Trophoblast concept as applied to therian mammals

JOURNAL OF MORPHOLOGY 196:127-136 (1988)

Trophoblast Concept as Applied to Therian Mammals DANIEL G. BLACKBURN, J. MARY TAYLOR, AND HELEN A. PADYKULA Department of Cell Biology, School of Medicine, Vanderbilt University, Nashville, Tennessee 37232 (D. G.B.); Oregon Regional Primate Research Center, Beaverton, Oregon 97006 (J. M. T); Department of Fisheries and Wildlife, Oregon State Uniuersity, Coruallis, Oregon 97331 (J.M. T); Department of Anatomy, University of Massachusetts Medical School, Worcester, Massachusetts 01605 (H.A. l?)

ABSTRACT Available evidence provides little support for a recent proposal that the term “trophoblast” be applied solely to eutherian mammals. Argu- ments for such a restricted usage are based on a dichotomous interpretation of therian reproduction that underestimates the developmental, structural, and functional diversity of trophoblastic tissues occurring within the infraclass Eutheria. The occurrence of developmental patterns that are phenotypically intermediate between those of commonly studied eutherians and metatherians suggests that blastocyst development is not fundamentally different in marsupials and eutherians.

The trophoblast of marsupials accomplishes most or all of the major functions of the eutherian trophoblast, including maternal-fetal physiological exchange, implantation, contribution to placental membranes, steroid metabolism, and possibly, immunological protection of the conceptus. Furthermore, application of the term “trophoblast” to marsupials is consistent with present and past usage, as well as with the original definition and etymological derivation of the term. Therefore, we recommend that the term “tr~phoblast’~ continue to be applied in a functional-morphological sense to the appropriate extraembryonic tissues of marsupials. Such use of functional (rather than taxonomic) criteria for application of this term avoids biasing interpretations of mammalian reproductive evolution.

One century ago, the eminent embryologist A.A.W. Hubrecht (1888,1889) coined the neo- logism “trophoblast” to describe a remarka- ble extraembryonic tissue of the mammalian conceptus. Hubrecht (1888, p. 511) originally introduced the term “trophoblast” and the concept that it represented in reference to therian mammals in general, the marsupial opossum included. Through further docu- mentation of developmental similarities among mammals, the trophoblast soon was accepted as a functionally important tissue that is common to all therians, and that is homologous to the extraembryonic ectoderm of monotremes and sauropsids (Hill, 1900, ’10; Hubrecht, ’08). Usage of the term “trophoblast” for marsupials and eutherians has persisted to the present day (e.g., Ramsey, ’82; Mossman, ’87; Taylor and Padykula, ’78; Tyndale-Biscoe and Renfree, ’87). The gen-

eral consensus holds that trophoblastic tissues of all therian mammals are homologous, at least in a broad sense (Luckett, ’77), and share a variety of structural, functional, and developmental similarities (Billington, ’71).

In a recent paper, Lillegraven (‘85) argued against use of the term “trophoblast” in reference to marsupials, on the grounds that metatherian and eutherian trophoblastic tissues are neither functionally equivalent nor likely to be homologous. This terminological proposal and the various interpretations on which it is based warrant careful consideration, for they represent a departure from concepts that have predominated ever since the

Daniel G. Blackburn is now at Department of Biology, Trinity College, Hartford, CT 06106

J. Mary Taylor is now at The Cleveland Museum of Natural History, Wade Oval, University Circle, Cleveland, OH 44106.

0 1988 ALAN R. LISS, INC.

128 D.G. BLACKBURN ET AL.

term “trophoblast” was first adopted. The issues raised by Lillegraven (’85) are much more than semantic; they involve interpretations of developmental patterns, functional inferences, and questions of homology, phylogeny, and reproductive evolution.

Our paper evaluates the concept of trophoblast from an alternative perspective to that presented by Lillegraven (‘79, ’85) and suggests reasons that the use of separate terms for the trophoblastic tissues of marsupials and eutherians is not justified by the available evidence.

