ABSTRACT
The reproductive diversity of extant cartilaginous fishes (class Chondrichthyes) is extraordinarily broad, reflecting more than 400 million years of evolutionary history. Among their many notable reproductive specialisations are viviparity (live-bearing reproduction) and matrotrophy (maternal provision of nutrients during gestation). However, attempts to understand the evolution of these traits have yielded highly discrepant conclusions. Here, we compile and analyse the current knowledge on the evolution of reproductive diversity in Chondrichthyes with particular foci on the frequency, phylogenetic distribution, and directionality of evolutionary changes in their modes of reproduction. To characterise the evolutionary transformations, we amassed the largest empirical data set of reproductive parameters to date covering nearly 800 extant species and analysed it via a comprehensive molecular-based phylogeny. Our phylogenetic reconstructions indicated that the ancestral pattern for Chondrichthyes is 'short single oviparity' (as found in extant holocephalans) in which females lay successive clutches (broods) of one or two eggs. Viviparity has originated at least 12 times, with 10 origins among sharks, one in batoids, and (based on published evidence) another potential origin in a fossil holocephalan. Substantial matrotrophy has evolved at least six times, including one origin of placentotrophy, three separate origins of oophagy (egg ingestion), and two origins of histotrophy (uptake of uterine secretions). In two clades, placentation was replaced by histotrophy. Unlike past reconstructions, our analysis reveals no evidence that viviparity has ever reverted to oviparity in this group. Both viviparity and matrotrophy have arisen by a variety of evolutionary sequences. In addition, the ancestral pattern of oviparity has given rise to three distinct egg-laying patterns that increased clutch (brood) size and/or involved deposition of eggs at advanced stages of development. Geologically, the ancestral oviparous pattern arose in the Paleozoic. Most origins of viviparity and matrotrophy date to the Mesozoic, while a few that are represented at low taxonomic levels are of Cenozoic origin. Coupled with other recent work, this review points the way towards an emerging consensus on reproductive evolution in chondrichthyans while offering a basis for future functional and evolutionary analyses. This review also contributes to conservation efforts by highlighting taxa whose reproductive specialisations reflect distinctive evolutionary trajectories and that deserve special protection and further investigation.
Subject(s)
Phylogeny , Viviparity, Nonmammalian , Animals , Female , Viviparity, Nonmammalian/physiology , Reproduction/physiology , Biological EvolutionABSTRACT
According to a longstanding paradigm, aquatic amniotes, including the Mesozoic marine reptile group Ichthyopterygia, give birth tail-first because head-first birth leads to increased asphyxiation risk of the fetus in the aquatic environment. Here, we draw upon published and original evidence to test two hypotheses: (1) Ichthyosaurs inherited viviparity from a terrestrial ancestor. (2) Asphyxiation risk is the main reason aquatic amniotes give birth tail-first. From the fossil evidence, we conclude that head-first birth is more prevalent in Ichthyopterygia than previously recognized and that a preference for tail-first birth likely arose in derived forms. This weakens the support for the terrestrial ancestry of viviparity in Ichthyopterygia. Our survey of extant viviparous amniotes indicates that fetal orientation at birth reflects a broad diversity of factors unrelated to aquatic vs. terrestrial habitat, further undermining the asphyxiation hypothesis. We propose that birth preference is based on parturitional mechanics or carrying efficiency rather than habitat.
