euhermaphridite phase (EP) shrimp were housed individually (i.e. without social and reproductive behavior), reproductive cost (energy for gametic production only) of MP shrimp was significantly lower than that of EP shrimp (with both male and female functions). However, growth of MP shrimp did not differ from that of EP individuals when they were housed with EP shrimp, i.e. when costs of both social and mating behavior were considered. When a MP shrimp copulated with EP shrimp more than once within a molt cycle, growth was significantly reduced. Result also indicated that resource holding power of L. wurdemanni was not associated with energy burden of female function. Our results do not support the hypothesis of size-dependent energetic cost in L. wurdemanni.

Surface glycoproteins are not the contact pheromones in the Lysmata shrimp

Behavioral evidence suggests that some male caridean shrimp, such as those of Lysmata species, identify conspecific females via contact pheromones that coat the cuticle surface of the females. In this study, we attempted to determine whether the contact pheromones in three Lysmata species, Lysmata ankeri, Lysmata boggessi, and Lysmata wurdemanni, are glycoproteins as hypothesized previously in a diverse group of aquatic invertebrates. Twenty lectins were screened and lectin-binding experiments indicated that lectin treatment did not affect mate recognition in the shrimps. The behavior of the male-phase (MP) shrimp in the three treatments (non-lectin-treated MP and lectin-treated euhermaphrodite-phase (EP) shrimp, lectin-treated MP and lectin-treated EP shrimp, and lectin-treated MP and non-lectin-treated EP shrimp) and in the control was not different in responding to lectin-treated and control EP shrimp. All the MP shrimp copulated with lectin-treated and control EP shrimp successfully. All the MP shrimp copulated with ethylenediamine tetraacetate-treated EP shrimp (with glycoproteins removed from their cuticle surface) immediately after they detected the EP shrimp. The results suggest that glycoproteins are not likely to be the contact sex pheromones in the three Lysmata shrimp species.

Effects of density and simulated recruitment and mortality on sex change in a protandric simultaneous hermaphroditic shrimp, Lysmata wurdemanni

Sex change in many hermaphrodite animals has been suggested to be environmentally determined, especially socially. To investigate whether sex change in the protandric simultaneous hermaphrodite shrimp Lysmata wurdemanni (Gibbes 1850) is socially mediated, two experiments were conducted in the laboratory between September 2002 and April 2004 using laboratory-cultured shrimp that originated from Port Aransas, Texas, USA. The size at sex change (from male to simultaneous hermaphrodite) in this shrimp is variable, with the minimum around 2.4 cm in total length (TL). Large shrimp (2.4–4.5 cm TL) still in the male-phase (MP) have been found in the wild and laboratory environments. This study tested the hypothesis that large MP shrimp delay changing to the euhermaphrodite-phase (EP) due to social control. In the first experiment, ten shrimp were raised in large (110-l) and small (20-l) containers to test the effect of habitat size/density on sex change. The percentage of shrimp changing to EP was significantly higher in the large container (low density) than in the small container after 60 and 120 days. But after 570 days sex ratios were the same, 2 MP:8 EP. In the second experiment, group composition was changed over time to simulate population recruitment and mortality. MP shrimp delayed sex change when EP shrimp were present. However, if group structure is stable, some MP shrimp may not change sex during their lifetime. Under certain demographic conditions, such as when postlarvae (PL) were added to (simulating recruitment) or EP shrimp were removed from (simulating mortality) a group, all old MP (from original PL) shrimp changed to EP. The response of old MP shrimp to simulated recruitment is faster than to simulated mortality. The present study confirms that social control affects the size and timing of sex change in L. wurdemanni. However, some MP shrimp never change sex suggesting that genetics might also play a role in the sex ratios of L. wurdemanni populations.

