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Sperm Storage in the Class Amphibia

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Sperm Storage in the Class Amphibia © PENSOFT Publishers A. Legakis, S. Sfenthourakis, R. Polymeni & M. Thessaloii-Legaki (eds.) The New Panorama of Animal Evolution Sofia - Moscow Proc. IS"' hit. Coiigr. Zoo/ogi/, pp. 431-438, 2003 Sperm Storage in the Class Amphibia D.M. Sever', L.C. Rania' & R. Brizzi^ 1. Department of Biology, Saint Mary's College, Notre Dame, Indiana 46556 USA 2. Department of Animal Biology and Genetics, University of Florence, Florence, Italy Abstract The three orders of extant amphibians are Caudata, Anura, and Apoda. In salamanders and newts (Caudata), absence of sperm storage in females is the ancestral condition (three families). In the derived condition, sperm storage occurs in cloacal glands called sper• mathecae, and their possession is a synapomorphy for females in the suborder Salaman- droidea (seven families). The anatomy and phylogeny of caudate spermathecae have been studied extensively (reviewed by Sever & Brizzi 1998). Internal fertilization has conver- gently evolved in a few frogs and toads (Anura), but females of just one species, Ascaphus truei Axe. known to possess oviducal sperm storage tubules (Ssts). Ssts of A. truei Are similar anatomically to such glands in squamate reptiles. This similarity is convergence perhaps due to design constraints imposed by the basic structure of the vertebrate oviduct. Al• though all caecilians (Apoda) apparently have internal fertilization and many are vivipa• rous, female sperm storage is unknown. Introduction The Lissamphibia (extant amphibians) consists of three orders, Caudata or Urodela (salamanders and newts, 500 species), Anura (frogs and toads, 4800 species), and Apoda or Gymnophiona (caecilians, 165 species). Sperm storage by females occurs in most species of salamanders, one species of frog, and is unknown in the caecilians. The anatomy of sperm storage glands has been extensively studied in salamanders and was recently reviewed by Sever & Brizzi (1998). Ascaphus /A//CV (Stejneger, 1899) is the only frog in which female sperm storage is known, and this phenomenon has been studied by Noble (1925), Van Dijk (1955,1959), Metter (1964), and Sever etal. (2001). Caudata Sperm storage occurs in all females found in the seven families of salamanders that comprise the suborder Salamandroidea (Sever 1991a, 1994). Instead of oviductal sperm storage, however, sperm are stored in cloacal glands called spermathecae. Possession of 432 The new panorama of animal evolution a cloaca is considered the ancestral condition for vertebrates (Wake 1979, 1987), but salamanders are the only vertebrates in which cloacal sperm storage glands have evolved (Sever 1994). The ancestral condition for salamanders is lack of sperm storage glands, a condition found in three families with external fertilization, Sirenidae, Hynobiidae, and Cryptobranchidae (Sever 1991b, 1994, Sever etal. 1996b). Sever & Brizzi (1998) mapped 14 characters involved with sperm storage in spermathecae on a phylogeny of salamander families taken from Larson & Dimmick (1993). The only character with definite phyletic value is whether sperm storage occurs in a "complex spermatheca" composed of a single compound tubulo-alveolar gland (Plethodontidae) or in "simple spermathecae" consisting of numerous simple tubular glands (other families). The variation in complex spermathecae of plethodontids was described by Sever (2000). The annual cycle of sperm storage has been studied at the ultrastructural level in two Plethodontidae (Sever 1997, Sever & Brunette 1993), three Salamandridae (Brizzi et al. 1995, Sever etal 1996a, 1999,2001), two Ambystomahdae (Sever 1995, Sever & Kloepfer 1993, Sever et al. 1995), one Amphiumidae (Sever et al. 1996c), and one Proteidae (Sever & Bart 1996). Studies still need to be done on representatives of the Rhyacotritonidae and Dicamptodontidae. Thus, female sperm storage has been studied in only 2% of the known species of salamanders, and much diversity exists among the few species that have been studied in reproductive habits and sperm storage characters (Sever & Brizzi 1998). More comparative work is needed before we resolve any of the questions concerning the significance of variability in sperm storage mechanisms among salamanders. Sever & Brizzi (1998) concluded that: (1) sperm storage is an ancient trait in salamanders, evolving in the common ancestor of all the current families in the Salamandroidea; (2) some of the differences observed among taxa in spermathecal characters may not be phyletically informative but related to other species-specific reproductive adaptations; (3) sperm storage is apparently obligatory prior to fertilization in salamandroids so that the dura tion of effective sperm s torage must be considered in any