Subject(s)
Fossils , Reptiles , Animals , Reptiles/anatomy & histology , FetusABSTRACT
In viviparous Mexican fishes of the family Goodeidae, embryos develop in the maternal ovarian lumen. They typically absorb maternal nutrients during gestation by means of "trophotaeniae," that is, specialized, elongated extensions of the hindgut that are exposed to the fluids, which occupy the ovarian lumen. The sole exception is Ataeniobius toweri, whose embryos lack trophotaeniae but are nevertheless matrotrophic. Thus, how its embryos obtain maternal nutrients is unclear. We studied a series of non-pregnant and pregnant ovaries of A. toweri using histology to identify the mechanism of maternal-embryo nutrient transfer. By early-gestation, embryos have depleted their yolk supplies. Yolks are released into the ovarian lumen and are ingested by the developing embryos, as shown by yolk material in their digestive tracts. The embryonic gut is lined by an epithelium consisting of columnar cells with apical microvilli, providing a means for nutrient absorption. Contrary to statements in the literature, embryos develop minuscule trophotaenial rudiments that extend slightly into the ovarian lumen. These structures are formed of an absorptive epithelium that overlies a vascular stroma, similar to the trophotaeniae of other goodeids. Through late gestation, vitellogenic follicles form and oocytes are discharged into the ovarian lumen, contributing to embryonic nutrition. Thus, histological evidence suggests that embryos chiefly obtain nutrients from ingestion of yolk and maternal secretions released into the ovarian lumen. This function possibly is supplemented by uptake via the small hindgut protrusions and other absorptive surfaces (e.g., the skin and the gill epithelium). Our observations are consistent with two evolutionary interpretations of the hindgut protrusions: (a) that they are rudimentary, evolutionary precursors of trophotaeniae formed by exteriorized hindgut; and (b) that they are vestigial remnants of trophotaeniae that were lost during a switch to a form of matrotrophy involving nutrient ingestion.
Subject(s)
Cyprinodontiformes , Embryo, Nonmammalian , Animals , Female , Nutrients , Oocytes , Ovary , PregnancyABSTRACT
We review morphological features of the amniote egg and embryos in a comparative phylogenetic framework, including all major clades of extant vertebrates. We discuss 40 characters that are relevant for an analysis of the evolutionary history of the vertebrate egg. Special attention is given to the morphology of the cellular yolk sac, the eggshell, and extraembryonic membranes. Many features that are typically assigned to amniotes, such as a large yolk sac, delayed egg deposition, and terrestrial reproduction have evolved independently and convergently in numerous clades of vertebrates. We use phylogenetic character mapping and ancestral character state reconstruction as tools to recognize sequence, order, and patterns of morphological evolution and deduce a hypothesis of the evolutionary history of the amniote egg. Besides amnion and chorioallantois, amniotes ancestrally possess copulatory organs (secondarily reduced in most birds), internal fertilization, and delayed deposition of eggs that contain an embryo in the primitive streak or early somite stage. Except for the amnion, chorioallantois, and amniote type of eggshell, these features evolved convergently in almost all major clades of aquatic vertebrates possibly in response to selective factors such as egg predation, hostile environmental conditions for egg development, or to adjust hatching of young to favorable season. A functionally important feature of the amnion membrane is its myogenic contractility that moves the (early) embryo and prevents adhering of the growing embryo to extraembryonic materials. This function of the amnion membrane and the liquid-filled amnion cavity may have evolved under the requirements of delayed deposition of eggs that contain developing embryos. The chorioallantois is a temporary embryonic exchange organ that supports embryonic development. A possible evolutionary scenario is that the amniote egg presents an exaptation that paved the evolutionary pathway for reproduction on land. As shown by numerous examples from anamniotes, reproduction on land has occurred multiple times among vertebrates-the amniote egg presenting one "solution" that enabled the conquest of land for reproduction.
Subject(s)
Vertebrates , Yolk Sac , Animals , Chorion , Extraembryonic Membranes , Female , Phylogeny , PregnancyABSTRACT
Reduced limbs and limblessness have evolved independently in many lizard clades. Scincidae exhibit a wide range of limb-reduced morphologies, but only some species have been used to study the embryology of limb reduction (e.g., digit reduction in Chalcides and limb reduction in Scelotes). The genus Brachymeles, a Southeast Asian clade of skinks, includes species with a range of limb morphologies, from pentadactyl to functionally and structurally limbless species. Adults of the small, snake-like species Brachymeles lukbani show no sign of external limbs in the adult except for small depressions where they might be expected to occur. Here, we show that embryos of B. lukbani in early stages of development, on the other hand, show a truncated but well-developed limb with a stylopod and a zeugopod, but no signs of an autopod. As development proceeds, the limb's small size persists even while the embryo elongates. These observations are made based on external morphology. We used florescent whole-mount immunofluorescence to visualize the morphology of skeletal elements and muscles within the embryonic limb of B. lukabni. Early stages have a humerus and separated ulna and radius cartilages; associated with these structures are dorsal and ventral muscle masses as those found in the embryos of other limbed species. While the limb remains small, the pectoral girdle grows in proportion to the rest of the body, with well-developed skeletal elements and their associated muscles. In later stages of development, we find the small limb is still present under the skin, but there are few indications of its presence, save for the morphology of the scale covering it. By use of CT scanning, we find that the adult morphology consists of a well-developed pectoral girdle, small humerus, extremely reduced ulna and radius, and well-developed limb musculature connected to the pectoral girdle. These muscles form in association with a developing limb during embryonic stages, a hint that "limbless" lizards that possess these muscles may have or have had at least transient developing limbs, as we find in B. lukbani. Overall, this newly observed pattern of ontogenetic reduction leads to an externally limbless adult in which a limb rudiment is hidden and covered under the trunk skin, a situation called cryptomelia. The results of this work add to our growing understanding of clade-specific patterns of limb reduction and the convergent evolution of limbless phenotypes through different developmental processes.
