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The Theropod Reproductive System

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The Theropod Reproductive System GAIA N°15, LlSBOAlLISBON, DEZEMBROIDECEMBER 1998, pp. 389-397 (ISSN: 0871-5424) THE THEROPOD REPRODUCTIVE SYSTEM Peter L. LARSON Black Hills Institute of Geological Research. Inc. PO Box 643, Hill City, SO 57745. USA ABSTRACT: Soft tissue preservation in theropods is extremely rare, and preservation of re­ productive soft tissue in vertebrate fossils is virtually unknown. It is possible, however, to draw conclusions about the theropod reproductive system by direct observation of fossil - evidence, along with inferences based upon the reproductive systems of extant crocodiles and birds -theropods' closest living relatives. The gender of a theropod probably was deter­ mined by sex chromosomes, with females the heterogametic sex. Male theropods ' pos­ sessed internal testes and a retractable penis. Females possessed paired ovaries and oviducts, along with a crocodilian-like system of storing mature eggs awaiting fertilization. Egg clutches of one to two dozen, or more, were laid at one sitting with the female laying a pair of eggs and then pivoting around the center ofthe clutch a few degrees before she lay her next pair. At least some theropods incubated their eggs, again confirming that they were very probably endotherms. RESUME: La preservation des parties molles des theropodes est extremement rare, tandis que celie des parties molles du systeme reproducteur est pratiquement inconnue en ce qui concerne les vertebres fossiles. Cependant, il est possible d'arriver a des conclusions quant au systeme reproducteur des theropodes par I'observation directe des fossiles, ainsi qu'en faisant quelques deductions fondees sur Ie systeme reproducteur des crocodiles et des oiseaux, seuls parents proches des theropodes encore existants. Le sexe des theropo­ des etait probablement determine par des chromosomes sexuels, les femelles representant Ie sexe heterogame. Les males theropodes possedaient des testicules internes et un penis retractile. Les femelles possedaient des ovaires apparies et des oviductes, ainsi qu'un sys­ teme de stockage des oeufs prets a etre fecondes proche de celui des crocodiles. Des grap­ pes d'une a deux douzaines d'oeufs, voire plus, etaient pond us en une fois, la femelle pondant une paire d'oeufs puis pivotant autour du centre de la grappe de quelques degres avant de pondre la paire d'oeufs suivante. Quelques theropodes au moins incubaient leurs oeufs, confirmant ainsi a nouveau qu'ils etaient tres probablement endothermes. INTRODUCTION phylogenetic bracket has been explained in detail by WITMER (1995)]. Non-avian theropods have been extinct for 65 million years. Their demise and the subsequent de­ SEXUAL DETERMINATION & DIMORPHISM struction of their bodies by biological, chemical, and meteorological agents have made direct study of In critically examining the biological processes of their soft parts impossible. except for a few rare oc­ extant species related to theropods, we can deter­ currences. Virtually nothing remains, for instance, of mine which of these processes were most likely their reproductive organs. Yet, it is still possible to re­ found in theropods. In considering the reproductive construct much of the basic information about these system, analysis begins with sexual determination soft tissues by studying the fossil remains we do in crocodiles and birds. have: evidence found in theropod skeletons and Most reptiles. amphibians, fishes, insects, and all nests. When this information is coupled with our mammals have sex chromosomes, X and Y, which knowledge about the reproductive systems found in produce enzymes that determine the gender of the theropods' closest living relatives, crocodiles and individual upon fertilization of the egg. The Y chro­ birds, we arrive at a better understanding of how mosome carries the genes for maleness in mam­ these animals' reproductive systems functioned. mals and most insects. However, the Y chro­ [This method of soft tissue inference using an extant mosome carries the genes for femaleness in birds, 389 artigos/papers P.L. LARSON reptiles, and some amphibians and fishes, and it is MALE SEX ORGANS AND FERTILIZATION assumed to be the primitive condition in vertebrates. Male crocodile and bird gonads, the testes, pro­ Females, in these cases, are the heterogametic sex, duce sperm on ly during the breeding season. During the gender with XY chromosomes (as opposed to that time, testes size increases ten-fold in crocodiles the homogametic gender, wh ich carries only XX). (JOAN EN & McNEASE, 1980), and up to 200 to 300 Sexual determination does not stop there, how­ times quiescent weight in birds (WELTY & BAPTISTA, ever. Despite the presence or absence of these 1988). [A duck's testes may equal one-tenth its body chromosomes, bird and crocodile embryos begin weight, with the left testis usually larger than the right life with the essential primordia for developing into (WELTY & BAPTISTA, 1988).] Millions of spermatozoa either sex. Forexample, while the sex of a