Sperm Storage in the Class Amphibia

© PENSOFT Publishers Sofia - Moscow

A. Legakis, S. Sfenthourakis, R. Polymeni & M. Thessaloii-Legaki (eds.) The New Panorama of Animal Evolution

Proc. IS"' hit. Coiigr. Zoo/ogi/, pp. 431-438, 2003

Sperm Storage in the Class Amphibia

D . M . Sever ' , L . C . R a n i a ' & R . B r i z z i ^

1. Department of Biology, Saint Mary's College, Notre Dame, Indiana 46556 U S A 2. Department of A n i m a l Biology and Genetics, University of Florence, Florence, Italy

A b s t r a c t

The three orders of extant amphibians are Caudata, A n u r a , and Apoda. I n salamanders and newts (Caudata), absence of sperm storage in females is the ancestral condition (three families). I n the derived condition, sperm storage occurs in cloacal glands called spermathecae, 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. k n o w n 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. A l though al l caecilians (Apoda) apparently have internal fertilization and many are v i v i p a rous, female sperm storage is unknown.

Introduction

T h e L i s s a m p h i b i a (extant a m p h i b i a n s ) consists of three orders , C a u d a t a or U r o d e l a ( s a l a m a n d e r s a n d n e w t s , 500 species) , A n u r a (frogs a n d toads, 4800 species) , a n d A p o d a or G y m n o p h i o n a (caec i l ians , 165 species) . S p e r m storage b y females occurs i n most species of s a l a m a n d e r s , one species of f rog , a n d i s u n k n o w n i n the caec i l ians . T h e a n a t o m y of s p e r m storage g l a n d s has been e x t e n s i v e l y s t u d i e d i n s a l a m a n d e r s a n d w a s recent ly r e v i e w e d b y Sever & B r i z z i (1998). Ascaphus /A/ /CV (Stejneger, 1899) is the o n l y f rog i n w h i c h female s p e r m storage is k n o w n , a n d this p h e n o m e n o n h a s been s t u d i e d b y N o b l e (1925), V a n D i j k (1955 ,1959) , Metter (1964), a n d Sever etal. (2001).

Caudata

S p e r m storage occurs i n a l l females f o u n d i n the s e v e n f a m i l i e s of s a l a m a n d e r s that comprise the suborder S a l a m a n d r o i d e a (Sever 1991a, 1994). Ins tead of o v i d u c t a l s p e r m storage, h o w e v e r , s p e r m are stored i n c loacal g lands ca l led spermathecae . Possess ion of

432 The new panorama of animal evolution

a c loaca is cons idered the ancestra l c o n d i t i o n for vertebrates ( W a k e 1979, 1987), b u t sa lamanders are the o n l y vertebrates i n w h i c h cloacal s p e r m storage g lands h a v e e v o l v e d (Sever 1994). T h e ancestra l c o n d i t i o n for s a l a m a n d e r s is l ack of s p e r m storage g l a n d s , a condi t ion f o u n d i n three f a m i l i e s w i t h ex terna l fer t i l iza t ion , S i ren idae , H y n o b i i d a e , a n d C r y p t o b r a n c h i d a e (Sever 1991b, 1994, Sever etal. 1996b).

S e v e r & B r i z z i (1998) m a p p e d 14 c h a r a c t e r s i n v o l v e d w i t h s p e r m s t o r a g e i n spermathecae o n a p h y l o g e n y of s a l a m a n d e r fami l i es t aken f r o m L a r s o n & D i m m i c k (1993). T h e o n l y character w i t h def ini te p h y l e t i c v a l u e i s w h e t h e r s p e r m storage occurs i n a " c o m p l e x s p e r m a t h e c a " com pose d of a s ingle c o m p o u n d tubulo-a lveo lar g l a n d (P le thodont idae) or i n " s i m p l e spe rm athe cae " cons is t ing of n u m e r o u s s i m p l e t u b u l a r g l a n d s (other f a m i l i e s ) . T h e v a r i a t i o n i n c o m p l e x spermathecae of p le thodont ids w a s descr ibed b y Sever (2000).

