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Morphological Specializations for Fetal Maintenance in Viviparous Vertebrates: an Introduction and Historical Retrospective

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Morphological Specializations for Fetal Maintenance in Viviparous Vertebrates: an Introduction and Historical Retrospective JOURNAL OF MORPHOLOGY 00:00–00 (2015) Morphological Specializations for Fetal Maintenance in Viviparous Vertebrates: An Introduction and Historical Retrospective Daniel G. Blackburn1* and J. Matthias Starck2 1Department of Biology, and Electron Microscopy Center, Trinity College, Hartford, Connecticut 06106 2Department of Biology, University of Munich, D-82152 Planegg-Martinsried, Germany ABSTRACT In many viviparous vertebrates, preg- 2010, and organized by Daniel G. Blackburn and nant females sustain their developing embryos and pro- James R. Stewart. The symposium participants vide them with nutrients by means of placentas and a and other researchers represented in this journal diversity of other types of specializations. With this issue are using a variety of research methods to article, we introduce a virtual (online) issue of the study a diversity of organisms. Their shared goal Journal of Morphology that presents 12 recent papers on fetal maintenance in viviparous vertebrates. We also is to understand the mechanisms by which vivipa- outline the history of research in this area and docu- rous females maintain their developing embryos. ment the central role of morphology in helping to In association with this commemorative issue of explain the function and evolution of specializations for the Journal of Morphology, the publishers are fetal nutrition. This virtual issue of the Journal of making freely available to readers a number of Morphology is an outgrowth of a symposium held under other relevant papers that have appeared in this auspices of the International Congress of Vertebrate journal since the 1880s through the present. In Morphology. The included papers reflect a diversity of this introductory paper, we explore relevant con- taxa, research methods, and biological issues. To cele- ceptual distinctions, the role of morphology in brate the publication of this virtual issue of the Jour- studies of specializations for fetal sustenance, and nal of Morphology, the publisher is making freely available to readers a number of other relevant papers the historical background of research in this area. published in the journal over the past 128 years. J. In addition, we summarize the nature and scope of Morphol. 000:000–000, 2015. VC 2015 Wiley Periodicals, Inc. the papers that make up this virtual issue of the journal. KEY WORDS: history of science; viviparity; matrotro- phy; fetal nutrition; morphology OVERARCHING ISSUES Conceptual Distinctions The distinction between animals that lay eggs and those that give birth to their young is a funda- INTRODUCTION mental one that dates in the biological literature In viviparous vertebrates, pregnant females to the writings of Aristotle. Although various bio- maintain developing embryos in their reproductive logical terms have been applied to this distinction, tracts from the time of fertilization until birth. To in the contemporary literature “oviparity” and meet the respiratory and nutritional needs of “viviparity” commonly are used to describe “egg- these embryos, vertebrates have evolved a remark- laying reproduction” and “live-bearing repro- able diversity of specializations, including placen- duction” respectively (e.g., Wourms, 1981; Black- tas and other features that accomplish maternal– burn, 1992, 2000a; Wake, 2002; Musick and Ellis, fetal nutrient transfer. Such specializations have 2005). Under this usage, “viviparity” refers to spe- fascinated biologists for centuries, and their struc- cies in which embryos develop in the maternal ture, function, and evolution constitute active areas of research. This article is an introduction to a virtual *Correspondence to: Daniel G. Blackburn, Department of Biology, (online) issue of the Journal of Morphology, one Trinity College, Hartford, CT 06106. that presents 12 recent papers on morphological E-mail: [email protected] specializations for fetal maintenance in live- bearing vertebrates. The genesis of this virtual Received 15 February 2015; issue was a symposium entitled “Fetal Nutritional Accepted 11 May 2015. Specializations in Viviparous Vertebrates” held at Published online 00 Month 2015 in the Tenth International Congress of Vertebrate Wiley Online Library (wileyonlinelibrary.com). Morphology (ICVM) in Punta del Este, Uruguay in DOI 10.1002/jmor.20410 VC 2015 WILEY PERIODICALS, INC. 2 BLACKBURN ET AL. reproductive tract. (The term “embryo” is used tion of viviparity and specializations for fetal here in the broad sense, to include developing off- nutrition raises significant questions about the spring that are conventionally called “larvae” and roles of selective pressures, constraints, adapta- “fetuses.” For a broader use of the term tion, exaptation, and other factors that have “viviparity,” see Wake, in press). For oviparous affected the evolution of these patterns (Shine, anurans and fishes in which a parent broods exter- 1985; Wake, 1982, 1985; Wourms et al., 1988; nally fertilized eggs or larvae in the mouth, stom- Blackburn, 2006, in press). Morphology is in an ach, on the dorsum, or in a body pouch (Greven, excellent position to address such questions. 