TROPHOBLAST DIVERSITY

Mammalian placental diversity reflects adaptation across evolutionary time and changing environments. As the outermost extraembryonic layer, the trophoblast is in direct contact with maternal tissues. During gestation, the versatile trophoblast becomes converted into several types of tissue that express structural and functional diversity. For example, in the marsupial bandicoot there are at least three trophoblast variants (Padykula and Taylor, ’76, ’77, ’821, in the rat there are at least four or five types, and in the human there are at least three variants (Langhans cytotrophoblast, syncytial trophoblast, and the peripheral cytotrophoblast that is in contact with the maternal decidua in the so-called “placental bed”) (Boyd and Hamilton, ’70).

Such trophoblastic diversity provides ver- satility in mammalian adaptation. By various mechanisms, the trophoblastic asso- ciations with the yolk sac and allantois accommodate the principal requirements of successful pregnancy, requirements that vary somewhat among therian species: namely, 1) to anchor the conceptus to maternal tissues; 2) to create a physiological “lifeline” assur- ing transfer of nutrients and wastes; 3) to provide passive immunity; 4) to prevent im- munologic rejection; and 5) to produce hor- mones such as gonadotropin, lactogen, estradiol, progesterone, and gonadotropin-releasing hormone (e.g., see Billington, ’71; Khodr and Siler-Khodr, ’78; Luckett, ’77; McCormack and Glasser, ’80; Mossman, ’87; Pumphrey, ’77).

The therian trophoblast exhibits the very structural and functional diversity one might expect of a functionally crucial tissue that is evolutionarily plastic, and that has been sub- jected to over 120 million years of strong and varied selective pressures. Billington (’71, p. 28) noted in his review of the trophoblast:

With the exception of the egg-lay- ing Monotremata (duck-billed platypus and spiny ant-eater), trophoblast is found in all mammals. Not surprisingly, there are considerable variations in the development, structure, and functions of the trophoblast. In some species it is principally the nutritive function that is developed, whilst in others, secretory and invasive properties are elaborated. To a large extent this reflects the type of development and structure.

Thus, for example, in the marsupial pera- melids, the trophoblast accomplishes an invasive implantation (Hughes, ’74), whereas in some other mammals, such as the strepsi- rhine primates, implantation is superficial and noninvasive (Luckett, ’77). Likewise, in some primates the trophoblast plays a role in the transfer of passive immunity, yet in carnivores, ruminants, and marsupials, lactation fulfills this function (Pumphrey, ’77; Cockson and McNeice, ’80).

Although structural and functional diversity of the trophoblast is well documented, few modern reviews take note of the inter- specific diversity manifested in early development of the trophoblast. Rather, generaIly two developmental patterns are described and attributed to the infraclasses Eutheria and Metatheria (Marsupialia). These patterns have been widely described and illus- trated (e.g., Lyne and Hollis, ’77; also see Wimsatt, ’75). In the so-called “eutherian pattern,” as typified by the mouse, early cleavage produces the morula, a compact mass of blastomeres, which lies surrounded by the zona pellucida. Blastocoel formation begins with cavitation between cells of the morula. As cleavage proceeds, the blastocoel continues to grow, resulting in formation of the blastocyst, which consists of an outer sphere of trophoblast cells and an inner cell mass. Developmental derivatives of the eutherian trophoblast include cytotrophoblast, syncytiotrophoblast, and trophoblastic giant cells, whereas the inner cell mass gives rise to the tissues of the embryo proper, as well as to extraembryonic mesoderm and endoderm (Rossant and Papaioannou, ’77; Luck- ett, ’78).

This “eutherian” (murine) pattern is often contrasted with that of metatherians. No morula is formed in marsupials; instead, blastomeres resulting from early cleavage

TROPHOBLAST CONCEPT IN THERIAN MAMMALS 129

become adpressed to the inner surface of the zona pellucida. As cleavage proceeds, a uni- laminar blastocyst soon results. Cells located at one pole of this blastocyst give rise to the embryo proper and to certain extraembryonic tissues, whereas the remaining cells constitute the marsupial trophoblast. Al- though an inner cell mass does not form in marsupials, prospective trophoblastic and nontrophoblastic populations are usually said to be distinguishable by criteria of size and position (Wimsatt, ’75; Luckett, ’77). Other cited differences between “eutherian” and “metatherian” developmental patterns include presence of deutoplasmolysis (“yolk-ex- trusion”) (Selwood and Young, ’83) and a shell membrane in marsupials, and irreversible determination of embryonic and extraembryonic cell lineages in eutherians (Lille- graven, ’85).

