Papers by Daniel Blackburn
The omphalallantoic placenta is a complex organ that is unique to viviparous squamates. Using tra... 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.
Transmission electron microscopy was used to examine the ultrastructure of the allantoplacenta of... more Transmission electron microscopy was used to examine the ultrastructure of the allantoplacenta of garter snakes during the last half of gestation. This placenta occupies the dorsal hemisphere of the egg and is formed through apposition of the chorioallantois to the inner lining of the uterus. The uterine epithelium consists of flattened cells with short, irregular microvilli and others that bear cilia. The lamina propria is vascularized and its capillaries lie at the base of the uterine epithelial cells. The chorionic epithelium consists of a bilayer of squamous cells that are particularly thin superficial to the allantoic capillaries. Neither the chorionic epithelium nor the uterine epithelium undergoes erosion during development. Although a thin remnant of the shell membrane intervenes between fetal and maternal tissue at mid-gestation, it undergoes fragmentation by the end of gestation. Thus, uterine and chorionic epithelial are directly apposed in some regions of the allantoplacenta, forming continuous cellular boundaries at the placental interface. During development, capillaries proliferate in both the uterine and chorioallantoic tissues. By late gestation, the interhemal diffusion distance has thinned in some areas to less than 2 μm through attenuation of the uterine and chorionic epithelia. Morphologically, the allantoplacenta is well adapted for its function in gas exchange. However, the presence of cytoplasmic vesicles, ribosomal ER, and mitochondria in the chorionic and uterine epithelial cells are consistent with the possibility of additional forms of placental exchange.
The Sixth International Congress of Vertebrate Morphology was held July 21–26, 2001, at the
Univ... more The Sixth International Congress of Vertebrate Morphology was held July 21–26, 2001, at the
University of Jena, Federal Republic of Germany. The Congress included a symposium entitled
‘‘Evolutionary Transformations of Fetal Membranes and Reproductive Strategies.’’ This symposium was organized by Ulrich Zeller, Andrea Mess (both of whom are at the Museum fur
Naturkunde, Humboldt - Universitat, Berlin), and Daniel Blackburn (Dept. of Biology, Trinity
College, Hartford, Connecticut, USA). Abstracts of the meeting were published in the June 2001
issue of the Journal of Morphology (Volume 248, Number 3).
Fetal membranes (such as the chorioallantois and yolk sac) are essential to embryonic development... more Fetal membranes (such as the chorioallantois and yolk sac) are essential to embryonic development, and have contributed importantly to the evolutionary and ecological diversity of vertebrates. Since the mid - 19th century, many scientific careers have been devoted to investigations of their structure, function, and development. However, significant gaps remain in our understanding of the diversity and evolution of fetal membranes. This symposium volume focuses on the use of cladistic principles and phylogenetic relationships to reconstruct the evolutionary morphology of fetal membranes. The main goal of the present paper is to introduce the application of such methods to the evolution of vertebrate fetal membranes, as well as to provide the reader with background information on relevant concepts and terminology. Contributions within this journal issue draw upon studies of metatherian and eutherian mammals, as well as sauropsid reptiles (notably squamates). Particular attention is given to historical transformations of fetal membranes associated with the evolution of such phenomena as placentation and matrotrophy, and reproductive strategies such as viviparity. What emerges from the contributed papers is a broad sampling of contemporary research on fetal membranes, and an overview of how these membranes have evolved to support embryonic life in diverse terrestrial and intra-uterine environments.
Phylogenetic information offers an important resource in analyses of reproductive diversity, incl... more Phylogenetic information offers an important resource in analyses of reproductive diversity, including interpretations of fetal membrane evolution. In this paper, we draw upon ongoing studies of South American and African lizards to consider the value of combining phylogenetic and reproductive evidence in the construction of evolutionary interpretations. South American lizards of the genus Mabuya exhibit several reproductive specializations that are convergent on those of eutherian mammals, including viviparity, long gestation periods, ovulation of tiny eggs, and placental supply of the nutrients for development. Studies of placental morphology and development indicate that New World Mabuya share several other derived features, including chorionic areolae and a “Type IV” epitheliochorial placenta with a villous, mesometrial placentome. Some characteristics of these lizards are shared by two African skinks, M. ivensii and Eumecia anchietae, including minuscule eggs, placentotrophy, an absorptive chorioallantois, and features of the yolk sac. Available evidence is consistent with two explanations: (1) placentotrophy originated in Africa, predating a trans-Atlantic colonization by Mabuya of the New World; and (2) placentotrophy arose two or three separate times among these closely related skinks. As illustrated by analysis of these animals, not only can data on fetal membrane morphology yield phylogenetic information, but phylogenetic evidence in turn provides a valuable way to reconstruct the evolution of fetal membranes in a biogeographic context. When appropriately interpreted, morphological and phylogenetic evidence can be combined to yield robust evolutionary conclusions that avoid the pitfalls of circular reasoning.
