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Persistence of reduced androgenic glands after protandric sex change suggests a basis for simultaneous hermaphroditism in a caridean shrimp.

Abstract. 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.

Introduction

Crustaceans exhibit a variety of sexual systems, ranging from gonochoristic (separate sexes) to a wide range of sequential, simultaneous, and mixed hermaphroditic systems (Charniaux-Cotton and Payen, 1985; Bauer, 2000; Avise, 2011; Weeks et al., 2014). Although most decapod crustaceans (shrimps, lobsters, crayfishes, crabs) are gonochoristic, numerous caridean shrimp species are sequential hermaphrodites, first developing as males and then changing sex to females (protandry) (Bauer, 2000; Chiba, 2007). A novel protandrous sexual system was described in the hippolytid carideans Lysmata wurdemanni (Gibbs, 1850) (Bauer and Holt, 1998) and Lysmata amboinensis (de Man, 1888) (Fiedler, 1998), in which individuals first develop as males, then later change to simultaneous hermaphrodites with a primarily female phenotype. However, the latter individuals have both male and female gonopores, and the gonads (ovotestes)--while primarily ovarian--retain a small posterior testicular portion that produces sperm. The testicular portion is equipped with vasa deferentia and ejaculatory ducts opening to the exterior by gonopores on the coxae of the fifth pereopods (i.e., most posterior walking legs), the usual location in caridean males. Such individuals are capable of successfully mating as males, while also reproducing as females (e.g., Bauer and Holt, 1998; Lin and Zhang, 2001; Bauer, 2002; Baeza, 2007). This sexual system was termed "protandric simultaneous hermaphroditism" (PSH) by Bauer in 2000; since that time, it has been described in several species of Lysmata (all that have been tested experimentally; Baeza, 2009). Protandric simultaneous hermaphroditism has since been confirmed in two other hippolytid species: Exhippolysmata oplophoroides (Laubenheimer and Rhyne, 2008; Braga et al., 2009) and Parhippolyte misticia (Onaga et al., 2012).

The simultaneous-hermaphrodite phase was originally termed the "female phase" (FP) because of its primarily female phenotype and its developmental homology with the female phase of protandric species (Bauer and Holt, 1998; Bauer, 2006). However, various other terms have been used for the simultaneous-hermaphrodite phase, such as "euhermaphrodite" (Lin and Zhang 2001), "simultaneous hermaphrodite" (Calado and [N.sub.a]rciso, 2003), or simply "hermaphrodite" (Baeza, 2009). In light of this variation in terminology used for PSH species, in this report we use the terms "male phase" (MP) and "female-phase simultaneous hermaphrodite" (FPSH) for the two sexual morphotypes of PSH.

Sex determination in decapod and other malacostracan crustaceans is physiologically controlled by the presence or absence of androgenic glands, which are endocrine organs situated on the distal vas deferens, or ejaculatory duct (Charniaux-Cotton and Payen, 1985; Sagi et al., 1997). AGs secrete an insulin-like peptide (IAG), which stimulates and controls the development of external sexual characteristics, testicular tissues, spermatogenesis, and mating behavior in males (Ventura et al., 2011a). Both males and females have AG anlagen (Hoffman, 1972; Charniaux-Cotton and Payen, 1985), which develop only in genetic males, stimulating development of the male phenotype. Ablation of AGs causes feminization of males, and implantation of AGs in genetic females masculinizes them. In protandric shrimps, AGs degenerate and then disappear in older MP individuals, bringing about sex change to the female phase (Carlisle, 1959; Hoffman, 1969; Frechette et al., 1970; Gavio et al., 2006; Kim et al., 2006). Berreur-Bonnenfant and Charniaux-Cotton (1965), Charniaux-Cotton (1975), and Charniaux-Cotton and Payen (1985) stated that androgenic glands degenerated and were absent in the FP of Lysmata seticaudata, in spite of a small testicular portion that is retained in an otherwise ovarian gonad. These authors considered the male gonadal characters of the female phase vestigial and non-functional as far as mating was concerned. However, protandric simultaneous hermaphroditism was later demonstrated in this species with observations of mating reported (d'Udekem d'Acoz, 2002), as in other Lysmata species.

