The eggs of Reptilia and Monotremata undergo meroblastic (partial) cleavage and are surrounded by tertiary shell membranes that are proteinaceous secretions of the oviduct (Hughes, 1977). The large yolk mass is enclosed by a choriovitelline membrane as a stage in yolk sac formation, amniogenesis proceeds by a process of folding, and a large allantoic vesicle develops. These characteristics are likely ancestral for amniotes and represent a combination of primitive and derived traits. The tertiary shell membranes (Gray, 1928; Packard and Packard, 1980) and choriovitelline membrane (Mossman, 1987; Elinson, 1989) have possible antecedents among anamniotes. For example, the yolk mass of some amphibians is enclosed and vascularized (Elinson, 1989). The addition of glycoproteins to the oviductal egg is common among vertebrates (Hughes, 1977), and the eggs of Amphibia are enclosed by proteinaceous layers, the egg capsules, secreted by the oviduct (Salthe, 1963). An amniochorion and a large allantoic vesicle are derived amniote characteristics that have no clear antecedent among modern Amphibia.
Meroblastic cleavage has evolved five times among modern vertebrates and is correlated with large yolk quantity in all lineages except teleosts (Collazo et al., 1994). Although some Amphibia ovulate moderately large eggs (Elinson, 1987; Del Pino, 1989), all have holoblastic cleavage, i.e., the egg is completely divided into blastomeres. Meroblastic cleavage, in which the yolk does not divide, is derived among amniotes and likely was associated with production of a large yolked egg. Meroblastic cleavage is an exaptation for increased egg size because of constraints imposed on morphogenesis by holoblastic cleavage (Elinson, 1989). The eggs of Reptilia and Monotremata cleave meroblastically, whereas those of Marsupialia (Tyndale-Biscoe and Renfree, 1987) and Eutheria (Balinsky, 1975) undergo a similar cleavage pattern although little or no yolk is present.
Like all organisms, eggs are defined by distinct functional characteristics that couple requirements for growth and metabolism to sources of these materials. One aspect of variation among the eggs of amniotes is related to differences in the source of materials, or conceptually, variation in the degree of independent existence. Differences in the pattern of exchange between the egg and the environment are a well-studied aspect of comparative egg physiology among amniotes (Packard and Packard, 1988). Expressed as a dichotomy, eggs either exhibit considerable flux of water, gases, and perhaps other molecules during development or they exchange principally gases. The latter pattern Needham (1931) termed "cleidoic". For example, the eggs of birds undergo minimal development prior to oviposition, are enclosed in a thick calcareous eggshell, and require only respiratory exchange and suitable temperature for successful incubation, whereas the eggs of monotremes are retained in utero, are enclosed in a thin shell membrane, and absorb uterine secretions all prior to oviposition.
Provisions to the egg are supplied by vitellogenesis prior to ovulation or by the maternal gonoduct following ovulation (Blackburn et al., 1985). If eggs are to be oviposited, oviductal secretions influence the subsequent pattern of exchange between the egg and the incubation environment. These secretions include albumen, proteins of the eggshell membranes, and inorganic minerals of the eggshell (Packard and DeMarco, 1991; Palmer and Guillette, 1991). Eggshells are composed of an inner, proteinaceous shell membrane and an outer inorganic layer (Packard and DeMarco, 1991). Both layers are variable among species of amniotes. Eggshells of oviparous species can be classified as either flexible or rigid based on the relative differences in thickness of the two layers and the degree of compactness of mineral units in the outer layer (Packard and Demarco, 1991).
Water movement into and out of the egg is correlated with the degree of mineralization of the eggshell (Ewert, 1985; Packard and Packard, 1988; Ackerman, 1991; Packard, 1991). The monotreme eggshell is not mineralized (Hughes, 1977) and undergoes exchange, at least during intrauterine development (Flynn and Hill, 1939; Hughes, 1984). Eggshell structure varies considerably among turtles (Ewert, 1985; Packard and Packard, 1988), but based on physical characteristics, eggshells have been defined as either pliable, hard-expansible, or brittle (Ewert, 1985). Using the dichotomy, rigid vs. pliable, Iverson and Ewert (1991) compared variation in eggshell characteristics to a cladogram for turtles. The resulting pattern revealed that eggshell rigidity is not phylogenetically constrained because few clades exhibit only a single shell type. Further, the most likely explanation for the pattern of eggshell distribution is that pliable shelled eggs are primitive and that rigid shelled eggs have evolved independently at least five times among turtles (Iverson and Ewert, 1991).