Subject(s)
Embryonic Development/physiology , Forelimb/anatomy & histology , Hindlimb/anatomy & histology , Lizards/anatomy & histology , Animals , Forelimb/embryology , Hindlimb/embryology , PhylogenyABSTRACT
Evolution of the terrestrial egg of amniotes (reptiles, birds, and mammals) is often considered to be one of the most significant events in vertebrate history. Presence of an eggshell, fetal membranes, and a sizeable yolk allowed this egg to develop on land and hatch out well-developed, terrestrial offspring. For centuries, morphologically-based studies have provided valuable information about the eggs of amniotes and the embryos that develop from them. This review explores the history of such investigations, as a contribution to this special issue of Journal of Morphology, titled Developmental Morphology and Evolution of Amniote Eggs and Embryos. Anatomically-based investigations are surveyed from the ancient Greeks through the Scientific Revolution, followed by the 19th and early 20th centuries, with a focus on major findings of historical figures who have contributed significantly to our knowledge. Recent research on various aspects of amniote eggs is summarized, including gastrulation, egg shape and eggshell morphology, eggs of Mesozoic dinosaurs, sauropsid yolk sacs, squamate placentation, embryogenesis, and the phylotypic phase of embryonic development. As documented in this review, studies on amniote eggs and embryos have relied heavily on morphological approaches in order to answer functional and evolutionary questions.
Subject(s)
Dinosaurs , Yolk Sac , Animals , Egg Shell , Reptiles , Retrospective StudiesABSTRACT
Evolution of the terrestrial, amniotic egg of vertebrates required new mechanisms by which yolk material could be processed for embryonic use. Recent studies on each of the major extant reptile groups have revealed elaborate morphological specializations for yolk processing, features that differ dramatically from those of birds. In the avian pattern, liquid yolk is housed in a yolk sac whose endodermal lining absorbs and digests yolk material and sends resultant nutrients into the blood circulation. In snakes, lizards, turtles, and crocodilians, as documented herein, the yolk sac becomes invaded by endodermal cells that proliferate and phagocytose yolk material. Blood vessels then invade, and the endodermal cells become arranged around them, forming elongated "spaghetti-like" strands that fill the yolk sac cavity. This pattern provides an effective means by which yolk material is cellularized, digested, and transported by vitelline vessels to the developing embryo. Phylogenetically, the (non-avian) "reptilian" pattern was ancestral for sauropsids and was modified or replaced in ancestors to birds. This review postulates that evolution of the "avian" pattern involved increased reliance on extracellular digestion of yolk, allowing embryonic development to occur more rapidly than in typical reptiles. Comparative studies of yolk processing that draw on morphological, biochemical, molecular approaches are needed to explain how and why the "reptilian" pattern was replaced in birds or their archosaurian ancestors.
Subject(s)
Lizards , Turtles , Animals , Birds , Reptiles , Snakes , Yolk SacABSTRACT
Recent studies have demonstrated a mechanism of embryonic yolk processing in lizards, snakes and turtles that differs markedly from that of birds. In the avian pattern, cells that line the inside of the yolk sac take up products of yolk digestion and deliver nutrients into the vitelline circulation. In contrast, in squamates and turtles, proliferating endodermal cells invade and fill the yolk sac cavity, forming elongated strands of yolk-filled cells that surround small blood vessels. This arrangement provides a means by which yolk material becomes cellularized, digested, and transported for embryonic use. Ultrastructural observations on late-stage Alligator mississippiensis eggs reveal elongated, vascular strands of endodermal cells within the yolk sac cavity. The strands of cells are intermixed with free yolk spheres and clumps of yolk-filled endodermal cells, features that reflect early phases in the yolk-processing pattern. These observations indicate that yolk processing in Alligator is more like the pattern of other reptiles than that of birds.