The presence or absence of androgenic glands, essential for the expression of male sexual characteristics, has not been well demonstrated or studied in the "female phase" (FPSH) of any caridean with a PSH sexual system. Persistence of AGs in some form may explain the presence of male gonadal characters and male copulatory ability in FPSHs. In this study, we tested the hypothesis that androgenic glands persist in the FPSHs of Lysmata wurdemanni, a species in which protandric simultaneous hermaphroditism otherwise has been well studied (reviewed in Bauer, 2006; Baeza, 2009).

Materials and Methods

Individuals of the shrimp Lysmata wurdemanni used in this study were collected during low nocturnal tides, using long-handled, 1-mm-mesh dip nets, from under ledges of the rock jetty adjacent to the marine laboratory of the University of Texas, Austin, at Port Aransas, TX (27 [degrees] 50' N, 97 [degrees] [O.sub.3]' W). Specimens used for dissection and size measurement of androgenic glands were taken from collections caught on May 8-9, 2000. Individuals were originally preserved in 10%--15% seawater formalin for 1-2 days, washed in water, and stored in 70% ethyl alcohol. Histological work was done on specimens from collections taken June 8-9, 2013; live specimens were anesthetized within one day by cooling, then placed in either Davidson's solution (Bell and Lightner, 1988) or in 10%--15% seawater formalin for 72-100 h, washed in water, then maintained in 70% ethyl alcohol.

As previously demonstrated by Bauer and Holt (1998), the gonads of L. wurdemanni are ovotestes, with an anterior ovarian and posterior testicular portion (Fig. 1A-C). Figure 1A-C was redrawn from figure la, d, and e in Bauer and Holt (1998), and modified by shading the testicular portion of the gonads and adding the androgenic glands, whose position along the ejaculatory duct was observed in this study. In smaller male-phase individuals, the oviducts are not visible, but the vasa deferentia, which terminate in distal ejaculatory ducts that open at the male gonopores, are well developed (Fig. 1A) and contain sperm. With MP growth, oviducts, which lead to the female gonopores, develop from the middle part of the ovotestes (Fig. IB). In MPs nearing sex change, vitellogenic oocytes are produced in the anterior ovarian section, as in female-phase simultaneous hermaphrodites nearing spawning (Fig. 1C).

For measurements of AG size, ejaculatory ducts--with roughly trianglular or pyramid-shaped AGs attached--were dissected out from both sides of MPs (n = 21) and FPSHs (n = 28), lightly stained in acid fuchsin in 70% ethanol, and then prepared for microscopic examination on slides using the mounting medium, CMC (Polysciences, Inc., Warrington, PA), which is a mixture of polyvinyl alcohol, lactic acid, and phenol. Slides of ejaculatory ducts from both sides were made because the small, fragile AGs are easily damaged or lost during dissection. For comparison of AG size among individuals, height and length of two sides, as shown in Figure ID, were made, using an ocular micrometer, and summed for each individual. For each individual, measurement of the left or right side was chosen by a random procedure; when only one AG measurement was available for an individual (left or right side), that side was used.

For histology, the ejaculatory ducts with attached AGs were dissected out, dehydrated in a gradual ethanol series to 100%, and infiltrated with xylene before infiltrating and embedding in paraplast medium at the 56-58 [degrees]C melting point. Transverse sections 5-7 [micro]m thick were cut from specimens, using a rotary microtome (Leica RM 2125 RT) and low-profile, disposable microtome blades (series DB80). Sections were stained with hematoxylin-eosin or Lendrum before permanent mounting in synthetic resin (Sheehan and Hrapchak, 1980).