The eggshells of squamates also vary, but all are flexible except for members of two subfamilies of gekkonid lizards (Packard and Packard, 1988). Unlike other squamates, in which the degree of mineralization is slight, these species have rigid eggshells that are heavily mineralized (Packard and Hirsch, 1989). The tuatara eggshell is flexible but differs structurally from most squamates (Packard et al., 1982). All crocodilians and birds produce heavily mineralized, rigid eggshells (Packard and DeMarco, 1991).
The distribution of flexible and rigid eggshell types among modern amniotes is most easily explained if the primitive amniote eggshell was flexible (Figure 6). This condition is present in monotremes and primitive lepidosaurs and likely is primitive for turtles (Iverson and Ewert, 1991). A mineralized eggshell membrane is a synapomorphy for Reptilia (Packard, 1994). A heavily mineralized, rigid eggshell evolved independently among archosaurs, some gekkonid lizards and at least five times among turtles.
In addition to contributing a substantial layer of minerals to the egg, the oviduct of archosaurs secretes a large mass of albumen which surrounds the yolk (Romanoff and Romanoff, 1949; Ferguson, 1982, 1985). The hydrophilic albumen traps and binds water and thus serves as a water reservoir during passage of the egg through the oviduct. This water is transferred to the yolk following oviposition (Romanoff and Romanoff, 1949; Hamilton, 1952; Ferguson, 1985). In contrast, the eggs of monotremes (Hughes, 1977; Hughes and Carrick, 1978) and lepidosaurs (Packard et al., 1977; Packard and Packard, 1988) contain little albumen, but see Tracy and Snell (1985) for an alternative interpretation for lepidosaurs. Recently, the first detailed study of protein during egg development in a lepidosaur, Anolis pulchellus, demonstrated that the oviduct does not contribute an albumen layer to the egg and water contributed by the oviduct is stored in yolk (Cordero-Lopez and Morales, 1995). This pattern may be typical for lepidosaurs with flexible eggshells. The calcareous eggs of geckos have not been studied. The amount of albumen supplied to eggs of archosaurs, lepidosaurs, and monotremes, is apparently correlated with the water flux characteristic of the eggs; eggs with rigid eggshells that do not take up water from the substratum contain a large mass of albumen. One possible hypothesis is that provision of a large amount of albumen evolved in heavily mineralized, rigid eggshells for water storage.
Turtle eggs provide a test for this hypothesis because all are provisoned with a substantial amount of albumen, yet they vary widely in water flux physiology and eggshell composition (Ewert, 1979; Packard and Packard, 1988). Ewert (1979) provides data for 15 species of turtles for which eggshell type and yolk and albumen quantities are known. For these species, albumen constitutes approximately one-half (X = 0.53 ± 0.06 SD) of the total mass of yolk plus albumen. Species with brittle shells (N = 7) do not differ significantly from species with parchment shells (N = 8) (F = 0.68, df 1,14, P = 0.42). Among these turtles, quantity of albumen is not correlated with eggshell type. If pliable eggshells are primitive for
Monotremata Chelonia Sphenodontida Squamata Archosauria
Monotremata Chelonia Sphenodontida Squamata Archosauria
turtles (Iverson and Ewert, 1991), the evolution of large albumen stores must have preceeded the evolution of rigid eggshells.
The phylogenetic distribution of quantity of albumen provision to eggs is most simply explained by the evolution of a large albumen provision within pliable shelled eggs of the earliest Reptilia (Fig. 6). Reduction in albumen provision is derived for Lepidosauria and the primitive condition is retained among Chelonia and Archosauria. An alternative hypothesis, which results in an evolutionary sequence only slightly more complex, is that a small albumen provision is primitive for Reptilia. This hypothesis requires that Lepidosauria retained the primitive condition (Packard and Packard, 1980) and Chelonia and Archosauria independently evolved large albumen stores.
Development of the yolk sac of Reptilia proceeds in three stages, each producing a distinct structure (Romanoff, 1960; Ewert, 1985; Ferguson, 1982, 1985; Stewart, 1993). The primary yolk sac is an extension of the area opaca that grows over the surface of the yolk to form a bilaminar omphalopleure (ectoderm and endoderm) (Hill, 1897). The bilaminar omphalopleure is converted to a vascularized trilaminar omphalopleure, the choriovitelline membrane (Mossman, 1937), by the insertion of mesoderm between the layers of ectoderm and endoderm. The choriovitelline membrane is the secondary yolk sac. The choriovitelline membrane is transitory because it is disrupted by the formation of a cavity, the extraembryonic coelom, within the mesodermal layer (Agassiz, 1857; Romanoff, 1960; Stewart, 1985). Development of the extraembryonic coelom produces the terminal yolk sac, the yolk sac splanchnopleure (endoderm and mesoderm), and the outer somatopleure (mesoderm and ectoderm). This sequence of events occurs in all Reptilia. In addition to the three stages outlined previously, a unique yolk sac membrane develops among Squamata (Weekes, 1935; Yaron, 1985; Stewart and Blackburn, 1988; Stewart, 1993). This tissue is formed from mesoderm that proliferates into the yolk mass (intravitelline mesoderm) and cavitates to form the yolk cleft. The inner margin of the yolk cleft is lined by splanchnopleure that is continuous with the yolk sac splanchnopleure originally associated with the choriovitelline membrane. The outer boundary of the yolk cleft, also splanchnopleure, forms the inner margin of the isolated yolk mass. The bilaminar omphalopleure lies at the perimeter of the isolated yolk mass. The isolated yolk mass is a synapomorphy for Squamata, or possibly Lepidosauria; the development of the yolk sac has not been studied in Sphenodon. The function of this structure is unknown, but as a result of its formation the outer boundary of the yolk sac at the abembryonic pole of squamates is unlike that of any other Reptilia. Blood vessels associated with the yolk sac are separated from the shell membrane by a nonvascular bilaminar omphalopleure, a narrow mass of yolk, and an extraembryonic coelom.