Subject(s)
Alligators and Crocodiles , Lizards , Turtles , Animals , Snakes , Yolk SacABSTRACT
In 1926, the German biologist Johanna (Hanni) Hrabowski published a study of the morphology and development of the fetal placenta in lizards that has proven to be of historical importance. Her anatomical descriptions and interpretations identified developmental patterns that differ from other amniotes -- features now recognized as unique attributes of squamate (lizards and snakes) development. Her 1926 monograph presented the first histological comparison of fetal membranes in closely-related oviparous and viviparous reptiles, thereby establishing a comparative framework for understanding placental specializations for viviparity. Hrabowski reported that yolk sac development did not differ between oviparous and viviparous species. The novel, shared components of yolk sac development she identified are now recognized as the foundation for the unique yolk sac placenta of reptiles, the omphaloplacenta. In addition, Hrabowski's extensive ontogenetic sampling and the detail and accuracy of her anatomical descriptions set high standards for subsequent studies of comparative evolutionary embryology.
Subject(s)
Extraembryonic Membranes/anatomy & histology , Lizards/anatomy & histology , Placenta/anatomy & histology , Anatomy, Comparative/history , Animals , Biological Evolution , Female , History, 20th Century , Placentation , Pregnancy , Viviparity, NonmammalianABSTRACT
The reptilian clade Squamata is defined primarily by osteological synapomorphies, few of which are entirely unambiguous. Studies of developing squamate eggs have revealed a uniquely specialized feature not known to occur in any other amniotes. This feature-the yolk cleft/isolated yolk mass complex-lines the ventral hemisphere of the egg. During its formation, extraembryonic mesoderm penetrates the yolk and an exocoelom (the yolk cleft [YC]) forms in association with it, cutting off a thin segment of yolk (the "isolated yolk mass" [IYM]) from the main body of the yolk. The YC-IYM complex has been observed and described in more than 65 squamate species in 12 families. In viviparous species, it contributes to the "omphaloplacenta," a type of yolk sac placenta unique to squamates. The only squamates known to lack the IYM are a few highly placentotrophic skinks with minuscule eggs, viviparous species in which it clearly has been lost. Given its absence in mammals, chelonians, crocodylians, and birds, the YC-IYM complex warrants recognition as a developmental synapomorphy of the squamate clade. As in extant viviparous lizards and snakes, the YC-IYM complex presumably contributed to the placenta of extinct viviparous squamates.
Subject(s)
Lizards/embryology , Mesoderm/embryology , Yolk Sac/embryology , AnimalsABSTRACT
Evolution of the large-yolked, amniotic egg required mechanisms by which extracellular yolk could be made available for embryonic development. In birds, the endodermal lining of the yolk sac absorbs and digests the yolk. In contrast, recent studies on lizards and snakes (squamates) have revealed that yolk is processed by means of a proliferating mass of "spaghetti-like" strands formed by endodermal cells attached to anastomosing blood vessels. To clarify the method of yolk processing in chelonians, we applied electron microscopy to an extensive series of embryos of the pond slider turtle, Trachemys scripta. Our findings demonstrate that proliferating endodermal cells phagocytose yolk spheres. These cells remain attached to one another following mitosis, thereby forming clumps that progressively occupy the yolk sac cavity. Upon invasion of blood vessels, the cells become organized into elongated, vascularized "spaghetti-like" strands of cells like those found in squamates. Residual yolk found in the body cavity of new hatchlings chiefly consists of these vascularized strands. Such strands of cells also develop in the false map turtle, Graptemys pseudographica (Emydidae). We infer that the developmental pattern by which yolk is processed is ancestral for both Chelonia and Reptilia, and therefore must have been modified or abandoned in birds or their archosaur ancestors.
