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A. Legakis, S. Sfenthourakis, R. Polymeni & M . Thessalou-Legaki (eds.) The N e w Panorama of Animal Evolution
Pwc. 18" Int. Congr. Zoology, pp. 439-446, 2003
Spenn Storage in the Class Reptilia
D.M. Sever' & W.C. Hamlett^
1. Department of Biology, Sairit Mary's College, Notre Dame, Indiana 46556 U S A 2. Indiana University School of Medicine, South Bend Center for Medical Education,
Notre Dame, Indiana 46556 U S A
Abstract
Reptilia contains some 7200 species of amniotes whose monophyly is supported by both morphological and molecular characters although sister-group relationships among the four major groups containing extant taxa remain controversial. These groups are Chelonia (turtles), Crocodilia, Rhynchocephalia, and Squamata. The Squamata is the largest group (6900 species) and contains Amphisbaenia, Sauria (lizards), and Serpentes (snakes). Internal fertilization and oviparity most likely are symplesiomorphies for modern reptiles, and vivipari ty has evolved independently numerous times in Sauria and Serpentes. Oviducal sperm storage is known in females of al l the above taxa except Amphisbaenia. In rhynchocephalians and crocodilians, however, sperm storage is poorly studied, and specialized sperm storage tubules (Ssts) are unknown. Ssts arose independently i n Chelonia and Squamata. Turtles possess albumen-secreting glands i n the anterior half of the oviduct (the tuba or isthmus), and the most distal of these glands also serve as Ssts; i n addition, some turtles possess Ssts in the adjacent segment of the oviduct, the uterus. Squa-mates lack albumen-secreting glands, and the ancestral state is possession of Ssts in the posterior infundibulum (uterine tube). Secondarily, iguanids have evolved vaginal Ssts.
Introduction
The Class Reptiha contains some 7200 species and includes Crocodiha (22 species), Chelonia (turtles, 260 species) Rhynchocephalia (2 species), Amphisbaenia (135 species), Sauria (lizards, 3200 species), and Serpentes (snakes, 1800 species; Rough et al. 1998). Amphisbaenids, lizards, and snakes comprise the Squamata, and rhynchocephalians are grouped vifith squamates to form the Lepidosauria. Crocodilians are grouped vk ith birds in the Archosauria, traditionally considered the sister taxon to Lepidosauria, and Chelonia usually is deemed the sister taxon to Archosauria + Lepidosauria (Fig. 1; Rough et al. 1998). Recent molecular work, however, indicates that Chelonia and Archosauria are closest sister-taxa, and thus Chelonia + Crocodiha is the sister group of Squamata (Fig. 1; Hedges & Poling 1999, Kumazawa & Nishida 1999). Rhynchocephalians may have their closest
440 The new panorama of animal evolution
TRADITIONAL
BIRDS
CROCODILIANS
SQUAMATES
TURTLES
MAMMALS
BIRDS
CROCODILIANS
TURTLES
LIZARDS
SNAKES
MAMMALS
T U R T L E S
CROCODILIANS
BIRDS
SQUAMATES
MAMMALS
HEDGES & POLING (1999)
BIRDS
T U R T L E S
LIZARDS
SNAKES
MAMMALS
KUMAZAWA & NISHIDA (1999) THIS STUDY
Fig. 1. Recent molecular studies have changed the w a y we traditionally v iew the phyletic relationships among amniotes. We adopt the v iew that turtles form sister group relationships w i t h crocodilians and birds. Since we have no data on the presence of Ssts i n crocodilians, we omit them form the cladogram that we use to trace reproductive characters. From Sever and Hamlett (2002).
sister-group relationships wi th Chelorua + Archosauria rather than Squamata (Hedges & Poling 1999), thus casting doubt on the Lepidosauria as a natural group.
In tills paper we use the molecular phylogenetic hypothesis ((Chelonia + Archosauria) (Squamata)) to trace evolution of sperm storage characters in reptiles using McClade 3.0 (Maddison & Maddison 1992). This paper is limited to female sperm storage in the oviduct. While little is known on this topic, even fewer observations exist on male sperm storage.
Results and discussion
Crocodilia.—Davenport (1995) reported that a female caiman {Paleosuchuspalpebrosus) laid 16 eggs, in at least one of which an embryo developed, 488 days after isolation from a male. Ferguson (1985) failed to find sperm storage structures in the alligator {Alligator mississippiensis) or the crocodile {Crocodyliis niloticus). Palmer & Guillette (1992) reported that the oviduct of A . mississippiensis has separate uterine regions for formation of the eggshell membranes and calcareous layer similar to those of birds and unlike other reptiles. Sperm storage tubules (Ssts) in birds are uterovaginal, and this area should be searched for similar structures in crocodilians.