In the terminal stage of incubation, the yolk sac of monotremes consists of two structurally distinct regions (Hughes, 1993). The dorsal surface of the yolk sac, which faces the amnion, is splanchnopleuric, whereas the choriovitelline membrane surrounds the remainder of the perimeter of the yolk and is in apposition to the shell membrane. This pattern is similar to a stage in development of the yolk sac of Reptilia. Development of the extraembryonic coelom adjacent to the embryo in Reptilia occurs during amniogenesis (Fisk and Tribe, 1949; Romanoff, 1960) and this cavity subsequently extends within the choriovitelline membrane about the perimeter of the yolk. Because there are no structural equivalents among Amphibia, the polarity of yolk sac structure is uncertain. Either monotremes are paedomorphic for this character or they represent the condition of the ancestral amniote egg. In marsupials, both a bilaminar omphalopleure and a choriovitelline membrane invest different regions of the yolk (Tyndale-Biscoe and Renfree, 1987). The terminal stage in yolk sac development among eutherians is basically one of three different conditions, a choriovitelline membrane, a yolk sac splanchnopleure, or a novel structure, an inverted yolk sac (Mossman, 1987).
The amniochorion is a synapomorphy for Amniota and the process of development by folding is similar in all Reptilia (Fisk and Tribe, 1949; Romanoff, 1960) and most Mammalia (Luckett, 1977). Details of amniogenesis are known for relatively few species of Reptilia, complicating any attempt to discern phylogenetic patterns. Two basic patterns of amniogenesis occur among amniotes-by the formation of folds and by cavitation. An analysis of the evolution of amnion formation by cavitation among Mammalia (Luckett, 1976, 1977) indicates that this developmental pattern is derived and the formation of amniotic folds, characteristic of Reptilia, is primitive. Amniogenesis by folding occurs as folds of the blastoderm in the head and trunk region of the embryo grow to extend over the embryo. The folds in the trunk region are composed entirely of ectoderm and constitute the seroamniotic connection (Fisk and Tribe, 1949). The seroamniotic connection is apparently a feature of amniogenesis in all amniotes in which amniotic folds develop. It is reported in monotremes (Hughes, 1984), turtles (Mitsukuri, 1891), lepidosaurs (Dendy, 1899; Hrabowski, 1926; Fisk and Tribe, 1949), and archosaurs (Fisk and Tribe, 1949; Romanoff, 1960). A permanent seroamniotic connection has been reported in monotremes (Hughes, 1984), turtles (Mitsukuri, 1891) and tuatara (Dendy, 1899). However, Fisk and Tribe (1949) examined specimens of tuatara analyzed by Dendy (1899) and found no evidence of a permanent seroamniotic connection. The seroamniotic connection is invaded by mesoderm in lizards and this new structure persists throughout embryonic development (Hrabowski, 1926). Among birds, the seroamniotic connection is invaded by mesoderm and then develops perforations that connect to the albumen sac (Romanoff, 1960).
An additional reported variation in amniogenesis is the pattern of closure of the amnion over the tail region of the embryo. In some species, the folds posterior to the seroamniotic connection of the trunk region form a circular opening to the amniotic cavity, the amniotic navel (Fisk and Tribe, 1949; Romanoff, 1960). In turtles (Mitsukuri, 1891), tuatara (Dendy, 1899; Fisk and Tribe, 1949), lizards (Fisk and Tribe, 1949), and birds (Romanoff, 1960) an extension of the seroamniotic connection forms a long tube posterior to the body of the embryo. This tube, the posterior amniotic tube, connects the amniotic cavity to the cavity under the vitelline membrane.
