- Hartford, Connecticut, United States
Daniel Blackburn
Trinity College, Connecticut, Biology, Faculty Member
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Reduced limbs and limblessness have evolved independently in many lizard clades. Skinks exhibit a wide range of limb-reduced morphologies, but only some species have been used to study the embryology of limb reduction (i.g., digit... more
Reduced limbs and limblessness have evolved independently in many lizard clades. Skinks exhibit a wide range of limb-reduced morphologies, but only some species have been used to study the embryology of limb reduction (i.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 as well as 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. 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 i...
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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... more
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 preferen...
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Certain forelimb muscles of anurans exhibit sexual dimorphism in mass and fiber composition, offering potential for studies of the effects of hormones on muscle characteristics. Androgen-responsiveness of major forelimb muscles of male... more
Certain forelimb muscles of anurans exhibit sexual dimorphism in mass and fiber composition, offering potential for studies of the effects of hormones on muscle characteristics. Androgen-responsiveness of major forelimb muscles of male leopard frogs, Rana pipiens, was evaluated by quantifying the effects of testosterone cypionate administration and castration on lyophilized muscle mass. The coracoradialis, pectoralis epicoracoideus, and pectoralis sternalis muscles were highly-responsive to testosterone treatment, showing a mean dry mass increase of approximately 50% over control values. However, the pectoralis abdominis muscle was unaffected by testosterone administration, and castration had no effect on any of the muscles. Testosterone sensitivity reflects both the degree of sexual dimorphism and the inferred functional roles of the muscles. Because their forelimb muscles vary markedly in androgen-sensitivity, leopard frogs show considerable promise as a model system for clarifyin...
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Research Interests: Physiology, Zoology, Biology, Morphology, Medicine, and 4 moreAnatomy, American alligator, Yolk, and yolk sac
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,... more
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.
Research Interests: Evolutionary Biology, Zoology, Biology, Medicine, Anatomy, and 3 moreUltrastructure, Yolk, and yolk sac
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... more
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...
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Compared with amphibians, oviparous reptiles and birds lay large eggs that contain abundant yolk. Because the yolk is extracellular, it must be taken up by cells of the yolk sac and metabolized so that products of yolk digestion can be... more
Compared with amphibians, oviparous reptiles and birds lay large eggs that contain abundant yolk. Because the yolk is extracellular, it must be taken up by cells of the yolk sac and metabolized so that products of yolk digestion can be transported to the embryo to fuel development. In birds, the yolk is processed by cells that line the inside of the yolk sac. A very different developmental pattern recently has been demonstrated in lizards and snakes in which the yolk sac cavity is converted to a compact mass of blood vessels lined by endodermal cells. In this study, we used scanning electron microscopy to determine which of these developmental patterns (if either) occurs in a representative chelonian, the North American Snapping Turtle (Chelydra serpentina (Linnaeus, 1758)). Our observations reveal that yolk-filled endodermal cells progressively fill the yolk sac cavity. These cells become organized around anastomosing blood vessels, forming elongated strands that are morphologicall...
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Oviparous amniotes produce a large yolky egg that gives rise to a free-living hatchling. Structural characteristics and functional attributes of the egg are best known for birds, which have a large mass of fluid yolk surrounded by an... more
Oviparous amniotes produce a large yolky egg that gives rise to a free-living hatchling. Structural characteristics and functional attributes of the egg are best known for birds, which have a large mass of fluid yolk surrounded by an extraembryonic yolk sac. Yolk nutrients are delivered to the embryo via the vascular yolk sac. This developmental pattern and nutrient transport mechanism is thought to be representative of all other lineages of amniotes. Recent discovery of a snake with cellularized yolk organized around a meshwork of blood vessels reveals an additional pattern for yolk mobilization, which may also occur in other squamate reptiles (lizards and snakes). This complex yolk sac raises interesting questions about developmental mechanisms and suggests a possible model for the transition between the egg of anamniotes and that of amniotes.