In his recent review, Lillegraven (’85) interpreted these two developmental patterns as evidence of a major phylogenetic dichotomy. Partly on the basis of the above developmental differences, he indicated that the trophoblast of eutherians is a neomorphic tissue that is not homologous to the marsupial “trophoblast” (ectodermal chorion). This view is consistent with previous suggestions that marsupials are reproductively primitive by virtue of their lack of “true” trophoblast ni l - legraven, ’75, ’79).

Interestingly, however, the primary comparative literature reveals few consistent differences in blastocyst development that would suggest a single, fundamental dichotomy at the infraclass level. Most of the sup- posed differences between marsupials and eutherians disappear when the range of vari- ation found among eutherians is considered. For example, the absence of a morula, cited as a metatherian characteristic, also charac- terizes some representatives of at least two eutherian orders (classification of McKenna, ’75)-Insectivora (Bluntschli, ’38; Goetz, ’37, ’38) and Macroscelidea (van der Horst, ’42; also see Tripp, ’71). Similarly, although deutoplasmolysis is widely cited as a metatherian feature, it is not unique to marsupials. On the contrary, it has been reported in a wide range of eutherian groups, including carnivores (Hamilton, ’34; Hill and Tribe, ’24; van der Stricht, ’23), chiropterans (van der Stricht, ’09), artiodactyls (Heuser and Stree- ter, ’29)’ perissodactyls (Hamilton and Day, ’45), and rodents (Austin, ’57; Lams, ’13; Odor, ’60). The argument that the blastocoel forms in fundamentally different ways in

metatherians and eutherians also invites challenge, for both the elephant shrew Elephantulus and the distantly related (McKenna, ’75; Eisenberg, ’81) tenrec Hemi- centetes conform to the so-called “metatherian pattern” in this regard (see Wimsatt, ’75). Furthermore, although a very early and irreversible determination of embryonic and extraembryonic cells is said to occur only in the “eutherian pattern,” this early determination has been investigated in only a hand- ful of species, and probably ought not be assumed to be either universal among eutherians or unique to that group. In Elephantu- lus, for example, cellular pluripotentiality reportedly is retained through the f 100 cell blastocyst stage, during which period all cells are estimated to have equal potential for differentiation into embryonic cells (van der Horst, ’42). Although this inference has not been tested experimentally in Elephantulus, it is compatible with the claim that mouse trophectoderm may receive contributions of cells from the inner cell mass (Rossant and Croy, ’85). At least in the mouse, it has become evident that the cell lineages of early development defy consistent, exact delinea- tion (Gardner, ’85). Comparative and experimental approaches focused on the derivation of extraembryonic tissues will be required to determine whether the labile developmental system of the mouse typifies the early development of all eutherian and marsupial mammals.

Some purported differences between metatherian and eutherian development that have been afforded major phylogenetic significance (Lillegraven, ’85) seem to be no greater than interordinal differences exist- ing within the infraclass Eutheria. For example, the developmental history of the cells forming the walls of the blastocyst is said to be markedly disparate in marsupials and eutherians, in that these cells give rise to the trophectoderm in eutherians but to both chorionic ectoderm and body ectoderm in marsupials (McCrady, ’44). However, Boyd and Hamilton (’52, p. 96) pointed out that “There are also striking variations in the differentiation of the trophoblastic portion of the chorion in different mammals.” For example, trophoblast (protoderm) of Macaca mulatta (= M. rhesus) and Homo sapiens has been interpreted as giving direct origin to extraembryonic mesoderm (Hertig, ’35, ’681, whereas that of the mouse does not give rise to any mesodermal component (Rossant and Papaioannou, ’77; Kaufman, ’83). Although


this interpretation has been questioned (Luckett, 1978), the possibility remains that even within the eutherians the trophoblast is not consistent in its prospective fate (Ram- sey, '82). Certain valid differences between metatherians and eutherians, such as the transitory remnant of a shell membrane in marsupials, are not relevant to the issues of homology and terminology.