Rhjmchocephalia.—Dawbin (1962) stated that 10 months may elapse between copulation and oviposition in the tuatara {Sphenodon punctatus), implying long-term
Sperm Storage in ttie Class Reptil ia 441
sperm storage may occur (St. Girons 1973). No sperm storage structures, however, have been found in the oviduct (Gabe & Saint-Girons 1964).
Amphisbaenia.—To our knowledge, no histological descriptions exist of the oviduct of any amphisbaerud, and we know of no observations on the potential for sperm storage.
Chelonia.—The first description of Ssts in turtles was in the box turtle {Terrapene Carolina) by Hattan & Gist (1975). Subsequently, Ssts were reported from 12 species representing six families (Gist & Jones 1989), and such structures probably exist i n the remaining seven families. Turtles have an extensive area in the anterior half of the oviduct, called the tuba by Gist & Jones (1987), i n which albumen-secreting glands occur. I n the most caudal end of this region some albumen glands also serve as Ssts. I n two species, Sternothenis odoratus and Gopheriis polyphemiis, Ssts also have been reported from the uterine region of the oviduct near the uterovaginal junction (Palmer & Guillette 1988, Gist & Congdon 1998). The only ultrastructural observations on the Ssts of turtles are T E M studies on T. carolinahy Gist & Fischer (1993).
In turtles: (1) sperm are found in glands located at the periphery and not the center of major glandular regions; (2) T E M of the albumen glands of T. Carolina show that tubules containing sperm are identical in ultrastructure to those that do not; (3) Ssts are therefore sites of sperm residence rather than tubules specialized for the maintenance of stored sperm; and (4) despite the lack of glands "specialized" for sperm storage, turtles have perhaps the longest periods of effective sperm storage (up to four years) known among vertebrates.
Serpentes.—The first observations on sperm storage in the oviduct of a female snake was made by Rahn (1940) but speciaHzed Ssts were not described until Fox (1956). No Ssts were found in the brown tree snake {Boiga irregularis) by Bul l etal. (1997), but these glands are no doubt widespread in snakes, and numerous accounts, often anecdotal, exist on long-term sperm storage in various species (reviewed by Sever & Ryan, 1999). The orily ultrastructural studies on the Ssts of snakes concern T E M of the garter snake, Thamnophis sirtalis (Hoffman & Wimsatt 1972), S E M of the ringneck snake, Diadophis punctatus (Perkins & Palmer 1996), and both T E M and S E M of the black swamp snake, Seminatrixpygaea (Sever & Ryan 1999).
Ssts occur i n a short region between the infundibulum and the uterus called the "uterine tube" (Perkins & Palmer 1996) or simply "the posterior infundibulum" to distinguish this region from the more anterior, aglandular regions of the infundibulum (Fox 1956, Blackburn 1998, Sever & Ryan 1999). I n many snakes in temperate regions, however, mating occurs in fall and the sperm are held over-winter i n vaginal or uterine sperm receptacles, and migrate to the tubal Ssts for a brief period of storage prior to ovulation i n the spring (Halpert etal. 1982, Aldridge 1992, Perkins & Palmer 1996).
Snake Ssts are usually characterized as compound alveolar but Sever & Ryan (1999) described them as simple or compound tubular in 5. pygaea. A s reported for turtles, the glands used for sperm storage do not appear specialized for this fimction. The epithelium of the glands and surrounding oviduct are similar in histology and consist of alternating ciliated and non-ciliated secretory cells (Sever & Ryan 1999).
Sauria.—In lizards, Ssts were first discovered and histologically described in the oviducts of the chameleons, Chamaeleo basiliscus, C. chamaeleon, and C. lateralis (Saint Girons 1962) and the green anole, Anolis carolinensis (Fox 1963). Other literature concerning histological studies on lizard Ssts is given in Table 1. The only ultrastructural
442 The new panorama of animal evolution
studies are S E M of the SST area i n A . carolinensis (Conner & Crews 1980) and several species of geckos (Girl ing et al. 1997, 1998), and T E M studies on Ssts of the gecko Acanthodactylus scutellatus (Bou-Resli etal. 1981) and the brown anole, Anolissagrei{Sevex and Hamlett 2002). Both vaginal and infundibular (tubal) Ssts are known (Table 1), and some species i n the Iguanidae (Cuellar 1966) and Agamidae (Saint Girons 1973) apparently have Ssts in both areas.