bird is nor­ are generated, stored in a tube called the epidi­ mally determined by the Y chromosome, in rare oc­ dymis, and delivered during mating through a sec­ casions in nature, and under experimental ond tube called the vas deferens. laboratory conditions, birds have been known to re­ Egg ferti lization (along with delivery of eggs in fe­ verse their sex (WELTY & BAPTISTA, 1988). Equally males) and removal of waste are performed through exceptional is the effect of the temperature of incu­ one opening, the cloaca. Male crocodiles (BELLAIRS, bation upon the sex of a crocodile. Utilizing a derived 1970) possess an intromittent organ, or penis, as do character shared with many species of turtles and snakes, lizards, turtles, and some bird species, in­ some li zards, if crocodile eggs develop in tempera­ cluding ostriches, most water fowl, and galliceans, tures of 28 - 30 ·C, they produce females. If they de­ such as chickens and turkeys (GILL, 1995). It is con­ velop in temperatures of 32 - 34 ·C, they produce structed from the folding of a portion of the floor of ma les. With intermediate temperatures, both sexes the cloaca, which produces a seminal groove that are produced (MAGNUSSON et a/., 1989). conducts the sperm from the vas deferens (BEL­ Because a bird's sex is determined in a more LAIRS, 1970). The penis is erected by the filling of ex­ primitive fashion than in crocodiles (via the effects of pandable blood vessels within a spongy tissue. X and Y chromosomes as opposed to temperature Once erected, the organ projects downward and for­ during incubation), it is appropriate to assume that ward from the cloaca, and thus may enter the cloaca this primitive condition was present in birds' thero­ of the female. During mating, the male usually pod ancestors. Also, like birds, the Y chromosomes climbs on the back of the female, and their tails twist must have carried the genes for femaleness. toward each other until their cloacas contact. The semina l groove essentially becomes a canal be­ In both crocodiles and birds, the male and female cause of the penile engorgement, and sperm emp­ gonads lie in the posterior dorsal area olthe abdomi­ ties from the vas deferens into the cloaca of the nal cavity, near the kidneys. Extrapolating from this female, and finally into the oviduct to fertilize the biological arrangement, it follows that the gonads of eggs (BELLAIRS, 1970). theropods must have been similarly positioned. These sex glands produce reproductive cells and The possession of a penis is a primitive condition secrete hormones which provoke sexual behavior (WELTY & BAPTISTA, 1988), which the birds listed such as courtship and mating. They are also respon­ above derived from their theropod ancestors. Most sible for secondary sexual characters (BELLAIRS, birds, however, do not possess a penis; mating in 1970; WELTY & BAPTISTA, 1988) seen as sexual di­ these more derived avian forms usually involves morphism. only a brief cloacal contact (referred to as a "cloacal kiss") for the transferal of sperm. Both crocodiles and birds exhibit sexual dimor­ phism, as evidenced in gender-specific variations in In reviewing the biology and mating habits of birds' plumage, coloration, ornamentation, behav­ theropods' closest relatives, we can sketch out the ior, or size. We can use these types of clues as excel­ probable structure of the soft tissue of extinct thero­ lent tools to determine theropod gender. For pods. Male theropods certainly possessed testes, example, depending upon the species, male or fe­ and, in a manner similar to their living relatives, male birds may be larger than their counterparts, or stored sperm in the epididymis and delivered it the sexes may be relatively equal in size (GILL, through the vas deferens. Theropods also must 1995). In crocodiles, males are always the larger have possessed a cloaca. This seems probable be­ gender (MAGNUSSON eta/., 1989). Likewise, sexual cause the generally more primitive crocodilians, and dimorphism is evidenced in robust and gracile thero­ the more derived birds originating from theropods, pod dimorphs, where skeletons of the two sexes are possess them. clearly different (CARPENTER, 1990; RAATH , 1990; Male theropods also must have had a penis, or LARSON & FREY, 1992; LARSON, 1994, 1995). The intromittent organ, that could be retracted back question has been in determining which gender is within the cloaca when not in use. This is the state in which, a subject discussed in more detail below. both crocodiles and primitive birds. However, even 390 THE THEROPOD REPRODUCTIVE SYSTEM stronger evidence for the existence of a theropod the paired ovaries attached to a yolk and surrounded penis comes from direct correlations between thero­ by a sac, or follicle. As the egg matures, it becomes pod and crocodile skeletons. larger and more heavily laden with yolk that will nur­ ture the developing embryo. When it reaches a cer­ After copulation, the crocodile penis is pulled tain size, the follicle ruptures and the egg is ovulated back into the cloaca by special "penis retractor" into the body cavity.
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