EVOLUTIONARY INTERPRETATION OF DEVELOPMENTAL DIVERSITY

Ultimately, an understanding of the evolution of the developmental diversity of mammals may require the use of cladistic, methods, which have proven valuable in other reconstructions of reproductive history (e.g., Luckett, '77; Blackburn, '85). Unfortu- nately, a complete cladistic analysis is not feasible at present, because of the scarcity of comparative data on developmental patterns and cell determination and also because of our poor understanding of the phylogenetic relationships of several major taxa (e.g., In- sectivora, sensu lato). An added complication is that a cladistic analysis of developmental features should be done within the context of a broad analysis of mammalian reproductive patterns, because of the possibility that syn- apomorphies of metatherian and eutherian development are convergent traits that have resulted from independent origins of viviparity (Sharman, '70) andor placentotrophy in the two infraclasses. A recent cladistic analysis concluded that mammalian scenarios with single vs. dual origins of viviparity and placentotrophy were nearly equal in terms of parsimony (Blackburn, '83).

Nevertheless, under some well-defined assumptions, a few provisional inferences are possible. Using monotremes as an outgroup, and assuming that marsupials and eutherians stemmed from a common ancestor that was viviparous and placentotrophic (Lille- graven, '75, '79), the presence of a shell membrane, deutoplasmolysis, and microlecithality seem likely to be primitive for therians, as Lillegraven ('85) has suggested. However, under the same assumptions, and barring major reversions by insectivorans and ma- croscelideans, the murine pattern of blastocyst formation (supra vide) must be a derived feature that originated sometime after the origin of the infraclass Eutheria. Conse- quently, if a murine-like developmental pattern is to be the criterion by which homologous trophoblastic tissues are de-

fined, then it must follow that some eutherians lack trophoblast. Use of other criteria for recognition of trophoblast homologues, however, leads to the very different conclusion that trophoblast is common to all therians (Luckett, '77). Clearly, one's interpretation of the evolutionary history of the trophoblast strongly depends upon the particular criteria adopted for defining trophoblast homologies.

ISSUES OF HOMOLOGY

Central to the view that the blastocoel and the tissue forming the blastocyst walls are not homologous between eutherians and metatherians is the presumed absence of phe- notypic and phylogenetic intermediates between nominal "eutherian" and "metatherian" developmental patterns. However, phenotypically intermediate patterns do exist, as seen in the insectivorans and macro- scelideans discussed above. Other eutherians that do not strictly conform to the "eutherian pattern" of early development include the lemur Galago demidovi (GBrard, '32) and the shrew Crocidura caerula (Tyndale-Biscoe and Renfree, '87). The existence of such developmental patterns, with characteristics of the patterns of metatherians and of more typical eutherians, is striking evidence that blastocyst similarities in the two therian groups manifest a common developmental plan.

Most investigators (e.g., Hill, 'lo, '18; Minot, '11; Hartman, '16, '19) of marsupial development have interpreted the area of enlarged cells at the embryonic pole of the blastocyst as being destined to give rise to the embryo proper, and therefore as being homologous to the eutherian inner cell mass. It follows from this interpretation that the re- mainder of the ectoderm of the marsupial blastocyst corresponds to the eutherian trophoblast (Hill, '10; Luckett, '77). In contrast, McCrady ('38) contended that no distinction could be made in the marsupial blastocyst between cells destined for embryonic and extraembryonic fates, and that the "embryonic" area of enlarged cells simply represents the neural (medullary) plate.

Interpretations advanced by McCrady ('38, '44) are difficult to reconcile with known aspects of vertebrate embryogeny. A basic feature of vertebrate development is the induction of neural plate formation by the underlying mesoderm (see Spemann and Mangold, '24; Spemann, '38; Waddington and Schmidt, '33). Thus, neural plate formation follows formation of the primitive streak. Yet,


McCrady (’38, p. 53) spoke of the “primitive streak arising within the neural plate” of the opossum Didelphis uirginiana. The area in question is unlikely to represent the neural plate; it develops prior to primitive streak formation and differentiates while in contact with endoderm (Hartman, ’19; McCrady, ’38). To account for the discrepancy, McCrady (‘38) suggested that this layer of endodermal cells included presumptive mesoderm. His interpretations would seem to require D. uirginiana to be fundamentally different from eutherians and other vertebrates with respect to developmental patterns and induc- tive mechanisms. Also untenable is Mc Crady’s (’44) suggestion that the neural plate of eutherians is represented by the embryonic disk.