study on the reproduction of these taxa; and (4) storage of sperm facilitates multiple matings and provides the conditions for sperm competition within the spermathecae of salamanders. Anura The presence of sperm in the lumen of the oviducts and in oviducal glands of females of the frog Ascaphus tnielwdLS first reported by Noble (1925). Ascaphus truei \s the sole member of the family Ascaphidae and is generally considered the sister taxon of all other anurans (Ford & Camiatella 1993). Ascaphus truei is associated with cold, clear mountain streams in disjunct populations in the Cascade Moimtains west to the coast from southern British Columbia to northwest California; in the Blue Mountains of southwestern Washington and northeastern Oregon; and in the Rocky Mountains of northern Idaho and western Montana (Metter 1968)'. Of the 4000+ species of anurans, A. trueivs, the only ' The Rocky Mountain populations of Ascaphus have recently been recognized as a new species, A. montanus (Nielson et al. 2001). Sperm Storage in the Class Amphibia 433 species known to engage in copulation. The male possesses a "tail" that, when engorged, forms a sulcus for passage of sperm and is inserted in the cloaca of the female (Noble 1925, Noble & Puhiam 1931, Slater 1931). Copulation has been assumed to be an adaptation that ensures fertilization in fast-moving water (Stebbins & Cohen 1995). Posterior to a short, aglandular infundibular region, the oviduct of ^. /n/t'/possesses: (1) a proximal, convoluted ampullary region where intrinsic tubular glands secrete gelatinous envelopes around eggs; (2) a middle ovisac region where fertilization occurs; and (3) a distal oviductal sinus formed by medial junction of the ovisacs. An oviductal sinus has previously been described in Frogs only for the viviparous African bufonid Nimbaphri/noides occidentalis (Xavier 1973). Sperm storage tubules (Ssts) occur in the anterior portions of the ovisacs and consist of simple tubular glands. Ssts and the rest of the oviductal lining stain positively with the periodic acid-Schiff's procedure for neutral carbohydrates, and this reaction is especially intense in reproductively active females. Sperm were found in the Ssts of gravid females as well as some non-vitellogenic females. The sperm are in orderly bundles in the Ssts, and although occasionally sperm nuclei were embedded in the epithelium, no evidence for spermiophagy was found. Apoda Apparently all caecilians have internal fertilization. The male possesses a cloacal structure called the phallodeum that is everted from the cloaca and serves for intromission of sperm into the female cloaca during copulation (Wake 1979). Many caecilians are viviparous, a derived condition within the Apoda (Wilkinson & Nussbaum 1998). We hypothesize that sperm storage occurs in the oviducts of female caecilians, but no observations on sperm in the oviduct of a female caecilian have yet been made. Comparative biology To date, Ascaphus truei is the only amphibian in which oviductal sperm storage has been reported. Indeed, the only other anamniotes in which oviductal sperm storage is known are elasmobranchs (Pratt 1993, Hamlett etal. 1998, Hamlett & Koob 1999, Hamlett etal. 1999) in the class Chondrichthyes, which is not considered the sister taxon of Amphibia. Females of some teleosts in the Osteichthyes store sperm (Howarth 1974), but they lack homologues to the oviduct (Kardong 1995). Instead sperm are stored in the ovary or a gonaduct (ovarian duct) formed from ovarian tissue (Howarth 1974, Constanz 1989). The extant representatives of Actinistia and Dipnoi, descendant taxa of sarcopterygiian sister groups of amphibians (Schultze 1994), possess oviducts (Millot & Anthony 1960, Wake 1987), and Latimeriais viviparous (Smith etal. 1975) indicating that fertiHzation is internal (Fig. 1). Sperm storage, however, has not been reported in Latimeria or any of the extant lungfish. Thus, no neontological evidence exists for sperm storage as the ancestral state for amphibians. The Lissamphibia is generally considered monophyletic. Most evidence supports a frog + salamander clade (Pough etal. 1998, Fig. 1). As noted previously, sperm storage is unknown in female caecilians, even though internal fertilization apparently occurs in all taxa (Fig. 1), and many caecilians are viviparous (Wilkinson & Nussbaum 1998). In 434 The new panorama of animal evolution Fig. 1. "Scenariogram" showing distribution of internal fertilization and sperm storage in the Lissamphibia with extant sacropterygiians (descendent taxa of piscine ancestors to amphibians) as outgroups. Within the amphibians, sperm storage glands evolved independently in the cloaca in one suborder of salamanders (Salamandroidea) and in the oviduct of one species of frog {Ascaphus truei). From Sever et al. (2001). salamanders, cloacal sperm storage
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