Results

Androgenic glands were located both in male-phase individuals and female-phase simultaneous hermaphrodites, on the concave side of the J-shaped ejaculatory ducts (Fig. 1A-C and Fig. 2). AGs are irregularly triangular (Fig. 2), and, in the specimens examined, ranged in size from 272-984 [micro]m in MPs (mean = 554.3 [micro]m [+ or -] SD = 176.0 [micro]m) and from 184-1432 [micro]m in FPSHs (mean = 686.9 [micro]m [+ or -] 248.1 [micro]m). As FPSHs are larger in body size than MPs in this sex-changing species (Fig. 3), it is difficult to directly compare mean AG size between sexual morphs. The overlap in body size of MPs and FPSHs was not great enough (Fig. 3) to utilize analysis of covariance to test the hypothesis of no difference in relative AG size between the two sexual morphs. However, the slopes of the regression lines of AG size on carapace length (CL), a measurement of body size, are very similar; but the regression line for FPSH is somewhat lower (more negative y-intercept), indicating a slight decrease in AG size with increasing FPSH body size.

Although relative androgenic gland size appears to differ little between the two sexual morphs, there is a distinct difference in their overall aspect and internal structure. The AGs of smaller male-phase individuals are compact and filled with AG cells (Fig. 2A, B and Fig. 4C, E). The AGs of larger MPs (Fig. 4A, B, D)--and especially FPSHs (Fig. 2C, D and Fig. 5A, B, D, E)--have a less compact, more reticulate appearance. This is due to the apparent breakdown and loss of AG cells, which are replaced by vacuolated areas, or empty spaces surrounded by connective tissue fibers, or else remnants of cell membranes (Fig. 4A, B, D for large MPs; Fig. 5A, B, D, E for FPSHs). In the largest FPSHs (Fig. 6), the AGs were largely empty of cells, but some nuclei and perhaps complete cells remained. In both MPs and FPSHs, well-developed AG cells were characterized by large, darkly stained nuclei within a granular cytoplasm (Fig. 4D, E and Fig. 5E, F). The ejaculatory ducts of both MP and FPSH individuals contained thumbtack-shaped sperm cells (Fig. 5C and Fig. 6A).

Discussion

Our results confirm for the first time that androgenic glands are present in the female-phase simultaneous hermaphrodites of Lysmata wurdemanni, a shrimp species with a protandric simultaneous hermaphroditic sexual system. AGs produce and maintain male external characteristics, testes and associated ducts, and male mating behavior in decapod crustaceans (reviews in Charniaux-Cotton and Payen, 1985; Ventura et al., 2011a). In purely protandric shrimps, AGs atrophy and disappear when the individual changes sex from male to female (Pandalus borealis: Carlisle, 1959; Pandalus platyceros: Hoffman, 1969; Argis dentata: Frechette et al., 1970; Pandalus hypsinotus: Okumura et al., 2005; Pandalopsis japonica: Kim et al., 2006; and Crangon franciscorum: Gavio et al., 2006). Spitschakoff (1912), Charniaux-Cotton (1958), Berreur-Bonnenfant and Charniaux-Cotton (1965), and Charniaux-Cotton and Payen (1985) considered Lysmata seticaudata to be a purely protandric species, although they observed and described the small testicular portion, male ducts, and spermatogenesis of the otherwise ovarian gonads in the "female" phase. However, no mating experiments were reported by them.

It was not until 1998 that Bauer and Holt (Lysmata wurdemanni) and Fiedler (Lysmata amboinensis) observed mating among these individuals, which confirmed that the "female" phase of Lysmata species was a functional simultaneous hermaphrodite, able to mate successfully both as male and female. A PSH sexual system has been demonstrated since then in all Lysmata species tested (Baeza, 2009), as well as in Exhippolysmata oplophoroides (Laubenheimer and Rhyne, 2008) and Parhippolyte misticia (Onaga et al., 2012). In the various Charniaux-Cotton papers cited above, AGs were illustrated for the male phase, but not for the female phase (here termed FPSH), although histological figures or plates were not presented. In a Master's thesis, Bundy (1983) did report the presence of AGs in either the MP or FPSH phases, but those observations were limited and not published.

