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Androdioecy and Hermaphroditism in Five Species of Clam Shrimps

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Androdioecy and Hermaphroditism in Five Species of Clam Shrimps Invertebrate Biology x(x): 1–11. © 2013, The American Microscopical Society, Inc. DOI: 10.1111/ivb.12012 1 2 3 Androdioecy and hermaphroditism in five species of clam shrimps 4 (Crustacea: Branchiopoda: Spinicaudata) from India and Thailand 5 6 Justin S. Brantner,1 Donald W. Ott,1 R. Joel Duff,1 La-orsri Sanoamuang,2 7 3 4 1,a 8 Gulli Palli Simhachalam, K. K. Subhash Babu, and Stephen C. Weeks 9 1 Integrated Bioscience Program, Department of Biology, The University of Akron, 10 Akron, Ohio 44325-3908, USA 11 2 Applied Taxonomic Research Center, Department of Biology, Khon Kaen University, 12 Khon Kaen 40002, Thailand 13 3 Department of Zoology, Acharya Nagarjuna University, Guntur, Andhra Pradesh, India 14 4 Department of Marine Sciences, Biochemistry and Microbiology, Cochin University of Science and Technology, 15 Lakeside Campus, Cochin, Kerala, 16, India 16 17 18 Abstract. Crustaceans in the order Spinicaudata display a broad range of reproductive 19 types, ranging from pure hermaphroditism to pure dioecy (separate males and females), and 20 mixes in between. One particularly interesting genus of these “clam shrimps” is Eulimnadia. 21 Based on offspring sex ratios, it has been suggested that all members of the genus are 22 androdioecious: populations consist of mixtures of males and hermaphrodites. However, 23 only two of the ~40 species in this genus have been examined histologically to confirm the 24 presence of ovotestes in the purported hermaphrodites of this group. Here, we report both 25 sex ratio and histological evidence that populations of five additional Eulimnadia species 26 from India and Thailand are indeed mixes of males and hermaphrodites (four species) or 27 hermaphrodite only (one species). Sex ratios of adults and offspring from isolated hermaph- 28 rodites are in accordance with those previously reported for 15 Eulimnadia species, and 29 histological assays of four of the five species show the presence of both testicular and ovar- 30 ian tissue in these hermaphrodites. As has been previously reported, the testicular tissue in 31 members of these Eulimnadia spp. is located in a small section at the distal end of the 32 gonad. In addition, the sperm produced in these hermaphrodites forms distinct plaques of 33 compacted chromatin. Overall, these data are consistent with a single origin of hermaphro- 34 ditism in the Eulimnadia, and support the notion that members of the entire genus are either 35 androdioecious or all-hermaphroditic. 36 Additional key words: Eulimnadia, Conchostraca, breeding systems, ovotestes 37 38 39 40 41 The Branchiopoda (Arthropoda; Crustacea) repre- bers of the Diplostraca (which includes clam 42 sents one of the most ancient crustacean lineages shrimps and water fleas) contain at least five differ- 43 that still includes extant representatives (Walossek ent breeding systems: dioecy (true males and true 44 1993; Martin & Davis 2001; Olesen 2007). The class females), hermaphroditism (individuals capable of 45 Branchiopoda is subdivided into the orders Anostra- self-fertilization due to testicular and ovarian tissue 46 ca, Notostraca, and Diplostraca (Martin & Davis occurring concomitantly in the same reproductive 47 2001; Olesen 2007). These taxa have been exten- tract), androdioecy (hermaphrodites and males), 48 sively studied by evolutionary biologists interested parthenogenesis (asexual reproduction), and cyclic 49 in, among other things, the diversity of breeding sys- parthenogenesis (multiple episodes of asexual repro- 50 tems that exist within and among branchiopod duction followed by marked periods of dioecy) 51 groups (Dumont & Negrea 2002). Specifically, mem- (Hebert & Finston 1993; Sassaman 1995; Martin & 52 Davis 2001; Dumont & Negrea 2002; Olesen 2007; 53 aAuthor for correspondence. Weeks et al. 2008). Of these five breeding systems, 54 E-mail: [email protected] four are found specifically in one suborder of the IVB 12012 Dispatch: 2.1.13 Journal: IVB CE: Tushara Journal Name Manuscript No. B Author Received: No. of pages: 11 PE: Hari Prakash 2 Brantner, Ott, Duff, Sanoamuang, Simhachalam, Babu, & Weeks 1 Diplostraca: the Spinicaudata. Such reproductive One taxon for which a detailed analysis of repro- 2 diversity makes these branchiopods ideal candidates ductive systems is needed is the genus Eulimnadia. 