Amniogenesis by folding was likely a process characteristic of the ancestral amniote egg. In all extant amniotes, a dorsal sheet of ectoderm, the seroamniotic connection, develops during amniogenesis. The development of an extraembryonic coelom adjacent to the embryo occurs in all extant amniotes during later stages of amniogenesis. Based on developmental pattern, Fisk and Tribe (1949) suggested that the seroamniotic connection is the homolog of the ancestral amniochorion. The possibility that this structure is retained in monotremes (Hughes, 1984, 1993) and turtles (Mitsukuri, 1891) but lost in lepidosaurs (Hrabowski, 1926; Fisk and Tribe, 1949) and archosaurs (Romanoff, 1960) distinguishes Diapsida from Anapsida and Monotremata.
The allantois is a synapomorphy for Amniota and an expanded allantoic vesicle is characteristic of monotremes and Reptilia (Luckett, 1977; Mossman, 1987). The pattern of distribution of the allantois is related to the development of the yolk sac. In monotremes, the permanence of the choriovitelline membrane restricts the allantois to the embryonic pole (Hughes, 1993). Among turtles (Agassiz, 1857), crocodilians (Ferguson, 1985), and birds (Romanoff, 1960), yolk sac splanchnopleure develops and the allantois expands into the extraembryonic coelom to enclose the entire egg contents. Among squamates (Stewart, 1993), expansion of the allantois follows two patterns: The allantois extends about the periphery of the egg as the isolated yolk mass is absorbed, or it extends into the yolk cleft and does not contact the perimeter of the egg at the abembryonic pole. The greatest variation in the development and structure of the allantois is associated with viviparity (Luckett, 1977; Mossman, 1987; Blackburn, 1993).
In addition to secretions contributing to albumen and eggshell formation, the oviduct of amniotes may contribute to embryonic nutrition by providing other organic and inorganic molecules (Blackburn et al., 1985). The degree of nutrient provision, or matrotrophy, would be expected to be related to the length of egg retention and thus most highly developed among viviparous species. The prevalence of matrotrophy among oviparous species has not been studied, but the absorption of uterine secretions by the eggs of monotremes (Flynn and Hill, 1939; Hughes, 1984) indicates that this pattern of embryonic nutrition is not restricted to viviparous species. Extended egg retention and viviparity result in a relationship between the egg and the developmental environment that may differ substantially from that of eggs oviposited at early embryonic stages. The pattern of water provision differs, respiratory constraints may differ, and the source of nutrition may differ, all of which may require embryonic modifications to access new sources or alter acquisition strategies. As a result, we might expect the greatest differences among amniote eggs and embryos to be correlated with reproductive mode. The development and structure of the extraembryonic membranes of viviparous amniotes (marsupials, eutherians, and squamates) are impressively diverse and the evolution of amniote placentation has been analyzed in numerous previous publications (Weekes, 1935; Mossman, 1937, 1987; Amoroso, 1952; Bauchot, 1965; Luckett, 1974, 1975, 1976, 1977, 1980; Yaron, 1985; Blackburn, 1985, 1993;
Stewart, 1993). A detailed review of placentation is beyond the scope of this work except to emphasize the general categories of diversity as they relate to the extraembryonic membranes. The primary placental exchange tissues of amniotes include allantoplacentation and several types of yolk sac placentation. In marsupials, squamates, and some eutherians, the choriovitelline membrane develops a functional interaction with the uterus, the choriovitelline placenta (Mossman, 1987; Tyndale-Biscoe and Renfree, 1987; Stewart, 1993). The choriovitelline placenta is permanent in marsupials and a few eutherians, but transitory in Squamata and most Eutheria. Many Eutheria (for example, rodents, lagomorphs, some Insectivora, and Chiroptera) have an inverted yolk sac placenta (Mossman, 1987). This structure results from the collapse of the yolk sac such that the opposing yolk sac membranes are placed in proximity. In some species, the splanchnopleuric yolk sac is apposed to a bilaminar omphalopleure; in others, the bilaminar omphalopleure is absent. In either condition, the yolk sac splanchnopleure adjacent to the embryo provides circulatory support for the embryonic side of the placenta. Two additional forms of yolk sac placentation occur among squamates and are associated with the isolated yolk mass-the omphaloplacenta and omphalallantoic placenta (Stewart, 1993). The allantois does not participate in placentation in most marsupials (Tyndale-Biscoe and Renfree, 1987), but does contribute to a diverse array of placental forms among squamates and eutherians (Mossman, 1937, 1987; Luckett, 1977; Blackburn, 1993).
The distribution of reproductive mode among modern amniotes indicates that oviparity is primitive and that viviparity has evolved once among Mammalia and numerous times among Lepidosauria. The clades Chelonia and Archosauria are oviparous and lecithotrophic. Matrotrophy evolved among Mammalia and independently among several lineages of Squamata.
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