One important difference between adaptive and non-adaptive explanations can be found in the evolu... more One important difference between adaptive and non-adaptive explanations can be found in the evolutionary sequence of structural and functional modifications. Phylogenetic analysis (cladistics) provides a powerful methodology for distinguishing exaptation from adaptation, by indicating whether character traits have predated, accompanied, or followed
evolution of particular functions. Such analysis yields falsifiable hypotheses that can help to distinguish causal relationships from mere correlation.
An understanding of the evolutionary morphology of extraembryonic membranes in reptiles requires ... 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.
Although pregnant viviparous squamates are sometimes claimed to be able to resorb inviable eggs a... more Although pregnant viviparous squamates are sometimes claimed to be able to resorb inviable eggs and embryos from the uterus, definitive evidence for such resorption is not available. After placing pregnant female Pseudemoia pagenstecheri into conditions under which embryonic development is terminated, we periodically harvested the gravid oviducts and examined them histologically. Females contained abnormal and degenerating eggs and embryos that had died in various stages of development. Dead embryos had undergone extensive cytolysis, dissolution, and aseptic necrosis and vitelline masses showed signs of deterioration and passage down the oviduct. The uterine mucosa lay in direct contact with the vitelline material, with no intact shell membrane intervening between them. Yolk was sometimes displaced into the exocoelom and allantoic cavity due to rupture of the extraembryonic membranes. Histological examination revealed no evidence of the uptake of yolk by the uterine epithelium or its accumulation in the subepithelial connective tissue. In many specimens, the uterine epithelium showed minuscule, apical granules. The position, appearance, and staining properties of the granules suggests them to be secretory, a manifestation of placentotrophy. Our observations indicate that P. pagenstecheri females retain dead eggs and embryos for several weeks or longer, yet do not resorb them during that period. This lizard is the second placentotrophic skink species in which resorption has been suspected, but in which abortive eggs appear to be retained or extruded instead of being resorbed by the oviducts. Researchers should not assume that squamates can digest and resorb oviductal eggs without definitive morphological evidence.
New World skinks of the genus Mabuya exhibit a unique form of viviparity that involves ovulation ... more New World skinks of the genus Mabuya exhibit a unique form of viviparity that involves ovulation of tiny (1 mm) eggs and provision of virtually all of the nutrients for embryonic development by placental means. Studies of the Brazilian species M. heathi reveal that the chorioallantoic placenta is unlike those reported in any other squamate genus and exhibits striking specializations for maternal–fetal nutrient transfer. The uterine lining is intimately apposed to the chorioallantois, with no trace of an intervening shell membrane or of epithelial erosion; thus, the placenta is epitheliochorial. The uterus exhibits multicellular glands that secrete organic material into the uterine lumen. Opposite the openings of these glands, the chorion develops areolae, invaginated pits that are lined by absorptive, columnar epithelium. A single, mesometrial placentome develops, formed by radially oriented uterine folds that project into a deep invagination of the chorion. Uterine epithelium of the placentome appears to be syncytial and secretory and overlies a rich vascular supply. The apposed chorionic epithelium is absorptive in morphology and contains giant binucleated cells that bear microvilli. Several specializations of the placental membranes of M. heathi are found among eutherian mammals, signifying evolutionary convergence that extends to histological and cytological levels. The chorioallantoic placenta of M. heathi and its relatives warrants recognition as a new morphotype for reptiles, defined here as the “Type IV” placenta. This is the first new type of chorioallantoic placenta to be defined formally for reptiles in over half a century.
Surface topography and cross-sections of the placental membranes were examined by scanning electr... more Surface topography and cross-sections of the placental membranes were examined by scanning electron microscopy in two species of Thamnophis. The chorionic epithelium of the chorioallantoic placenta consists of broad, squamous cells that lack surface specializations. The apposed uterine epithelium contains ciliated cells and larger, nonciliated cells. Neither the epithelium of the chorion nor that of the uterus is eroded; thus, underlying capillaries are not exposed to the luminal surface. In both the omphaloplacenta and the omphalallantoic placenta, epithelium of the omphalopleure consists of brush-border cells bearing prominent microvilli, interspersed with cells bearing minuscule microvilli. These surface epithelial cells are joined at their apices and their lateral surfaces are extensively sculpted by intercellular channels, presenting the appearance of an epithelium specialized for absorption. Deep to the epithelium lie the yolk spheres of the isolated yolk mass, interspersed with endodermal cells. Surface topography of the uterine epithelia of the omphaloplacenta and omphalallantoic placenta is relatively unspecialized. The acellular shell membrane separates maternal and fetal tissues in each of the three placental types. Marked differences in surface features of the chorioallantois and omphalopleure probably reflect different roles of these membranes in gas exchange and transfer of water and nutrients.