Cost of maleness on brood production in the shrimp Lysmata wurdemanni (Decapoda: Caridea: Hippolytidae), a protandric simultaneous hermaphrodite

Individuals of Lysmata wurdemanni first mature in a male phase (MP) and then change to the external phenotype of females (female-phase=FP). The FPs retain the male gonadal system and function both as male and female (simultaneous hermaphrodites). The cost of maleness to FPs on fecundity was estimated with an experiment in which the social environment (FP opportunity to function as a male) was varied. The effect of maleness on brood size (number of embryos brood−1) and frequency of spawning (interspawn interval in days) was measured in FPs maintained in different social environments (treatments) over two complete spawning cycles. In treatment 1 (isolated FP) and 2 (1 FP, 1 MP), FPs could only function as females. In treatments 3 (2 FPs) and 4 (5 FPs, 5 MPs), FPs could breed both as male and female.Baseline brood size was described for FPs with a regression equation of brood size on FP body size (carapace length). Brood size is positively and isometrically related to FP size. Brood sizes, adjusted for FP body size using the baseline regression equation, were compared among treatments 2–4 (isolated FPs in treatment 1 did not produce fertile broods). Brood sizes were significantly greater in FPs in treatment 2 (only female breeding) than in treatments 3 and 4 (both male and female sexual function possible). However, spawning was less frequent (longer interspawn intervals) in treatments 1 and 2 than in treatments 3 and 4. Total fecundity over a four-month breeding period was estimated with a model using mean treatment brood sizes and interspawn intervals. Estimates of total fecundity in FPs functioning both as male and female were much lower, in spite of somewhat more frequent spawning, than those in which male function was not allowed. The ‘price’ (cost) of maleness on fecundity appears to be compensated by the high selective advantage of male mating ability in the simultaneous hermaphrodite FPs of Lysmata species.

Development of sexual morphs in two simultaneous hermaphroditic shrimp, Lysmata wurdemanni and Lysmata rathbunae

Summary Development of secondary sexual morphs from post-larva to maturation was described for two simultaneous hermaphroditic shrimp, Lysmata wurdemanni and L. rathbunae. In post-larval stage and male-phase (MP) individuals, both endopods of the first pleopods and appendix interna (AI) of pleopod 2 increase as shrimp grow. The morph change from MP to the euhermaphrodite phase (EP) is a gradual process involving five molts. A reliable and simple criterion for identifying MP, transitional-phase, and EP shrimp is presented.

Experimental test of socially mediated sex change in a protandric simultaneous hermaphrodite, the marine shrimp Lysmata wurdemanni (Caridea: Hippolytidae)

In Lysmata wurdemanni, individuals begin benthic life in a male phase (MP) but later change to a female phase (FP) with female external morphology, but with both male and female reproductive capacity (protandric simultaneous hermaphroditism). Previous studies have demonstrated that the size (timing) of sex change varies considerably in natural populations. We experimentally tested for social mediation of sex change by rearing male-phase individuals (MPs) in both large and small social groups with different sexual and size composition. In the “large group” experiment, speed of sex change was inversely related to the abundance of female-phase individuals (FPs) in the group (sex-ratio induction). Increased allocation to female function (more rapid change to FP) may occur when male mating opportunities are lower because the simultaneous-hermaphrodite FP can immediately reproduce as a female while maintaining male mating capacity. When FPs are abundant, delayed sex change might be adaptive because the costs of female reproduction are considerable. An MP may gain reproductively by increased growth before changing to FP at a larger size (fewer but much larger broods). Size-ratio induction of sex change by small MPs was suggested but not confirmed. Experimental results from “small groups” (1–2 individuals) were qualitatively similar but not as conclusive as those from large groups. The number and complexity of social interactions in large groups may be necessary to stimulate labile sex change in this species. In L. wurdemanni, sex change may be influenced not only by abiotic factors related to breeding [Bauer (2002) Biol Bull 203:347–357] but also by social factors in certain demographic situations.