Subject(s)
Egg Yolk/ultrastructure , Turtles/embryology , Animals , Animals, Newborn , Egg Yolk/cytology , Embryo, Nonmammalian/ultrastructure , Embryonic Development , Endoderm/cytology , Microscopy, ElectronABSTRACT
Features of embryonic development in birds traditionally have been assumed to be shared by sauropsids in general. Herein, we document a pattern of yolk processing and cellularization in the Eastern fence lizard (Sceloporus undulatus) that is fundamentally different from that of birds. In the avian pattern, cells of the yolk sac lining phagocytose, and digest yolk material. These cells release products of digestion into underlying blood vessels for transport back to the embryo. In contrast, microscopic examination of the developing eggs of S. undulatus reveals that the yolk mass is converted into vascularized, "spaghetti-like" strands that fill the yolk sac cavity. Three successive developmental stages are involved. First, the liquid yolk is invaded by proliferating endodermal cells, which phagocytose and digest the yolk material. These cells form clumps that progressively fill the yolk sac cavity. Second, small blood vessels derived from the yolk sac vasculature invade the yolk sac cavity. Third, the endodermal cells become organized in monolayers around these vessels. This arrangement provides a means by which large numbers of endodermal cells can digest yolk, with each cell being positioned to release products of digestion into an adjacent blood vessel for transport to the embryo. The mechanism of yolk processing in this lizard species is similar to that of recently studied snakes. From its phylogenetic distribution, we infer that this pattern probably is ancestral for squamate sauropsids.
Subject(s)
Lizards/anatomy & histology , Lizards/embryology , Yolk Sac/embryology , Animals , Blood Vessels/anatomy & histology , Cell Aggregation , Cell Proliferation , Embryo, Nonmammalian/anatomy & histology , Embryo, Nonmammalian/cytology , Embryo, Nonmammalian/ultrastructure , Neovascularization, Physiologic , Yolk Sac/cytology , Yolk Sac/ultrastructureABSTRACT
Early amniotic vertebrates evolved large-yolked eggs that permitted production of well-developed, terrestrial hatchlings. This reproductive pattern required new mechanisms for cellularizing the yolk and mobilizing it for embryonic use. In birds, cells that line the yolk sac cavity phagocytose and digest the yolk material, a pattern that is commonly assumed to be universal among oviparous amniotes. However, recent evidence challenges the assumption that all squamate reptiles conform to the avian developmental pattern. In this paper, scanning electron microscopy and histology were used to study mechanisms of yolk processing in two colubrid snakes, the kingsnake Lampropeltis getula and the milksnake L. triangulum. Endodermal cells from the yolk sac splanchnopleure proliferate massively as they invade the yolk sac cavity, forming elaborate chains of interlinked cells. These cells grow in size as they phagocytose yolk material. Subsequently, vitelline capillaries invade the masses of yolk-laden cells and become coated with the endodermal cells, forming an elaborate meshwork of cell-coated strands. The close association of cells, yolk, and blood vessels allows yolk material to be cellularized, digested, and transported for embryonic use. The overall pattern is like that of the corn snake Pantherophis guttatus, but contrasts markedly with that of birds. Given recent evidence that this developmental pattern may also occur in certain lizards, we postulate that it is ancestral for squamates. Studies of lizards, crocodilians, and turtles are needed to clarify the evolutionary history of this pattern and its implications for the evolution of the amniotic (terrestrial) vertebrate egg.
Subject(s)
Biological Evolution , Colubridae/genetics , Colubridae/physiology , Egg Yolk/physiology , Ovum/physiology , Animals , Egg Yolk/cytology , Ovum/ultrastructureABSTRACT
Non-avian reptiles commonly are assumed to be like birds in their overall patterns of development. However, colubrid corn snakes (Pantherophis guttatus) have mechanisms of yolk cellularization and processing that are entirely different from the avian pattern. In birds, a vascular "yolk sac" surrounds and digests the liquid yolk. In contrast, in corn snakes, the yolk material is converted into vascularized cords of yolk-filled cells. In this study, we used stereomicroscopy, histology, and scanning electron microscopy to analyze this unusual developmental pattern in corn snakes. Our observations reveal that the yolk sac cavity is invaded by endodermal cells that proliferate, absorb yolk spheres, and form aggregates of interconnected cells within the liquid yolk mass. As development proceeds, small blood vessels arise from the yolk sac omphalopleure, penetrate into the yolk mass, and become tightly encased in the endodermal cells. The entire vitellus ultimately becomes converted into a mass of vascularized, "spaghetti-like" strands of yolk-laden cells. The resulting arrangement allows yolk to be digested intracellularly and yolk products to be transported to the developing embryo. Indirect evidence for this pattern in other species raises the possibility that it is ancestral for squamates and quite possibly Reptilia in general.