Our observations and histological evidence definitely show that androgenic glands are present in both the male (MP) and "female" (FPSH) phases of Lysmata wurdemanni. The position, shape, and cellular structure of AGs have been described in other male caridean and protandric (especially) species (e.g., Hoffman, 1969; Frechette et al., 1970; Okumura et al., 2005; Kim et al., 2006). However, in smaller MPs, AGs are compact and replete with androgenic gland cells, similar to sexually active MPs in the protandric species Pandalus platyceros (AG stages 2-3; Hoffman, 1969). In larger MPs and FPSHs, AGs become more reticulate in appearance due to the loss of AG cells, which leaves spaces (vacuolated areas) surrounded by connective tissue fibers and possibly cell remnants (AG stages 4-5 of MPs transforming to FPs; Hoffman, 1969). In the largest FPSHs observed, AGs had scarcely any complete AG cells, with large spaces surrounded by connective tissue fibers and cellular debris (i.e., stage 6, or the "ghost" stage of P. platyceros sex-changing MPs; Hoffman, 1969). A similar atrophy of AGs in sex-changing MPs has been reported in other protandric species, with a loss of androgenic gland cells that are replaced by empty spaces and connective tissue (Okumura et al., 2005; Kim et al., 2006). However, in these protandric species, AGs are completely lost in the female phase (FP), but they persist in FPSHs of L. wurdemanni, albeit in a deteriorated form.

Although our results show that the androgenic glands are retained in the female-phase simultaneous hermaphrodites of L. wurdemanni, attention must be paid to the limitations of our histological methods. Here we show only the gross morphology of AGs and their cellular contents. The ultrastructure of organelles important in hormone secretion (rough endoplasmic reticulum, Golgi apparatus) and other cellular details were not observed so that we could compare possible differences in AG functionality between MPs and FPSHs. Thus, interpretation of our results, and conclusions drawn from them, should be made with caution. However, our results do suggest that protandric simultaneous hermaphroditism is made possible in L. wurdemanni and other PSH species by the retention of AGs and their continued, but reduced, production of AG hormone, the factor responsible for maleness in decapod crustaceans. In Macrobrachium rosenbergii, the expression of AG hormone, male morphology, and mating activity vary with the relative development of AGs among male morphs (Ventura and Sagi, 2012). The partial atrophy of AGs in FPSHs of L. wurdemanni might account for the change of MPs to individuals with an external female phenotype, but which retain full male (and female) reproductive capacity (i.e., FPSHs).

Variation in allocation to male function (mass of stored sperm + testes) and female function (ovarian mass) was measured by Baeza (2007) in FPSHs of L. wurdemanni. Male allocation declined and female allocation increased with increasing FPSH size. These observations are concordant with the presence of androgenic glands and their apparent continual degeneration in the FPSH phase. In L. wurdemanni, and possibly other PSH species, the gradual atrophy of AGs and hypothesized reduction of AG hormone output may trigger the changes and, finally, the molt from MP to FPSH. In this molt, the external male characteristics (e.g., appendices masculinae) are lost and female breeding dress and spawning capacity are completely expressed (Bauer and Holt, 1998). But unlike purely protandric species, in PSH species the androgenic glands of FPSHs--with a reduced number, and presumed functionality, of secretory AG cells (and IAG output)--may account for the observed retention of the male gonopores, reduced male characters, and male mating behavior after sex change.