T h e a n n u a l cyc le of s p e r m storage h a s be e n s t u d i e d at the u l t r a s t r u c t u r a l l e v e l i n t w o P le thodont idae (Sever 1997, Sever & Brunet te 1993), three S a l a m a n d r i d a e ( B r i z z i et al. 1995, Sever etal 1996a, 1999,2001) , t w o A m b y s t o m a h d a e (Sever 1995, Sever & K l o e p f e r 1993, S e v e r et al. 1995), one A m p h i u m i d a e (Sever et al. 1996c), a n d one Prote idae (Sever & B a r t 1996). S tudies s t i l l n e e d to be done o n representat ives of the R h y a c o t r i t o n i d a e a n d D i c a m p t o d o n t i d a e . T h u s , female s p e r m storage has been s t u d i e d i n o n l y 2 % of the k n o w n species of s a l a m a n d e r s , a n d m u c h d i v e r s i t y exists a m o n g the f e w species that h a v e been s t u d i e d i n r e p r o d u c t i v e habi ts a n d s p e r m storage characters (Sever & B r i z z i 1998). M o r e c o m p a r a t i v e w o r k i s n e e d e d before w e r e s o l v e a n y of the ques t ions c o n c e r n i n g the s i g n i f i c a n c e of v a r i a b i l i t y i n s p e r m s torage m e c h a n i s m s a m o n g s a l a m a n d e r s .

Sever & B r i z z i (1998) concluded that: (1) s p e r m storage is a n ancient trait i n sa lamanders , e v o l v i n g i n the c o m m o n ancestor of a l l the current famil ies i n the Sa lamandroidea ; (2) some of the differences observed a m o n g taxa i n spermathecal characters m a y not be p h y l e t i c a l l y i n f o r m a t i v e but related to other species-specific reproduct ive adaptations; (3) s p e r m storage is apparent ly obligatory pr i or to fert i l izat ion i n sa lamandro ids so that the d u r a tion of effective s p e r m s torage m u s t be considered i n any s tudy on the reproduction of these taxa; a n d (4) storage of s p e r m facilitates m u l t i p l e mat ings a n d p r o v i d e s the condit ions for s p e r m compet i t ion w i t h i n the spermathecae of sa lamanders .

Anura

T h e presence of s p e r m i n the l u m e n of the oviducts a n d i n o v i d u c a l g lands of females of the f rog Ascaphus tnielwdLS f irst reported b y Noble (1925). Ascaphus truei \s the sole m e m b e r of the f a m i l y A s c a p h i d a e a n d is general ly considered the sister taxon of a l l other a n u r a n s ( F o r d & C a m i a t e l l a 1993). Ascaphus truei is associated w i t h co ld , clear m o u n t a i n streams i n dis junct populat ions i n the Cascade M o i m t a i n s w e s t to the coast f r o m southern B r i t i s h C o l u m b i a to n o r t h w e s t C a l i f o r n i a ; i n the B l u e M o u n t a i n s of s o u t h w e s t e r n W a s h i n g t o n a n d northeastern Oregon; a n d i n the R o c k y M o u n t a i n s of nor thern Idaho a n d w e s t e r n M o n t a n a (Metter 1968)'. O f the 4000+ species of a n u r a n s , A. trueivs, the on ly

' 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 k n o w n to engage i n copulat ion. T h e male possesses a " t a i l " that, w h e n engorged, forms a s u l c u s for passage of s p e r m a n d is inserted i n the cloaca of the female (Noble 1925, N o b l e & P u h i a m 1931, Slater 1931). C o p u l a t i o n has been a s s u m e d to be a n adaptation that ensures fer t i l izat ion i n f a s t - m o v i n g w a t e r (Stebbins & C o h e n 1995).

Poster ior to a short , a g l a n d u l a r i n f u n d i b u l a r region, the o v i d u c t of ^ . /n/t ' /possesses: (1) a p r o x i m a l , c o n v o l u t e d a m p u l l a r y reg ion w h e r e i n t r i n s i c tubular g l a n d s secrete gelat inous enve lopes a r o u n d eggs; (2) a m i d d l e ovisac region w h e r e fer t i l i za t ion occurs ; a n d (3) a d i s t a l o v i d u c t a l s i n u s f o r m e d b y m e d i a l j u n c t i o n of the ovisacs . A n o v i d u c t a l s i n u s h a s p r e v i o u s l y been descr ibed i n Frogs o n l y for the v i v i p a r o u s A f r i c a n b u f o n i d Nimbaphri/noides occidentalis ( X a v i e r 1973). S p e r m storage tubules (Ssts) occur i n the anter ior port ions of the ov i sacs a n d consist of s i m p l e tubular g lands . Ssts a n d the rest of the o v i d u c t a l l i n i n g s t a i n p o s i t i v e l y w i t h the per iodic ac id-Schi f f ' s procedure for n e u t r a l carbohydrates , a n d this react ion i s especia l ly intense i n r e p r o d u c t i v e l y ac t ive females . S p e r m w e r e f o u n d i n the Ssts of g r a v i d females as w e l l as some non-vi te l logenic females . T h e s p e r m are i n o r d e r l y b u n d l e s i n the Ssts , a n d a l t h o u g h occas ional ly s p e r m n u c l e i w e r e e m b e d d e d i n the e p i t h e l i u m , no ev idence for s p e r m i o p h a g y w a s f o u n d .