Squamate reptiles represent an ideal group for studies of viviparity, because they have evolved t... more Squamate reptiles represent an ideal group for studies of viviparity, because they have evolved this reproductive pattern frequently, relatively recently, and at low taxonomic levels. A phylogenetic approach shows particular promise in helping us interpret anatomical, physiological, and ecological diversity. This review summarizes four major categories of active investigation: (1) reproductive anatomy and physiology; (2) placental structure and function; (3) reproductive endocrinology; and (4) reproductive and physiological ecology. Evolutionary reconstructions suggest that on many occasions viviparity has evolved concomitantly with functional placentation, through reduction of the shell membrane and hormonal modifications that prolong gestation. Studies of placentotrophic clades as well as reproductively bimodal species offer great potential for explaining the evolution of viviparity and placentation. However, live-bearing squamates are reproductively diverse, and appear to have solved physiological problems associated with viviparity by a variety of mechanisms. Consequently, studies on one or a few squamate species appear increasingly unlikely to yield all-inclusive explanations. Future studies and analyses should abandon assumptions of universal physiological mechanisms and a single historical sequence, in favor of the documentation of diversity in phylogenetic and quantitative terms.
The classification of reproductive patterns inherited from the 19th century reflects mammalian bi... more The classification of reproductive patterns inherited from the 19th century reflects mammalian biases and fails to capture our understanding of amniote reproductive diversity. Much more useful is a bipartite classification that fully distinguishes between two separate reproductive parameters -- sources of nutrients for development, and state of the reproductive product at emergence from the mother. "Oviparity" and "viviparity" are used in their literal senses to refer to "egg-laying" and "live-bearing" reproduction. "Lecithotrophy" refers to provision of nutrients to the embryo via the yolk, and "matrotrophy" to provision by alternative means (e.g., a placenta, a pattern termed "placentotrophy"). Use of these terms has several advantages, including elimination of confusion associated with the archaic term "ovoviviparity". The system also recognizes commonality between patterns involving maternal provision of nutrients before birth or hatching (e.g., to eggs and embryos) and afterwards (to neonates). Growing consensus around the bipartite classification of reproductive patterns reflects recognition of the importance of a common biological vocabulary that applies widely across traditional methodological, disciplinary, and taxonomic boundaries.
Although viviparity is widely considered to evolve irreversibly from oviparity, an analysis of sq... more Although viviparity is widely considered to evolve irreversibly from oviparity, an analysis of squamates by de Fraipont, Clobert, and Barbault in 1996 presented evidence to the contrary; it also argued that oviparous egg-guarding evolves from viviparity. The response by Shine and Lee in 1999 offers significant criticisms of this analysis and challenges its conclusions. My paper shows that the analysis by de Fraipont et al. exhibits several methodological shortcomings: use of outdated taxonomy and non-monophyletic groups, questionable codification of character states, focus on a very limited data base, analysis of taxonomic categories that are unnecessarily inclusive, and reliance on an invalid correlation between reproductive mode and body size. In comparison to the present analysis (in which 102-115 potential origins of viviparity are defined), de Fraipont et al. have focused on a small number of evolutionary transitions and have generated multiple, conflicting hypotheses about each; the result is highly inflated estimates of heterodox transformations that mainly reflect discrepant phylogenetic interpretations. I therefore support and expand upon Shine and Lee's conclusions. A reversion from viviparity to oviparity cannot be ruled out on theoretical grounds, but evidence for its occurrence among squamates thus far remains exceedingly weak.
Encyclopedia of Reproduction. Academic Press, 1999
Placentae are organs formed from extraembryonic and parental tissues that help sustain embryos ph... more Placentae are organs formed from extraembryonic and parental tissues that help sustain embryos physiologically during their development. In viviparous squamate reptiles, in which the fetus develops to term inside the maternal oviduct, the placental membranes typically accomplish gas exchange and provide water and small quantities of nutrients to the embryo. In certain lizards, placental membranes supply virtually all of the nutrients for embryonic development. Morphological attributes of squamate chorioallantoic placentae correlate with the degree of placentotrophy. Some viviparous species of amphibians exhibit specializations for maternal-fetal nutrient provision that are functionally analogous to placentae. Simple placenta-like structures that function in gas exchange are occasionally found among egg-laying amphibians.