2011; Wake, in press), the term “pseudoviviparity” can be applied (Blackburn, 1999a, in press). THE ROLE OF MORPHOLOGY A separate distinction is based on the sources of Functional Issues nutrients for embryonic development. In “lecithotrophy” the ovum’s own yolk provides For viviparous embryos, development within the nutrients for development, whereas in maternal reproductive tract (oviduct, uterus, or “matrotrophy,” extravitelline nutrients are pro- ovary) confers both difficulties and potential vided to embryos/fetuses by the pregnant female means for their resolution. The most immediate during their gestation in her reproductive tract problem facing a viviparous embryo is exchange of (Wourms, 1981; Blackburn, 1992, 1994; Mess respiratory gases, given the hypoxic nature of the et al., 2003; Stewart, 2013). Lecithotrophy and female reproductive tract. Many types of special- matrotrophy represent extremes of a continuum, izations facilitate maternal-fetal gas exchange, because in many viviparous species, the embryos including fetal membranes (such as the chorioal- derive nutrients from their own yolk as well as lantois and yolk sac), embryonic gills, fins, tail, other (postovulatory) maternal sources (Wourms skin, and pericardial sac, and on the maternal et al., 1988; Stewart, 1992, 2013; Marsh- side, modifications to lining of the oviduct, uterus, Matthews, 2011). “Placentotrophy” is a form of and ovary. Squamates face an additional func- matrotrophy that involves a placenta—defined as tional problem, in that viviparity requires evolu- an “intimate apposition of the fetal organs to the tionary loss of the eggshell, which thereby maternal or paternal tissues for physiological deprives the embryo of a significant source of cal- exchange” (Mossman, 1937). Other forms of matro- cium (Stewart and Ecay, 2010; Stewart, 2013; trophy include “histotrophy” (embryonic absorption Stewart and Blackburn, 2014). Physiological diffi- of maternal nutrients); “oophagy” (ingestion of sib- culties aside, viviparity also opens opportunities ling yolks); “embryophagy” (cannibalism of sibling for supplementation of yolk supplies with mater- embryos, sometimes called “adelphophagy”); and nal nutrients, given the proximity of fetal and “matrophagy” (ingestion of maternal tissues) maternal tissues. (Wourms, 1981; Blackburn et al., 1985; Wourms Morphological approaches are essential in stud- et al., 1988; Blackburn, in press). ies of mechanisms by which pregnant females sus- tain their developing embryos. In cases of matrotrophy, aspects to be analyzed include histo- Implications for Evolution logical and cytological specializations for nutrient The fact that viviparity and matrotrophy have synthesis, secretion, and embryonic uptake; the evolved convergently in diverse animal lineages histochemical nature of maternally supplied has been widely- recognized for more than a cen- nutrients; the developmental origins and morpho- tury (Haacke, 1885; Giacomini, 1906; Gadow, genesis of specializations for matrotrophy; and the 1910; Kerr, 1919). Phylogenetic analyses of squa- timing during gestation of maternal—fetal nutri- mate reptiles in the 1980s concluded that vivipar- ent transfer. Features that enhance maternal— ity has evolved at least 90 times (Blackburn, 1982, fetal gas exchange (such as increased vascularity 1985; Shine, 1985), a number that has increased and decreased diffusion distances) can likewise be to more than 115 origins as further data have considered. Structural analysis also can lead to accumulated (Blackburn, 1999b, 2000b, in press). new, testable functional hypotheses, such as the Multiple origins also have been defined in fishes inference of sodium-coupled water transport across (Dulvy and Reynolds, 1997; Blackburn, 2005; cf. the yolk sac placenta of viviparous snakes (Black- Musick and Ellis, 2005), caecilian amphibians burn et al., 2002). Relevant techniques include his- (Gower et al., 2008), and extinct reptiles (Organ tology, scanning, and transmission electron et al., 2009; Blackburn and Sidor, in press). An microscopy, histochemistry, and confocal micros- analysis published in this virtual issue of Journal copy, in conjunction with physiological and bio- of Morphology has identified more than 150 evolu- chemical methods that have become subsumed tionary origins of vertebrate viviparity and 33 sep- within contemporary morphology. The papers fea- arate origins of matrotrophy
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