Subject(s)
Colubridae/anatomy & histology , Colubridae/embryology , Embryo, Nonmammalian/anatomy & histology , Yolk Sac/anatomy & histology , Yolk Sac/embryology , Animals , Embryo, Nonmammalian/ultrastructure , Ovum/physiology , Ovum/ultrastructure , Yolk Sac/ultrastructure , Zea maysABSTRACT
Ultrastructure of the placental tissues from redbelly watersnakes (Nerodia erythrogaster) was analyzed during late pregnancy to provide insight into placental development and function. Examination of the chorioallantoic placenta with transmission electron microscopy reveals that chorionic and uterine epithelia are extremely attenuated but intact and that the eggshell membrane is vestigial and lacks a calcareous layer. These features minimize the interhemal diffusion distance across the placenta. Scanning electron microscopy reveals that fetal and maternal components of the placentas are richly vascularized by dense networks of capillaries. Although the yolk sac omphalopleure has largely been replaced by chorioallantois by late gestation, it retains patches of yolk droplets and regions of absorptive cells with microvilli and abundant mitochondria. Transmission electron microscopy reveals that yolk material is taken up for digestion by endodermal cells. As yolk is removed, allantoic capillaries invade to occupy positions just beneath the epithelium, forming regions of chorioallantoic placentation. Ultrastructural features indicate that the chorioallantoic placenta is specialized for gas exchange, while the omphalallantoic ("yolk sac") placenta shows evidence of functions in yolk digestion and maternal-fetal nutrient transfer. Placental features of this species are consistent with those of other thamnophines, and are evolutionarily convergent on snakes of other viviparous clades.
Subject(s)
Colubridae/embryology , Placenta/ultrastructure , Placentation/physiology , Allantois/embryology , Allantois/ultrastructure , Animals , Biological Evolution , Chorion/embryology , Chorion/ultrastructure , Female , Microscopy, Electron, Scanning , Microscopy, Electron, Transmission , Pregnancy , Yolk Sac/embryology , Yolk Sac/ultrastructureABSTRACT
As part of a broad survey of placental structure, function, and evolution in reptilian sauropsids paraffin-section histology was used to study microscopic anatomy of the uterus and fetal membranes of three species of North American watersnakes (Nerodia: Colubridae). The pre-ovulatory uterus is poorly vascularized with inactive shell glands. These shell glands are activated during vitellogenesis but regress during pregnancy. Two placentas develop through apposition of the uterine lining to the chorioallantois and the yolk sac omphalopleure. Fetal and maternal components of the chorioallantoic placenta are progressively vascularized during development. Their epithelia are attenuated, but (contrary to a previous report), epithelia of neither the uterus nor the chorion are eroded. The fetal portion of the yolk sac placenta is an omphalallantois, formed of avascular omphalopleure, isolated yolk mass, and allantois. This placenta is progressively replaced by chorioallantoic placenta during mid- to late-development through depletion of the isolated yolk mass. The chorioallantoic placenta is anatomically specialized for maternal-fetal gas exchange, and its expansion during development reflects the growing needs of the fetus for gas exchange. The yolk sac placenta is morphologically unsuited for gas exchange, but may serve other functions in maternal-fetal exchange.