Regarding the view that embryonic and extraembryonic ectoderm cannot be distin- guished anatomically in the bilaminar blastocyst of marsupials (McCrady, ’38), the matter is still undecided because of insufficient evidence and, in some respects, may be moot. Descriptive studies of fixed whole mounts and histological sections, such as were used by McCrady and his contemporar- ies, can provide only a crude approximation of cell fates and tissue origins. During the past 10 years, the use of labeled and trans- planted primordia has permitted substantial revision of the classical fate maps of several representative vertebrates (e.g., see Le Douarin and McLaren, ’84; Noden, ’83, ’84; Rossant and Papaioannou, ’77; Smith and Malacinski, ’83). Because such techniques have not yet been applied to marsupials (Sel- wood, ’861, judgement should be withheld pending more definitive experimental evidence. An additional consideration is that cell determination often precedes anatomical differentiation. Thus, the important issue is the time of appearance of precursor populations in the blastocyst and the factors deter- mining their fates, rather than whether cellular progenitors of embryonic and chorionic ectodermal tissues are structurally distinct.

The argument that the eutherian trophoblast is a neomorphic tissue without a homologue in marsupials has several puzzling implications. For example, if one accepts the idea that the ectodermal chorion of marsupials is not equivalent to the trophoblast of eutherians, then where is the ectodermal chorion of eutherians, or is there any? Like- wise, if the epidermis arises from the ectocho-

rion in marsupials (McCrady, ’38) but develops strictly from the inner cell mass in eutherians (Kaufman, ’83, Fig. 2), then does it follow that the marsupial and eutherian epidermises are not homologous?

The discrepancy between Lillegraven’s (‘85) interpretations and our own may reflect in part the absence of clear criteria for applying the concept of homology to early developmental stages. Indeed, the absence of such criteria constitutes a difficult, unresolved problem for evolutionary and developmental biology. Lillegraven (’85, p. 296) stated “No cellular unit of the eutherian blastula is rec- ognizable unequivocably as the homologue of a specific part of a marsupial blastocyst.” This approach applies the concept of homology as a phylogenetic tool to cells at a time when their prospective potencies for differentiation may be far greater than their prospective fates. In isolation from the early blastocyst, the inner cell mass can be fully capable of giving rise to elements normally derived from trophectoderm, as in vivo and in vitro experiments with disaggregated mouse embryos have shown (Kaufman, ’83). Such developmental lability greatly compli- cates, if not invalidates, routine usage of the homology concept for cell populations of early development. de Beer (’71) addressed this issue in his treatise on homology:

It does not seem to matter where in the egg or the embryo the living substance out of which homologous organs are formed comes from. Therefore, correspondence between homologous structures cannot be pressed back to similar- ity of position of the cells of the embryo or the parts of the egg out of which these structures are ultimately differentiated.

It appears to be a vertebrate “strategy” in embryogenesis t o rely heavily on mechanisms of cell interactions, or “power of regu- lation” (Weiss ’39) to achieve cellular commitment. Such cellular determination may develop as a consequence of cell posi- tioning and may be progressive at the cellular level rather than synchronous throughout the embryo (Gerhart et al., ’83; Kaufman, ’83). This pattern provides vertebrates with tremendous ontogenetic latitude as they be- gin to fashion their embryos (in utero, in an eggshell, or elsewhere; with different


amounts of yolk; under different tempera- tures and metabolic rates; etc.), before mov- ing toward a stage of commitment and the expression of homologies during organogen- esis. In fact, interactive mechanisms may ex- plain how a particular germ layer or tissue can arise in different ways in related organ- isms, as is often the case among vertebrates.