Apoda

A p p a r e n t l y a l l caec i l ians h a v e i n t e r n a l fer t i l iza t ion . T h e m a l e possesses a c loacal s t r u c t u r e c a l l e d the p h a l l o d e u m that i s e v e r t e d f r o m the c l o a c a a n d s e r v e s for i n t r o m i s s i o n of s p e r m into the female cloaca d u r i n g c o p u l a t i o n ( W a k e 1979). M a n y caecil ians are v i v i p a r o u s , a d e r i v e d condit ion w i t h i n the A p o d a ( W i l k i n s o n & N u s s b a u m 1998). We h y p o t h e s i z e that s p e r m storage occurs i n the o v i d u c t s of female caec i l ians , but no observat ions o n s p e r m i n the o v i d u c t of a female caec i l ian h a v e ye t been m a d e .

Comparative biology

To date, Ascaphus truei is the on ly a m p h i b i a n i n w h i c h o v i d u c t a l s p e r m storage has been reported. I n d e e d , the o n l y other anamniotes i n w h i c h o v i d u c t a l s p e r m storage is k n o w n are e lasmobranchs (Pratt 1993, H a m l e t t etal. 1998, H a m l e t t & K o o b 1999, H a m l e t t etal. 1999) i n the class Chondrichthyes , w h i c h is not considered the sister taxon of A m p h i b i a . Females of some teleosts i n the Osteichthyes store s p e r m ( H o w a r t h 1974), but they lack homologues to the o v i d u c t ( K a r d o n g 1995). Instead s p e r m are stored i n the o v a r y or a gonaduct ( o v a r i a n duct) formed f r o m o v a r i a n tissue ( H o w a r t h 1974, C o n s t a n z 1989).

T h e extant representatives of Ac t in i s t ia a n d D i p n o i , descendant taxa of sarcopterygi ian s ister groups of a m p h i b i a n s (Schul tze 1994), possess o v i d u c t s ( M i l l o t & A n t h o n y 1960, W a k e 1987), a n d Latimeriais v i v i p a r o u s ( S m i t h etal. 1975) i n d i c a t i n g that fer t iHzat ion is i n t e r n a l ( F i g . 1). S p e r m storage, h o w e v e r , h a s not been reported i n Latimeria or a n y of the extant l u n g f i s h . T h u s , no neontological ev idence exists for s p e r m storage as the ancestra l state for a m p h i b i a n s .

T h e L i s s a m p h i b i a i s genera l ly cons idered m o n o p h y l e t i c . M o s t ev idence s u p p o r t s a frog + s a l a m a n d e r c lade ( P o u g h etal. 1998, F i g . 1). A s noted p r e v i o u s l y , s p e r m storage i s u n k n o w n i n female caec i l ians , e v e n t h o u g h in terna l fe r t i l i za t ion a p p a r e n t l y occurs i n a l l taxa ( F i g . 1) , a n d m a n y caeci l ians are v i v i p a r o u s ( W i l k i n s o n & N u s s b a u m 1998). I n


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).

s a l a m a n d e r s , c l o a c a l s p e r m s torage i n s p e r m a t h e c a e i s a s y n a p o m o r p h y for the S a l a m a n d r o i d e a ( F i g . 1) , a n d is u n i q u e w i t h i n vertebrates . A s i d e f r o m Ascaphus, o n l y a f e w a n u r a n s h a v e i n t e r n a l f e r t i l i za t ion , w i t h s p e r m transfer a c c o m p l i s h e d b y c loacal appos i t ion . T h e s e species i n c l u d e Mertensophryne micranotis ( G r a n d i s o n & A s h e 1983) a n d four species of "Nectophrynoides"{sertsti^Nake 1980) w i t h i n the Bufonidae f r o m A f r i c a , a n d Eleurodactyliis jasperi ( W a k e 1978) a n d E. coqui ( T o w n s e n d et al. 1981) w i t h i n the L e p t o d a c t y l i d a e f r o m P u e r t o R i c o . O b v i o u s l y , research needs to be done to determine w h e t h e r o v i d u c t a l s p e r m storage occurs i n caeci l ians a n d i n t e r n a l f e r t i l i z i n g b u f o n i d s a n d l eptodac ty l ids . Ascaphus truei, h o w e v e r , is not the sister t a x o n of a n y caec i l ian or of


the other in te rna l f e r t i l i z i n g frogs ( F i g . 1) , so o v i d u c a l s p e r m storage m u s t be cons idered i n d e p e n d e n t l y d e r i v e d i n A. truei.

