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Comparative Biology of Sperm Storage in Female Salamanders

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Comparative Biology of Sperm Storage in Female Salamanders THE JOURNAL OF EXPERIMENTAL ZOOLOGY 282:460-476 (1998) Comparative Biology of Sperm Storage in Female Salamanders DAVID M. SEVERN* AND ROSSANA BRIZZI' 'Department of Biology, Saint Mary's College, Notre Dame, Indiana 46556 ^Dipartimento di Biologia Animale e Genetica, Universita di Firenze, 50125 Firenze, Italia ABSTRACT Females in seven of the ten families of salamanders possess cloacal glands called spermathecae that store sperm. The annual cycle of sperm storage has been studied by light and electron microscopy in eight species representing five families. In these taxa, we recognized 14 characters associated with the spermathecae and traced their evolution on a phylogeny of sala• manders based upon other characters. The plasticity and phyletic significance of the spermathecal characters varied greatly. Plethodontids have complex spermathecae while other families possess simple spermathecae; thus, this character has phyletic value as well as being highly conserved within the Salamandroidea. Other characters, such as carbohydrate histochemistry, are highly plastic and show no obvious phyletic trends. The significance of some of these variable characters, such as duration of sperm storage, is apparent only after including in the analysis other aspects of the reproductive cycle, such as length of the mating season. Additional comparative studies, em• ploying the protocol used in this paper, will help further clarify the relationships between phyletic and functional variability in sperm storage mechanisms in salamanders. J. Exp. Zool. 282:460- 4 76, 1998. © 1998 Wiley-Liss, Inc. In amphibians with external fertilization (most sperm from those involved in oogenesis, ovula• frogs, some salamanders), close timing must oc• tion, and fertilization. cur among: maturation and transfer of male and In the past decade, we have conducted exten• female gametes (mature, jelly-coated eggs in the sive studies on the annual cycle of sperm storage oviducts and mature, capacitated sperm in the in various salamanders selected with especial em• Wolffian ducts); maximal development of male phasis on their phylogenetic relationships and re• and female secondary sexual characters; male and productive adaptations (Brizzi et al., '89, '95; female sexual urges leading to migration and mat• Sever, '91b, '92a, '94a, '95, '97; Sever and Bru• ing behaviors; and existence of appropriate envi• nette, '93; Sever and Kloepfer, '93; Sever et al., ronmental surroundings. '95, '96a, '96b; Sever and Bart, '96). We believe Female salamanders in the seven families sufficient data exist on a diverse assemblage of composing the suborder Salamandroidea store taxa to allow a first attempt at a synthesis of sperm in exocrine glands, the spermathecae, in the comparative biology of sperm storage in fe• the dorsal roof of the cloaca (Sever, '91a). In male salamanders. Hence, one purpose of this oviparous species, sperm are released on eggs paper is to produce a procedural and phyletic as they pass through the cloaca, so fertilization framework for further studies on sperm storage is internal. The ability to store sperm for ex• in salamanders. We also report our initial find• tended periods before fertilization allows de• ings on the plasticity of spermathecal characters coupling of mating activity from oogenesis, among the urodeles, and analyze the relation• ovulation, and fertilization/oviposition; allows ships of this variability to species-specific repro• delay of fertilization until environmental condi• ductive adaptations. tions are most favorable; allows extension of the mating period; facilitates multiple matings; and provides the conditions for sperm competition (i.e., meeting the criteria established by Parker, Grant sponsor: National Science Foundation; Grant number: DEB 90-24918; Grant sponsor: Ministero DeH'Universita e della Ricerca '84). From a regulatory standpoint, sperm stor• Scientifica e Tecnologica. age permits segregation of hormones involved in *Correspondence to: Dr. David M. Sever, Department of Biology, Saint Mary's College, Notre Dame, IN 46556. E-mail: dsever@saint stimulating mating behavior and storage of marys.edu © 1998 WILEY-LISS, INC. SPERM STORAGE IN FEMALE SALAMANDERS 461 MATERIALS AND METHODS TABLE 2. Spermathecal characters Determination of the annual cycle of sperm 1. Cloacal glands: A = absent; A^ = present storage in the spermathecae requires examina• 2. Spermathecae: B = absent; B^ = present tion of females: sexually active but unmated; 3. Type of spermathecae: C - simple; C^ = complex 4. Histochemistry: D = PAS+; = alcian blue+; D' = both mated, but prior to ovulation, fertilization, and PAS+ and alcian blue+ oviposition; immediately after oviposition; and 5. Secretory vacuoles: E = mixed density; = uniform from various periods following oviposition, ex• density tending into a period when females are not 6. Secretory activity: F = uniform; F^ = regionalized sexually active (Sever, '97). Tissue from the 7. Timing of release of secretion: G = storage; G"*^ = mating; G' = oviposition; G^ = degradation spermathecal area was taken from freshly sac• 8. Mode of release of secretion: H = merocrine; = rificed individuals representing each of these apocrine periods, and the tissue prepared by similar 9. Types of epithelial cells: I = one type; I^ = two types methods (cf., Brizzi et al., '95; Sever, '97) for 10. Spermiophagy by the epithelium: J = absent; = examination by light and transmission electron present throughout; j' = present but regionalized microscopy (TEM). 