It is important to recall that another “new” extraembryonic membrane in amniotes, the amnion, also varies in its manner of differentiation within the Mammalia (see Luckett, ’77, for a review). The amnion is formed by folding of the extraembryonic somatopleure in monotremes, marsupials, and many eutherians, but develops by cavitation within the inner cell mass in certain other eutherians. Both modes of formation are represented within the orders Rodentia, Chiroptera, Primates, and Insectivora, whereas artiodactyls and some primates exhibit a mode of amniogenesis intermediate between folding and cavitation. Were it not for the fact that patterns of amniogenesis cut across well-established taxonomic bounda- ries, it might be tempting to use differences in amniogenesis to separate eutherians phy- logenetically into two or more major groups nearly at the level of the eutherian-marsupial division. But historically, despite suggestions that various features of amniogenesis may be “primitive” or “advanced,” the name amnion has long been applied to that extraembryonic membrane in all amniotes.

FUNCTIONAL-MORPHOLOGICAL CRITERIA

Another perspective rests on the original proposal (Hubrecht, 1888, 1889) and subse- quent acceptance of a functional-morphological definition for the term “trophoblast.” In all marsupials and eutherians for which we have relevant information, the tissue known as “trophoblast” exhibits the functions rec- ognized by Hubrecht and those implied by the etymology (see Lillegraven, ’85) of the term. Furthermore, marsupial trophoblast, like eutherian trophoblast, has been impli- cated in maternal-embryonic physiological exchange (Renfree, ’73, ’83; Tyndale-Biscoe et al., ’741, implantation (Hughes, ’74; Luck- ett, ’771, contribution to the placental membranes (e.g., Hill, ’10; Padykula and Taylor, ’76; Sharman, ’61; Krause and Cutts, ’85), and steroid metabolism (Bradshaw et al., ’75; Heap et al., ’80; Renfree, ’83). Whether the trophoblast plays an immunological role dur-

ing pregnancy remains largely unknown in most marsupials and several major eutherian groups, although indirect evidence on one marsupial species suggests the possibility of some sort of fetal barrier to immunological rejection by the mother, presumably at the placental fetomaternal junction (i.e., the chorionic-decidual interface) (Walker and Tyn- dale-Biscoe, ’78; Renfree, ’83; Rodger et al., ’85; Tyndale-Biscoe and Renfree, ’87). How- ever, even if marsupial trophoblastic tissues eventually were demonstrated to have no immunological functions, this demonstration would provide but another example of the considerable functional and phylogenetic diversity of this extraordinary tissue among mammals.

The term “trophoblast” is unusual in our biological lexicon with respect to the clarity and consistency of its usage. In contrast, in- consistency and ambiguity have historically accompanied the application of several other terms to extraembryonic membranes, including “chorion” and “choriovitelline” (see Mossman, ’37; Ramsey, ’82; Stewart, ’85; Stewart and Blackburn ’88). No other available term is as precise and descriptive in denoting the functionally important tissue known in marsupials as “trophoblast.” “Ec- todermal chorion” is insufficient in that it omits extraembryonic ectoderm of the uni- laminar blastocyst, of the bilaminar blastocyst, and of the bilaminar omphalopleure, none of which is truly “chorionic” (see Moss- man, ’37). Substitutions of “choriovitelline membrane” and “chorioallantoic membrane” are imprecise in that these two terms are much more inclusive than “trophoblast” and are inadequate because such usage provides no term for the functionally active blastocyst tissue of marsupials prior to estab- lishment of these two membranes.

Boyd and Hamilton (’52, p. 96) summarized the situation well:

Whatever its phylogenetic origin and nature may be, it is the trophoblast which forms the outer, bounding layer of the developing mammalian zygote and through it in the early post-cleavage stages of development all ex- changes between embryo and maternal organism must take place. In many eutheria, indeed, the trophoblastic bounding layer per- sists throughout gestation. The


trophoblast in the course of development becomes lined with extraembryonic somatopleuric mesoderm and the two layers together are called the chorion (‘true’ chorion or serosa).