3 for studies of the evolution of breeding systems. Members of Eulimnadia inhabit temporary playas, 4 The suborder Spinicaudata comprises three fami- ditches, and many other ephemeral freshwater habi- 5 lies (Cyzicidae, Leptestheriidae, and Limnadiidae) tats throughout the world, from the tropics to the 6 that are collectively known as “clam shrimps” deserts (Dumont & Negrea 2002). Hermaphrodites 7 (Martin & Davis 2001; Olesen 2007). Historically, produce desiccation-resistant cysts, which they bury 8 sex ratio studies on the Spinicaudata have been the within the top several millimeters of the soil. These 9 method used to identify breeding systems (Sassaman cysts hatch rapidly following hydration under spring 10 1995). Sex ratio determination in clam shrimp popu- and summer conditions (at water temperatures 11 lations is based solely on external morphological above 18°C), releasing a nauplius larva. Larval and 12 characters (i.e., claspers in males, and eggs in juvenile growth is extraordinarily rapid: most 13 females/hermaphrodites). In many species of clam shrimp reach reproductive size in 4–7 d in the labo- 14 shrimps, sex determination occurs 5–8 d following ratory at 27–30°C (Sassaman & Weeks 1993; Weeks 15 hatching from desiccation-resistant eggs (Sassaman et al. 1997), and in as little as 4–6 d in the field 16 & Weeks 1993; Brendonck 1996; Weeks et al. 1997, (Vidrine et al. 1987). The hermaphrodites produce 17 2002). Using these morphological indicators to iden- thousands of eggs in their lifetime, generating 18 tify the sex of individuals in populations of clam clutches ranging from 100 to 300 eggs, one to two 19 shrimps, four breeding systems have been identified times a day (Knoll 1995; Weeks et al. 1997). Sexual 20 in the suborder Spinicaudata: dioecy, androdioecy, dimorphism is pronounced. The thoracic append- 21 hermaphroditism, and parthenogenesis. ages of hermaphrodites are unmodified, but the first 22 Before evolutionary hypotheses regarding the evo- two pairs of thoracic appendages in males undergo 23 lution of breeding systems can be tested within the differentiation into claw-like claspers, which are 24 Spinicaudata, a more accurate assessment of the used to hold on to the margins of a hermaphro- 25 reproductive status of species is necessary. Such dite’s carapace during mating. Natural populations 26 assessments require examinations that extend of Eulimnadia are typically hermaphrodite-biased 27 beyond mere sex ratio determinations. Aside from (Mattox 1954), with some populations completely 28 Wingstrand’s (1978) descriptive account of bran- lacking males (Zinn & Dexter 1962; Stern & Stern 29 chiopod spermatology, which included examination 1971). Weeks et al. (2008, 2009a) have inferred that 30 of some representatives of Spinicaudata, few studies the entire genus Eulimnadia comprises either 31 have looked at the reproductive biology of the Spin- androdioecious or all-hermaphroditic species. 32 icaudata from a cellular and histological perspec- Androdioecious species typically are mixtures of all- 33 tive, despite its importance in understanding hermaphrodite and mixed male/hermaphrodite pop- 34 phylogenetic relationships (Martin & Davis 2001). ulations (Sassaman & Weeks 1993; Weeks et al. 35 A few cellular and histological studies have exam- 2008). Sex is determined in these clam shrimp by a 36 ined clam shrimps in the family Leptestheridae, e.g., Z-W chromosomal system (Weeks et al. 2010) in 37 Leptestheria dahalacensis RUPPELL€ 1837 and Eolep- which there are three chromosomal types: ZZ 38 testheria ticinensis BALSAMO-CRIVELLI 1859 (Tomma- males, ZW “amphigenic” hermaphrodites, and WW 39 sini & Scanabissi Sabelli 1992; Scanabissi Sabelli & “monogenic” hermaphrodites; both hermaphroditic 40 Tommasini 1994; Scanabissi & Mondini 2000). In types can self-fertilize or mate with males (Sass- 41 addition, a few ultrastructural and histological stud- aman & Weeks 1993). When selfing, the monogenic 42 ies have been conducted to assess reproductive hermaphrodites “breed true”, producing 100% 43 diversity in the family Limnadiidae; these have monogenic hermaphroditic offspring, whereas the 44 focused on Eulimnadia texana PACKARD 1871 (Zuc- amphigenic hermaphrodites produce 25% male, 45 ker et al. 1997; Scanabissi et al. 2006), Eulimnadia 50% amphigenic hermaphrodite, and 25% mono- 46 agassizii PACKARD 1874 (Weeks et al. 2005), and genic hermaphrodite offspring when selfed (Sass- 47 Limnadia lenticularis LINNAEUS 1761 (Zaffagnini aman & Weeks 1993). Weeks et al. (2008) used 48 1969; Tommasini & Scanabissi Sabelli 1992; Scan- these sex ratio predictions to assess offspring rea- 49 abissi & Mondini 2002a). Clearly, to better under- rings from isolated hermaphrodites and found 15 50 stand the evolution and diversity of breeding Eulimnadia species to be either androdioecious or 51 systems found within the Spinicaudata, a more all-hermaphroditic. Hermaphrodites from only two 52 extensive examination of the histological and cellu- of these 15 species (E. texana and E. agassizii) have 53 lar structure of clam shrimp reproductive systems been examined histologically (Zucker et al. 1997; 54 must be undertaken. Weeks et al. 2005). Because the genus Eulimnadia Invertebrate
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