11. Sperm degradation in the lumen: K = present; K'^ = absent The species that have been studied using this 12. Desquamation of the epithelium: L = epithelium remains protocol are: Ambystoma tigrinum and A. opa- intact; = desquamation into the lumen; 1? = cum in the Ambystomatidae; Amphiuma trida- desquamation into the stroma; = desquamation into ctylum in the Amphiumidae; Eurycea cirrigera both the lumen and the stroma 13. Intraepithelial leukocytes: M = absent; = present and Plethodon cinereus in the Plethodontiade; 14. Duration of sperm storage: N = <1 month; = 1-2 Necturus beyeri in the Proteidae, and Notoph• months; N' = 2-3 months; = 4-5 months; N* = 6 thalmus viridescens and Salamandrina terdigit- months; = >6 months ata in the Salamandridae (Table 1). Our critical review of these studies led to the recognition of a number of characters relating specifically to RESULTS the spermathecae (Table 2). Different states of Fig. 1 shows the result of tracing character evo• these characters were coded numerically with no lution in this manner. Where the nodes for par• prejudice concerning ancestral or derived condi• ticular states were equivocal, one of the equally tion (Tables 3, 4). Using McClade 3.0 (Maddison parsimonious solutions was chosen, except for and Maddison, '92), these characters were map• character A, where the ancestral state for cau- ped on a phylogeny of the taxa based upon the dates was left equivocal. The consistency indices preferred cladogram of interfamilial relation• for the characters range from 0.60 to 1.00, with ships of salamanders proposed by Larson and an overall index of 0.80. Dimmick ('93). Character A: Presence of cloacal glands TABLE 1. Species for which the ultrastructure of the annual The ancestral state is equivocal, but cloacal cycle of spermathecal sperm storage has been studied using glands of at least one type are found in all sala• the protocol described in the text mander families except Sirenidae (Figs. 1, 2A; Family Sever, '91a,c). Species Reference Character B: Presence or absence Ambystomatidae of spermathecae Ambystoma opacum Sever and Kloepher, '93 Sever etal.,'95 Hynobiids and cryptobranchids have cloacal Ambystoma tigrinum Sever, '95 glands but lack those that produce spermato- Amphiumidae phores and store sperm (Fig. 2B-D; Sever, '91c). Amphiuma tridactylum Sever et al.,'96b Plethodontiade This condition is considered the ancestral state Eurycea cirrigera Sever, '91b, '92b for females in all families of salamanders except Sever and Brunette, '93 Sirenidae (Fig. 1). Plethodon cinereus Sever, '97 Proteidae Character C: Type of spermathecae Necturus beyeri Sever and Bart, '96 Salamandridae Simple spermathecae characterize six families Notophthalmus viridescens Sever etal,'96a and consist of simple tubuloalveolar glands open• Salamandrina terdigitata Brizzi et al., '89, '95 ing individually into the roof and lateral walls of 462 D.M. SEVER AND R. BRIZZI TABLE 3. Character matrix Character Taxon A B C D E F G H I J K L M N Sirenidae A 0 0 0 0 0 0 0 0 0 0 0 0 0 Cryptobranchidae Al B 0 0 0 0 0 0 0 0 0 0 0 0 Hynobiidae Al B 0 0 0 0 0 0 0 0 0 0 0 0 Ambystoma opacum Al Bi C Di E F G H I J K Li Ml Ni Ambystoma tigrinum Al Bi C D^ E F G' H I J K L M N Amphiuma tridactylum Al Bi C D E F G^ Hi I J K Li M N3 Eurycea cirrigera Al Bi ci D El pi G H I J2 K 1} M N' Plethodon cinereus Al Bi Ci D' E F G H I Jl K L M Necturus beyeri Al Bi c D E F G H II J K L M Notophthalmus viridescens Al Bi c D El F Gi J I Jl K L M Salamandrina terdigitata Al Bi c Di E F G H I Jl K Li Ml the anterior half of the cloaca (Fig. 3A; Sever, tion of the states within the Salamandridae and '94a). Complex spermathecae, found only in the Ambystomatidae are equivocal (Fig. 1). Plethodontidae (the largest family of salaman• ders) consist of compound tubuloalveolar glands Character E: Ultrastructure of the (Fig. SB; Sever, '87, '94a,b). A single common duct secretory vacuoles connects distal acini to the middorsal roof of the This character refers to whether secretory vacu• anterior end of the cloaca. As pointed out by Sever oles have a mixed density (an electron dense core ('94a), the ancestral state is equivocal, and it is surrounded by flocculent material. Fig. 4C), or equally parsimonious to consider either type an• whether they have a uniform electron density, as cestral to the other or to hypothesize that the found in Eurycea cirrigera and Notophthalmus character is polyphyletic.
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