Mating Without Anterior Pleopods in a Simultaneous hermaphroditic shrimp, Lysmata Wurdemanni (Decapoda, Caridea)

The effects of copulatory rami removal of male-role shrimp (male-phase (MP) or euhermaphrodi te-phase (EP)) on mating behavior of a simultaneous hermaphroditic shrimp, Lysmata wurdemanni, were investigated in the laboratory. There was no difference in general mating behavior between male-role shrimp with or without ablation of copulatory pleopods. However, ablation highly significantly (P < 0.001) affected copulation frequency. The influence was also sex dependent (P < 0.001). In general, copulation frequency in ablated EP shrimp was significantly higher (P < 0.05) than in ablated MP of the same treatment. Ablation of either pleopod 1 or pleopod 2 in MP shrimp did not affect mating behavior or spermatophore transfer. The success of spermatophore transfer was negatively correlated with the mean copulation frequency (R = ?0.9707, P < 0.001). Normally, spermatophores were deposited on the base of the last two pairs of pereiopods. Ablation of the pleopods may lead to failure of emission or improper deposition of a spermatophore. Some new mating behaviors are described and a possible mating mechanism for the shrimp is proposed.

Fertilization Success without Anterior Pleopods in Lysmata Wurdemanni (Decapoda: Caridea), a Protandric Simultaneous Hermaphrodite

Abstract The modifications of the first two pleopods in male shrimp have long been considered to serve in insemination of the female. The role of pleopods 1 and 2 in mating in a protandric simultaneous hermaphroditic shrimp, Lysmata wurdemanni, were investigated. Results indicate that the modified endopod of pleopod 1 is not needed to transfer sperm in both male-phase (MP) and euhermaphrodite-phase (EP) shrimp. Absence of pleopod 2 does not affect the sperm-transfer success in both MP and EP shrimp. Removal of pleopod 1 also has no impact on fertilization in the MP shrimp; however, sperm transfer is affected by removal of pleopod 1 in some EP shrimp. Even when both pleopods 1 and 2 are completely ablated, about 20% of the shrimp can still fertilize successfully and another 20% partially successfully.

Protandric Simultaneous Hermaphroditism in the Marine Shrimp Lysmata Californica (Caridea: Hippolytidae)

Abstract To investigate the extent of protandric simultaneous hermaphroditism (PSH) in the genus Lysmata, observations were made on the sexual system of L. californica, a species from the warm-temperate eastern Pacific. Observations on a large number of female-phase individuals (FPs) from a museum collection indicated that FPs with broods containing advanced embryos spawn again (successively) soon after brood hatching. Female-phase individuals maintained in pairs went through successive cycles of embryo brooding concomitant with gonadal vitellogenesis, hatching, molting, and spawning. Time-lapse video observations confirmed that FPs are able to copulate as males and inseminate postmolt, prespawning FPs. Prespawning FPs maintained alone did not produce successful broods of embryos. Thus, FPs of L. californica are outcrossing simultaneous hermaphrodites. Size-frequency distributions of sexual phases showed that individuals develop first in the male phase (MP) and then change to the female phase. Individuals...

Simultaneous hermaphroditism in the marine shrimp Lysmata wurdemanni (Caridea: Hippolytidae): an undescribed sexual system in the decapod Crustacea

Simultaneous hermaphroditism with out- crossing, a previously unconfirmed sexual system in decapod crustaceans, is documented in the shrimp Lysmata wurdemanni (Gibbes), using time-lapse video observations on mating in pairs of ''female-phase'' (FP) individuals. Copulations between FPs resulted in suc- cessful spawning and development of embryos. However, female-phase hermaphrodites maintained in isolation were unable to self-fertilize spawned eggs. All smaller individuals possessed characters typical of cari- dean males, including male gonopores, appendices masculinae, ejaculatory ducts, and cincinnuli on the first pleopods. However, the gonad of these male-phase (MP) individuals was an ovotestis with an undeveloped ovar- ian portion. FPs, which spawn eggs and incubate embryos, also had male gonopores and an ovotestis terminating in ejaculatory ducts containing sperm. In FPs, male pleopod characters were absent or reduced, and a female incubatory character, expanded pleopod flanges, showed a greater relative size. Smaller size classes of the population were composed only of MPs while larger size classes consisted of both MPs and FPs. ''Transitionals,'' individuals with MP characters but an ovotestis containing vitellogenic oocytes, were rare and overlapped completely in size with FP and larger MP individuals. It is suggested that not all MPs transform into FP hermaphrodites. Social interactions may medi- ate MP change into FP hermaphrodites in L. wurde- manni. The social system of L. wurdemanni and other Lysmata spp. may determine the exact form of the sex- ual system in these species.