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The yolk splanchnopleure and chorioallantoic membrane of oviparous reptiles transport calcium from the yolk and eggshell to the developing embryo. Among oviparous amniotes, the mechanism of calcium mobilization to embryos has been studied... more
The yolk splanchnopleure and chorioallantoic membrane of oviparous reptiles transport calcium from the yolk and eggshell to the developing embryo. Among oviparous amniotes, the mechanism of calcium mobilization to embryos has been studied only in domestic fowl, in which the mechanism of calcium transport of the yolk splanchnopleure differs from the chorioallantoic membrane. Transport of calcium is facilitated by calbindin-D(28K) in endodermal cells of the yolk splanchnopleure of chickens but the chorioallantoic membrane does not express calbindin-D(28K). We used immunoblotting to assay for calbindin-D(28K) expression in yolk splanchnopleure and chorioallantoic membrane of the corn snake, Elaphe guttata, to test the hypothesis that the mechanism of calcium transport by extraembryonic membranes of snakes is similar to birds. High calbindin-D(28K) expression was detected in samples of yolk splanchnopleure and chorioallantoic membrane during late embryonic stages. We conclude that calbi...
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The viviparous Brazilian scincid lizard Mabuya heathi exhibits a suite of reproductive specializations widely believed to be confined to the eutherian mammals. This skink ovulates the smallest known reptilian egg (≃1.0 mm in diameter).... more
The viviparous Brazilian scincid lizard Mabuya heathi exhibits a suite of reproductive specializations widely believed to be confined to the eutherian mammals. This skink ovulates the smallest known reptilian egg (≃1.0 mm in diameter). Placental transport accounts for >99% of the dry mass of the periparturient fetus, representing a degree of placentotrophy proportionately greater than that reported in any other non-mammalian vertebrate. Placental morphology and the timing of fetal growth implicate the chorioallantoic placenta in maternal-fetal nutrient transfer. The yolk sac placenta regresses prior to any major increase in embryonic dry mass. Precocial gonadal maturation and postponement of reproductive investment until well after ovulation enables females to become pregnant at 3-4 months of age, long before attainment of full adult body size.
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Research Interests: Physiology, Zoology, Biology, Morphology, Medicine, and 14 moreEmbryo, Anatomy, Lizards, Female, Animals, Lizard, Embryonic Development, Degeneration, Oviduct, Uterus, Resorption, Embryos, Yolk, and ovum
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Abdominal hypaxial muscles of male anurans function in vocalization by causing forcible expulsion of pulmonary air through the larynx. The hypaxial muscles were studied in the leopard frog, Rana pipiens, to test whether functions of these... more
Abdominal hypaxial muscles of male anurans function in vocalization by causing forcible expulsion of pulmonary air through the larynx. The hypaxial muscles were studied in the leopard frog, Rana pipiens, to test whether functions of these muscles in males are reflected in sexual dimorphism and in androgen responsiveness. The combined abdominal oblique muscles and the rectus abdominis showed significant sexual dimorphism in wet mass and dry mass. However, the abdominal oblique muscles were less concentrated in protein content in males than in females. In overwintering males, exogenous testosterone cypionate stimulated a significant increase in mass and protein content of the abdominal oblique and rectus abdominis muscles. Castration had no effect on muscle mass or on the response to androgen treatment.
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Research Interests: Evolutionary Biology, Reproduction, Theoretical biology, Literary Darwinism Or Evolutionary Literary Theory, Biological Sciences, and 17 morePregnancy, Mathematical Sciences, Reptiles, Lizards, Female, Animals, Vertebrates, Snakes, Stephen Jay Gould, Biological evolution, Viviparity, Oviparity, Oviposition, Reptiles Reproduction Ecology and Conservation, Punctuated Equilibrium, Phylogenetic Reconstruction, and Placentation
Research Interests: Physiology, Zoology, Development Studies, Embryology, Morphology, and 4 morePlacenta, Reptiles, Lizards, and Viviparity
The omphalallantoic placenta is a complex organ that is unique to viviparous squamates. Using transmission EM and light microscopy, we examined this placenta in garter snakes in order to understand its structural organization and... more
The omphalallantoic placenta is a complex organ that is unique to viviparous squamates. Using transmission EM and light microscopy, we examined this placenta in garter snakes in order to understand its structural organization and functional capabilities. The omphalallantoic placenta is formed from the uterine lining and the bilaminar omphalopleure, the latter of which is associated with the isolated yolk mass and allantois. A thin shell membrane separates the fetal and maternal tissues throughout gestation. The uterine epithelium contains cuboidal cells with large droplets or granules and appears to be secretory. Epithelium of the omphalopleure is specialized for absorption and contains cells with prominent microvilli and others with large cytoplasmic droplets or granules. The brush-border cells are rich in mitochondria and Golgi bodies and interdigitate extensively with adjacent cells, forming elaborate intercellular canaliculi. Their morphology is consistent with their proposed role in sodium-coupled water movement. During development, the isolated yolk mass becomes depleted as yolk droplets are digested by cells of the omphalopleure and allantois. However, the allantois does not fuse to or vascularize the inner face of the omphalopleure. Consequently, the distance between fetal and maternal circulatory systems remains large (about 250–300 μm), precluding efficient gas exchange and hemotrophic transfer. The morphology of the omphalallantoic placenta strongly suggests that it functions in nutrient transfer through uterine secretion and fetal absorption. J. Morphol. 256:187–204, 2003. © 2003 Wiley-Liss, Inc.