Indeed, by this functional definition, per- haps the term “trophoblast” should be applied as well to those nonmammalian amniotes (e.g., see Giacomini, 1891; ten Cate- Hoedemaker, ’33; Weekes, ’35; Blackburn and Vitt, ’84; Blackburn et al., ’84) in which extraembryonic ectoderm has the capacity to absorb exogenous nutrients from a maternal source. Application of the term “trophoblast” to placentotrophic nonmammals does have precedent in the literature (Hubrecht, ’08; ten Cate-Hoedemaker, ’33; Delsol et a1 ., ’81). Lillegraven (‘79, ’85) has also acknowledged a physiological definition for the term “trophoblast.” Therefore, general acceptance of the term “trophoblast“ to denote a functional component of the extraembryonic portion of certain reptiles as well as mammals, along with recognition that it is inappropriate to use uncommitted embryonic cells as phylogenetic markers, appear sufficient to resolve this problem.

TERMINOLOGICAL BIASES AND EVOLUTIONARY INTERPRETATIONS

After several decades of neglect, the evolutionary history and adaptive significance of mammalian reproductive patterns have re- cently been receiving attention on a broad scale. A variety of conflicting interpretations are being supported in the literature (e.g., see Sharman, ’70, ’76; Miiller, ’73; Tyndale- Biscoe, ’73; Renfree, ’77, ’81, ’83; Hayssen, ’85). Lillegraven (‘69, ’75, ’79) has contrib- uted valuably to this dialogue as an eloquent proponent of the view that extant marsupials are adaptively inferior and reproductively primitive to the living eutherians. According to this interpretation, the closest common ancestor of extant metatherians and eutherians was viviparous and reproduced much as do living marsupials. Among the several alternative interpretations are that viviparity evolved independently in metatherians and eutherians (Sharman, ’70; Tyndale-Bis- coe, ’73, that monotremes re-evolved ovipar- ity from viviparity (Mossman, ’87), and that extant marsupials exhibit a specialized reproductive pattern that may be adaptive in

particular circumstances (Parker, ’77; Kirsch, ’77; Hayssen et al., ’85).

As the controversy continues, it is essential to guard against latent biases implicit in terminological usage. For example, the largely synonymous terms “placental mammal” and “eutherian” falsely imply that marsupials lack functional placentae and are other than “true” therian mammals. These and other such terminological problems have been discussed by Padykula and Taylor (‘82), Renfree (’831, and Hayssen et al., (‘85).

“Trophoblast” is an example of a term whose usage has the potential to prejudice discussion toward a particular view of mammalian reproductive evolution. Simply by re- stricting use of the term “trophoblast” to eutherians, it becomes easy to argue that trophoblast is an innovation unique to eutherians, and that by lack of this tissue marsupials are primitive and inferior to eutherians. Alternatively, such usage could also promote the scenario in which marsupials and eutherians independently have evolved placentation (and viviparity), the rationale being that placental functions are accomplished by “nonhomologous” tissues. These considerations provide further justification for not placing taxonomic restrictions on usage of the term.

By the same token, suggested application of the term “trophoblast” to all therian mammals ought not necessarily to be taken as support for the concept that eutherians and marsupials share a common viviparous ancestor that reproduced via a microlecithal blastocyst. Nor should trophoblast be uncrit- ically regarded as a synapomorphy that u- nites the therian subclasses or links them to placentotrophic reptiles. Recognition of the general (broad) homologies of the derivatives of extraembryonic ectoderm among amniotes (Luckett, ’77), along with the recommended use of the term “trophoblast” in a functional-morphological sense (Hubrecht, 18891, should help t o ensure that the evolutionary issues continue to be judged on the basis of empirical rather than semantic considerations.

ACKNOWLEDGMENTS

For offering comments on drafts of the manuscript, we are indebted to Drs. Virginia Hayssen, Ha A. Masar, Harland W. Moss- man, Oliver P. Pearson, James R. Stewart, Wesley K. Whitten, and several anonymous reviewers. We gladly acknowledge Dr. Drew


M. Noden for suggesting some relevant literature, and Dr. Marilyn B. Renfree for pro- viding prepublication book excerpts (Tyndale- Biscoe and Renfree, ’87). We also wish to thank Dr. Jason A. Lillegraven for stimulat- ing and supporting discussion of the issues. This work was supported in part by NIH Training Grant HD-07043 (to D.G.B.). This is technical paper No. 8038, Oregon Agricul- tural Experiment Station.

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Trophoblast concept as applied to therian mammals

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