Comparative biology.—Character states were determined for location of Ssts and various other reproductive characters for reptiles, birds, and mammals (Table 2). Birds are well known to possess Ssts at the uterovaginal junction (Bakst 1987), and mammals either lack Ssts, or store sperm in the uterus or the uterotubal (isthmus) region (e.g., Racey 1979, Bedford & Breed 1994, Suarez 1998). Mapping of these characters on the phylogeny chosen for this study reveals that an ancestral state for Ssts in amniotes cannot be determined and that Ssts evolved independently in birds, turties, squamates, and mammals (Fig. 2).
The ancestral state for squamates is possession of infundibular Ssts. The lizard data from Table 1 can be mapped on a phylogeny of lizards taken from Pough etal. (1998). The result (Fig. 3) indicates that vaginal Ssts are a specialization found i n the Iguania, and that some iguanids also have either retained infundibular Ssts or re-evolved them.
Conclusions
Sperm storage evolved independently in Chelonia and Squamata. The ancestral state for turtles is storage in posterior albumen-producing glands. The ancestral state for squamates is receptacles in the posterior infundibulum (uterine tube). Vaginal Ssts are
Table 1. Literature on location of sperm storage tubules (Ssts) i n l izards. From Sever and Hamlett (2002).
Reference Family Infundibulum Vagina
Agamidae X X Saint Girons 1973, YMmari etal 1990
Anguidae X Saint Girons 1973
Chameleonidae X Saint Girons 1962
Eublepharidae X Cuellar 1966
Gekkonidae X Cuellar 1966; Bou-Resli ^ / 1 9 8 1 ; Murphy-Walker & Haley 1996, Gir l ing ^/^Z. 1997
Iguanidae : X Cuellar 1966, Adams & Cooper 1988
Polychrotidae X Fox 1962, Conner & Crews 1980
Scincidae X Saint Girons 1962, Schaefer & Roeding 1973
Sperm Storage i n the Class Reptilia 443
Table 2. Character states and their polarities for sperm storage tubules (Ssts) and some other reproductive characters in reptiles. From Sever and Hamlett (2002).
A - Fertilization 0 - external 1 - internal
B - Ovary Birds 0 - solid 1 - hollow Turtles
C - Albumen Snakes 0 - present 1 - absent Lizards - 1
D - Ssts Lizards - 2 0 - absent Mammals - 1 1 - posterior infundibulum Mammals - 2 2 - tubal albumen glands 3 - uterovaginal 4 - vaginal 5 - uterus or uterotubal
A B c D
1 0 0 3 1 0 0 2* 1 1 1 1 1 1 1 1 1 1 1 4 1 0 0 0 1 0 0 5
'uterine glands also reported as Ssts in two species of turtles
A ' B C
•H-B ' C ' D '
D5
B I R D S
T U R T L E S
L I Z A R D S - 1
L I Z A R D S - 2
S N A K E S
M A M M A L S - 1
M A M M A L S - 2
Fig. 2. Ssts evolved independently in birds, turtles, squamates, and mammals. A m o n g squamates, the ancestral state is infundibular Ssts, and vaginal Ssts have subsequently evolved in some l izards. From Sever and Hamlett (2002).
secondarily derived in iguanids. Oviducal Ssts in birds (+ crocodilians?) and mammals are also independently derived. A n y similarities among these taxa i n anatomy of the Ssts arise from convergence perhaps due to design constraints of the vertebrate oviduct.
Sperm production, mating, and ovulation are often out of phase wi th one another in reptiles (Schuett 1992). Thus female (as wel l as male) sperm storage is an obligatory part of the reproductive cycle in many species. We know very little about sperm storage in reptiles. Ultrastructural studies are essential to study sperm/epithelial interactions
444 The new panorama of animal evolution
Fig. 3. Vaginal Ssts are a specialization found only i n the Iguania. Some iguanids also have either retained infundibular Ssts or re-evolved them. From Sever and Hamlett (2002).
in Ssts; yet out of 7200+ species of reptiles, we have T E M observations on just one turtle, two lizards, and two snakes. We know virtually nothing about the physiology of sperm storage i n reptiles, i .e. , how viability is maintained and capacitation achieved. Since reptiles are the stem amniote group, they are useful models to include in comparative analyses of oviductal sperm storage mechanisms in birds and mammals. For a more extensive discussion, see Sever and Hamlett (2002).
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