Protandric simultaneous hermaphroditism is a very advantageous sexual system; the individual can reproduce as a male when young (small), and as a simultaneous hermaphrodite when older and larger. Female-phase simultaneous hermaphrodites are able to reproduce as males with very little cost to female fecundity (Baeza, 2007). Why, then, are there so few PSH species and many more protandric shrimp species, in which female-phase (FP) individuals can reproduce only as females? Ecological situations postulated to lead to simultaneous hermaphroditism in non-sessile invertebrates include low population density and/or reduced mobility (e.g., Ghiselin, 1969). In these situations, where the frequency of contact between potential mating partners is low, simultaneous hermaphroditism is an advantage. A review of the ecology and social organization of Lysmata (Bauer, 2000, 2006) and subsequent work since (Baeza, 2009) show that some species live in low-density populations in FPSH pairs (as tropical fish cleaners). However, other Lysmata species live in small groups or high-density aggregations ("crowd species"). In these groups, especially the high-density aggregations, there is high frequency of contact between sexual morphs. as in purely protandric species. Bauer (2000, 2006) proposed a historical contingency hypothesis, in which the low-density tropical "pair species" are thought to be ancestral to the "crowd" species. However, this hypothesis is not generally supported by phylogenetic studies, as reviewed by Baeza (2013). That researcher proposed an alternative, and as yet untested, hypothesis involving low male mating opportunities and brooding constraints in an ancestral group.

These and other such hypotheses are evolutionary scenarios which assume that particular selective pressures in certain environments result in protandric simultaneous hermaphroditism. If so, these conditions must be rare, as there are so few PSH species compared to protandric species, whose sexual system is satisfactorily explained by the "size advantage model" (Ghiselin. 1969: Warner. 1975). What is an alternative to the sociobiological or ecological explanations for the origin of PSH'.' Perhaps a purely chance event--such as a fortuitious mutation, in protandric species. of the IAG genes, responsible for AG development and expression--accounts for the origin of PSH and its relative rarity in caridean shrimps. If AG shutdown in the male phase were incomplete due to such a mutation, continued but reduced AGs and IAG production could allow for sex change to the female phase. However, there would be partial retention of the male reproductive system and completely functional male mating behavior seen in the female-phase simultaneous hermaphrodites of PSH species. There should be little selection for loss or reversal of PSH. no matter what the social organization or ecological situation. Testing a mutational hypothesis, however, is problematical. It might be accomplished by comparison of 1AG gene structure and expression among gonochoric, purely protandric, and PSH species.

The presence of androgenic glands in female-phase simultaneous hermaphrodites of other PSH species (Lysmata, Exhippolysmata oplophoroides, Parhippolyte misticia) remains to be determined. Importantly, the ultrastructure of AGs in FPSHs of these species may reveal the presence of abundant rough endoplasmic reticulum (RER), which is characteristic of AG secretory activity (Okumura et al., 2005; Kim et al., 2006; Ventura et al., 201 la). Furthermore, techniques used in confirming, measuring, and silencing expression and activity of the insulin-like peptide of the androgenic gland (IAG)--like those used in studies of the gonochoric shrimp Macrobrachium rosenbergii (Ventura et al., 201 la, b; Ventura and Sagi, 2012)--on MPs and FPSHs of L. wurdemanni and/or other PSH species, along with phylogenetic studies (reviewed in Baeza, 2013), may lead to an understanding of how protandric simultaneous hermaphroditism evolved in caridean shrimps.

Acknowledgment

This is Laboratory of Crustacean Research (University of Louisiana, Lafayette) Contribution No. 180.

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JOSE LUIS BORTOLINI (1) AND RAYMOND T. BAUER (2,*)

(1) Departamento de Biologia Comparada, Facultad de Ciencias, Universidad Nacional Autonoma de Mexico, Ciudad de Mexico, D. F., Mexico; and (2) Department of Biology, University of Louisiana, Lafayette, Louisiana 70504-3602

Received 4 December 2015; accepted 25 January 2016.

(*) To whom correspondence should be addressed. E-mail: rtbauer@louisiana.edu

Abbreviations: AG, androgenic gland; CL, carapace length; FP, female phase; FPSH, female-phase simultaneous hermaphrodite; IAG, insulin-like peptide of the androgenic gland; MP, male phase; PSH, protandric simultaneous hermaphroditism.
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Author:Bortolini, Jose Luis; Bauer, Raymond T.
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Date:Apr 1, 2016
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