T h u s , o v i d u c t a l s p e r m storage i n Ascaplms truei i s a c lassic e x a m p l e of h o m o p l a s y t h r o u g h convergence (Sanderson & H u f f o r d 1996). S t ruc tura l a n d funct ional s imi lar i t i es i n s p e r m storage b e t w e e n A. trueiarvd other vertebrates w i t h o v i d u c t a l s p e r m storage therefore are not b a s e d u p o n direct descent b u t related either to s i m i l a r f u n c t i o n a l adaptations a n d / o r to internal des ign restraints (Wake 1991). I n the latter case, s t ruc tura l a n d p h y s i o l o g i c a l constraints o n the basic vertebrate o v i d u c t a n d s p e r m morpholog ies m a y l i m i t the opt ions for e x p r e s s i o n of o v i d u c t a l s p e r m storage.

T h e group of anamniotes p h y l e t i c a l l y closest to frogs a n d w i t h w h i c h frogs share the m o s t d e v e l o p m e n t a l s i m i l a r i t i e s (the closest ge ne ra t ive s y s t e m . W a k e 1996) i s the C a u d a t a . N u m e r o u s d i f f e r e n c e s , h o w e v e r , o c c u r b e t w e e n the s p e r m a t h e c a e of s a l a m a n d e r s a n d the Ssts of Ascaplms truei T h e d i s t a l port ions of the spermathecae of s a l a m a n d e r s are t y p i c a l l y a lveolar , lack c i l i a , a n d possess basa l m y o e p i t h e l i u m (Sever & B r i z z i 1998). Secretory ac t iv i ty i n sa lamander spermathecae is somet imes regional ized a n d seasonal , d e p e n d i n g u p o n the taxa (Sever 1994). A great dea l of v a r i a t i o n also occurs i n react ion to carbohydrate stains w i t h , h o w e v e r , most species s h o w i n g A B + react ions for c a r b o x y l a t e d g l y c o s a m i n o g l y c a n s (Sever 1994).

I n some forms the s p e r m are i n order ly a r r a y s i n the spermathecae (Sever a n d H a m l e t t 1998) w h e r e a s i n others , s p e r m are i n tangled masses (Sever et al. 1999). A l i g n m e n t of s p e r m m a y d e p e n d to some degree u p o n the a n a t o m y of the spermatheca (more o r d e r l y i n c o m p o u n d g l a n d s t h a n s i m p l e t u b u l a r ) . S p e r m i o p h a g y b y the s p e r m a t h e c a l e p i t h e l i u m h a s been descr ibed i n v a r i o u s taxa of s a l a m a n d e r s (Sever & B r i z z i 1998).

T h e Ssts of Ascaphus truei more c losely resemble those of squamate repti les ( F o x 1956, G i r l i n g etal. 1997, Sever & R y a n 1999). O v i d u c t a l s p e r m storage g lands are k n o w n f r o m a l l groups i n the rept i le -b i rd c lade except A m p h i s b a e n i a ( i n w h i c h they l i k e l y occur) a n d R h y n c h o c e p h a l i a ( G i s t & Jones 1987). L i k e rept i les , the Ssts of A. truei dcce s i m p l y cont inuat ions of the o v i d u c a l l i n i n g , a n d conta in c i l iated non-secretory cel ls a n d n o n -ciHated secretory cel ls . M y o e p i t h e l i u m is absent, but the o v i d u c t possesses l a y e r s of s m o o t h m u s c l e ( tunica m u s c u l a r i s ) s u p e r f i c i a l to the m u c o s a . T h e l i n i n g s a n d g lands of rept i l i an oviducts are general ly described as P A S + , l ike those oiA. truei, w i t h little reaction to ac id ic mucosubstances . S p e r m i n the Ssts of A. truei axe genera l ly i n close a l ignment , a l t h o u g h i n squamates , this condi t ion v a r i e s ( F o x 1956, Sever & R y a n 1999). A l t h o u g h s p e r m n u c l e i are somet imes f o u n d e m b e d d e d i n Ssts of repti les (Sever & R y a n 1999) a n d of A. truei, no ev idence exists for s p e r m i o p h a g y i n these taxa .

I n conc lus ion , o v i d u c a l Ssts i n d is tant ly related vertebrate taxa s h o w more s imi lar i t ies t h a n ex is t b e t w e e n Ssts i n Ascaphus truei and spermathecae i n s a l a m a n d e r s , m e m b e r s of sister taxa . T h e basic s t ructure of the vertebrate o v i d u c t , therefore, m a y l i m i t the range of features associated w i t h o v i d u c a l s p e r m storage. F o r a m o r e ex tens ive d i s c u s s i o n , see Sever (2001).

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Sperm Storage in the Class Amphibia

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