Research Interests: Physiology, Zoology, Electron Microscopy, Morphology, Female, and 4 moreAnimals, Colubridae, Uterus, and ovum
Research Interests: Physiology, Zoology, Development Studies, Embryology, Morphology, and 4 morePlacenta, Reptiles, Lizards, and Viviparity
Research Interests: Ancient History, Reproduction, Dairy Science, Biotechnology, Lactation, and 12 moreAnimal Production, Mammals, Milk Technology, Multituberculate mammal evolution and phylogeny, Early mammalian evolution, Female, Animals, Biological evolution, Mammal ecology, Milk production, Food Sciences, and Dairying
Although abortive uterine eggs are often assumed to be resorbed by females of the viviparous skink Chalcides chalcides, little microscopic evidence of resorption of such eggs is available. Oviducts from pregnant female C. chalcides in... more
Although abortive uterine eggs are often assumed to be resorbed by females of the viviparous skink Chalcides chalcides, little microscopic evidence of resorption of such eggs is available. Oviducts from pregnant female C. chalcides in which egg resorption was inferred were examined histologically to seek a morphological basis for resorption. Uterine histology at the site of abortive eggs was very similar to that of lizards in early pregnancy. The uterine epithelium consisted of a monolayer of pseudostratifed columnar cells that showed no evidence of yolk phagocytosis. The uterine lamina propria exhibited shell glands and modest vascularity, typical of early gestation, and contained neither yolk droplets nor accumulating leukocytes. Unattenuated regions of the lamina propria contained occasional macrophages and mast cells, some of the latter of which were undergoing degranulation. The abortive eggs often were collapsed with ruptured shell membranes, and some were undergoing extrusion from the incubation chambers down the oviduct. In eggs that had begun developing, extraembryonic ectoderm and endoderm were atypical in location, and had failed to enclose yolk leaking from the eggs. Oviducts sampled from later in the reproductive season were reproductively inactive, and showed no trace of abortive eggs or egg components. We postulate that abortive eggs are extruded from the oviduct by pregnant females under conditions of physiological stress, as a means of enhancing future reproductive effort.
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Examination of late-stage placental material of the lizard Chalcides chalcides from the Hubrecht Laboratorium (Utrecht, The Netherlands) reveals several cytological and histological specializations that appear to have been superimposed... more
Examination of late-stage placental material of the lizard Chalcides chalcides from the Hubrecht Laboratorium (Utrecht, The Netherlands) reveals several cytological and histological specializations that appear to have been superimposed over a morphological pattern that is typical for squamates. The chorioallantoic placenta is highly vascularized and consists of a single mesometrial placentome and a generalized paraplacentomal region, both of which are epitheliochorial. The placentome is deciduate, and contains deeply interdigitating folds of hypertrophied uterine and chorioallantoic tissue. Chorionic epithelium lining the placentome comprises enlarged, microvilliated cells, a small proportion of which are diplokaryocytes. The placentomal uterine epithelium is not syncytial and consists of enlarged cells bearing microvilli. The yolk sac placenta is a true omphaloplacenta (sensu stricto), being formed by juxtaposition of uterine tissues to an avascular, bilaminar omphalopleure. Epithelium of the omphalopleure is stratified and is hypertrophied into papillae that project into detritus of the uterine lumen. The omphalopleure is separated from the yolk sac proper by a yolk cleft that is not confluent with the exocoelom and is not invaded by the allantois. Neither an omphalallantoic placenta nor a true choriovitelline placenta is present in late gestation. Morphologically, the mature placentae of C. chalcides are among the most specialized to have been described in reptiles, reflecting the substantial maternal-fetal nutrient transfer that occurs in this species. © 1993 Wiley-Liss, Inc.