Encyclopedia of Reproduction. Academic Press, 1999
Viviparity is a reproductive pattern in which females retain developing eggs inside their reprodu... more Viviparity is a reproductive pattern in which females retain developing eggs inside their reproductive tracts or body cavity and give birth to offspring capable of a free-living existence. Oviparity, in contrast, is a pattern in which females deposit eggs that develop and hatch in the external environment. These patterns can be viewed as "reproductive strategies," patterns that have advantages as well as disadvantages that affect their evolution. An advantage of viviparity, for example, is that embryos are protected and physiologically maintained by the pregnant female. In many viviparous species, the mother provides nutrients to the embryo during gestation, a pattern known as "matrotrophy." Viviparity has originated on over 160 times among animals and is found among bony fishes, cartilaginous fishes, amphibians, mammals, and squamate reptiles, as well as in several invertebrate groups. Viviparity and matrotrophy are phenomena of considerable biological interest. They have been studied from the standpoints of morphology, physiology, endocrinology, ecology, and evolution.
Race and Racism in Theory and Practice, 2000
The main goal of this chapter is to explore the concept of race from a biological standpoint, and... more The main goal of this chapter is to explore the concept of race from a biological standpoint, and to demonstrate how and why its explanatory power is so limited. The evidence reveals that race is largely a social construct that fails to meet the criteria of a meaningful biological concept, a fact with significant implications for politics, society, and the practice of medicine.
In lizards and snakes, the oviducts function in fertilization, sperm storage, egg transport, eggs... 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. Seasonal 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.
Among squamate reptiles, gravid females commonly are said to be able to resorb infertile and malf... more Among squamate reptiles, gravid females commonly are said to be able to resorb infertile and malformed eggs from their oviducts. This pattern, if it existed, would allow females to recycle nutrients from abortive attempts at reproduction, and to increase lifetime reproductive potential by modulating reproductive effort according to environmental circumstances. However, a review of the literature reveals that evidence for oviductal egg resorption is weak, and does not preclude other fates for abortive eggs (egg retention or expulsion). Furthermore, for the oviduct to resorb eggs would require that it have the functional properties of the digestive tract, properties that may be incompatible with its several reproductive functions. Future work should not assume oviductal egg resorption in squamates without definitive evidence that the eggs are not simply aborted or retained by females following absorption of water.
A recent paper in J. theor. Biol. has challenged the proposed application of punctuated equilibr... more A recent paper in J. theor. Biol. has challenged the proposed application of punctuated equilibrium models to the evolution of reptilian viviparity and placentation. While clarifying some aspects of the models, the paper's criticisms reflect misinterpretations of the literature and an unnecessary reluctance to apply punctuationist concepts to extant taxa. The punctuated equilibrium model retains potential for clarification of the patterns of stasis and episodic change that may well have characterized squamate reproductive history.
Abdominal hypaxial muscles of male anurans function in vocalization by causing forcible expulsion... 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 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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Papers by Daniel Blackburn
University of Jena, Federal Republic of Germany. The Congress included a symposium entitled
‘‘Evolutionary Transformations of Fetal Membranes and Reproductive Strategies.’’ This symposium was organized by Ulrich Zeller, Andrea Mess (both of whom are at the Museum fur
Naturkunde, Humboldt - Universitat, Berlin), and Daniel Blackburn (Dept. of Biology, Trinity
College, Hartford, Connecticut, USA). Abstracts of the meeting were published in the June 2001
issue of the Journal of Morphology (Volume 248, Number 3).
evolution of particular functions. Such analysis yields falsifiable hypotheses that can help to distinguish causal relationships from mere correlation.
University of Jena, Federal Republic of Germany. The Congress included a symposium entitled
‘‘Evolutionary Transformations of Fetal Membranes and Reproductive Strategies.’’ This symposium was organized by Ulrich Zeller, Andrea Mess (both of whom are at the Museum fur
Naturkunde, Humboldt - Universitat, Berlin), and Daniel Blackburn (Dept. of Biology, Trinity
College, Hartford, Connecticut, USA). Abstracts of the meeting were published in the June 2001
issue of the Journal of Morphology (Volume 248, Number 3).
evolution of particular functions. Such analysis yields falsifiable hypotheses that can help to distinguish causal relationships from mere correlation.