Subject(s)
Colubridae/anatomy & histology , Placenta/embryology , Placentation/physiology , Allantois/embryology , Allantois/ultrastructure , Animals , Biological Evolution , Chorion/embryology , Chorion/ultrastructure , Extraembryonic Membranes/ultrastructure , Female , Mammals , Placenta/ultrastructure , Pregnancy , United States , Yolk Sac/embryology , Yolk Sac/ultrastructureABSTRACT
In eggs of oviparous reptiles, fetal membranes maintain developing embryos through the exchange of respiratory gases and provision of water and calcium. As part of a survey of reptilian fetal membranes, we used scanning electron microscopy to study fetal membrane morphology in the oviparous Pueblan milksnake, Lampropeltis triangulum campbelli. The chorioallantois initially is an avascular structure lined by enlarged chorionic and allantoic epithelia. Upon vascularization, the chorionic epithelium becomes greatly attenuated, enhancing the potential for gas exchange; the allantoic epithelium also flattens. The bilaminar omphalopleure of the yolk sac lacks blood vessels, but it becomes vascularized by allantoic capillaries and transformed into an omphalallantois. Upon regression of the isolated yolk mass, this membrane is converted to chorioallantois, equipping it for gas exchange. Allantoic fluid serves as a water reservoir, and we postulate that it facilitates water uptake by establishing an osmotic gradient. Early in development, epithelia of both the chorion and the omphalopleure show apical microvilli that greatly increase the cell surface area available for water uptake. However, these features are incompatible with gas exchange and are lost as oxygen needs take precedence. A comparison of the fetal membranes to those of other squamate species (both oviparous and viviparous) reveals characteristics that are probably ancestral for snakes, some of which are plesiomorphic for Squamata. The widespread phylogenetic distribution of these features reflects their utility as adaptations that serve functional requirements of squamate embryos.
Subject(s)
Chorioallantoic Membrane/ultrastructure , Colubridae/embryology , Extraembryonic Membranes/ultrastructure , Allantois/embryology , Allantois/ultrastructure , Animals , Biological Evolution , Chorioallantoic Membrane/blood supply , Chorioallantoic Membrane/embryology , Extraembryonic Membranes/embryology , Oviparity , Ovum/growth & development , Ovum/ultrastructure , Yolk Sac/embryology , Yolk Sac/ultrastructureABSTRACT
Although placental diversity in mammals received growing attention in the 1600s through the early 1800s, placentation was not documented in reptiles until the mid-19th century. In his classic 1855 study on a viviparous lizard, Cesare Studiati (University of Pisa) described a structural/functional arrangement of fetal and maternal tissues that meets contemporary criteria for recognition of placentation. Through the fortuitous selection of a highly placentotrophic species, Chalcides chalcides, Studiati recognized the functional role of placental tissues in provision of oxygen as well as nutrients. Although Studiati worked in a pre-evolutionary milieu and without the benefits of histological techniques, his findings revealed that viviparous reptiles could exhibit placental specializations that paralleled those of mammals. Accordingly, his classic paper initiated a highly productive body of research that has continued to the present and highlighted specializations of a species that has figured importantly in placental research.
Subject(s)
Lizards/physiology , Physiology, Comparative/history , Placentation , Viviparity, Nonmammalian , Animals , Female , History, 19th Century , PregnancyABSTRACT
In reptilian sauropsids, fetal (extraembryonic) membranes that line the eggshell sustain developing embryos by providing for gas exchange and uptake of water and eggshell calcium. However, a scarcity of morphological studies hinders an understanding of functional specializations and their evolution. In kingsnakes (Lampropeltis getula), scanning electron microscopy reveals two major fetal membranes: the chorioallantois and yolk sac omphalopleure. In early development, the chorioallantois contains tall chorionic epithelial cells, avascular connective tissue, and enlarged allantoic epithelial cells. During its maturation, the chorionic and allantoic epithelia thin dramatically and become underlain by a rich network of allantoic capillaries, yielding a membrane ideally suited for respiratory gas exchange. Yolk sac development initially is like that of typical lizards and snakes, forming an avascular omphalopleure, isolated yolk mass (IYM), and yolk cleft. However, unlike the situation in most squamates studied, the omphalopleure becomes transformed into a "secondary chorioallantois" via three asynchronous events: flattening of the epithelium, regression of the IYM, and vascularization by the allantois. Progressive expansion of chorioallantois parallels growing embryonic needs for gas exchange. In early through mid-development, external surfaces of both the chorionic and omphalopleure epithelium show an abundance of irregular surface protrusions that possibly increase surface area for water absorption. We postulate that the hypertrophied allantoic epithelial cells produce allantoic fluid, a viscous substance that facilitates water uptake and storage. Our findings are consistent with a previous study on the corn snake Pantherophis guttatus, but include new observations and novel functional hypotheses relevant to a reconstruction of basal squamate patterns.