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In lizards and snakes, the oviducts function in fertilization, sperm storage, egg transport, eggshell deposition, maintenance of the early embryo, and expulsion of the egg or fetus. In viviparous forms they also contribute to placentae... more
In lizards and snakes, the oviducts function in fertilization, sperm storage, egg transport, eggshell deposition, maintenance of the early embryo, and expulsion of the egg or fetus. In viviparous forms they also contribute to placentae responsible for gas exchange and nutrient provision to the fetus. Dissections of species of 30 genera coupled with data from the literature indicate that squamate oviducts vary interspecifically in seven macroscopic features, including the extent and nature of regional differentiation, vascular supply, topographic asymmetry, number of oviducts, vaginal pouches, and relationship to the cloaca. The uterus, infundibulum, and vagina differ histologically in their epithelia, glands, and myometrial layers. Season cyclicity occurs in all three oviductal regions, most prominently in the uterus, and is under endocrinological control. Regional and cytological specializations reflect the diverse functions performed by the oviduct. Definitive evidence for oviductal albumen production and egg resorption is lacking. In viviparous squamates, three uterine specializations may facilitate maternal-fetal gas exchange: an attenuated epithelium, reduced uterine glands (and a reduced shell membrane), and increased vascularization. Contrary to previous reports, pregnant uteri show no epithelial erosion or capillary exposure. Specializations for nutrient provision to the fetus include mucosal hypertrophy, enlarged glandular epithelia, and multicellular glands whose secretions are absorbed by the chorioallantois. Comparisons with other amniotes indicate that squamates inherited the oviduct as an organ with capabilities for egg uptake and transport, fertilization, eggshell deposition, and oviposition. Other features have evolved convergently among squamates: infundibular sperm receptacles, unilateral oviduct loss, uterine gestation, placentation, and specializations for placentotrophy. Cladistic analysis indicates that oviductal features associated with deposition of tertiary egg investments in reptiles reflect evolutionary convergence as well as secondary simplification, rather than a unidirectional trend towards increased specialization.
Research Interests: Placenta, Reptiles, Lizards, Female, Animals, and 6 moreSnakes, Biological evolution, Viviparity, Oviduct, Uterus, and Structure Function
An understanding of the evolutionary morphology of extraembryonic membranes in reptiles requires information about oviparous as well as viviparous species. We are studying histology and ultrastructure of the extraembryonic membranes of... more
An understanding of the evolutionary morphology of extraembryonic membranes in reptiles requires information about oviparous as well as viviparous species. We are studying histology and ultrastructure of the extraembryonic membranes of snakes to clarify the evolutionary history of reptilian fetal membranes, including determination of basal (ancestral) ophidian and squamate patterns. Microscopic anatomy of the membranes of oviparous corn snakes (Elaphe guttata) was examined using light and electron microscopy. At mid – development the inner surface of the eggshell is lined by two extraembryonic membranes, the chorioallantois and the omphalallantoic membrane. The chorioallantois consists of a bilayered cuboidal epithelium that overlies the allantoic blood vessels. During development, allantoic capillaries become more abundant, and the chorionic epithelium thins, decreasing the diffusion distance for respiratory gas exchange. The abembryonic pole of the egg is delimited by a bilaminar omphalopleure and isolated yolk mass, the latter of which is lined on its inner face by the allantois. The isolated yolk mass regresses developmentally, and patches of yolk droplets become isolated and surrounded by allantoic blood vessels. By late development, the abembryonic hemisphere has been fully vascularized by allantoic vessels, forming a “secondary chorioallantois.” With regard to its extraembryonic membranes, Elaphe gutatta is similar to viviparous snakes. However, this species exhibits features that have not previously been reported among squamates, perhaps reflecting its oviparous reproductive habits. Morphological evidence for the uptake of eggshell material by epithelia of the chorion and omphalopleure suggests that the potential for absorption by extraembryonic membranes predates the origin of viviparity. J. Exp. Zool. 299A:48–58 2003. © 2003 Wiley-Liss, Inc.