Suckerfooted Bats

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Female Reproductive Tract and Placentation in Sucker-Footed Bats(Chiroptera: Myzopodidae) Endemic to Madagascar

A.M. Carter a ,*, S.M. Goodman b ,c , A.C. Enders d

a Department of Physiology and Pharmacology, University of Southern Denmark, Odense DK-5000, Denmark b Field Museum of Natural History, Chicago, IL, USA

c Vahatra, Antananarivo, Madagascar d Department of Cell Biology and Human Anatomy, University of California, Davis, CA 95616, USA

Accepted 20 February 2008

Abstract

The reproductive tract was examined in four non-pregnant and two gravid specimens of Myzopoda . The ovaries had little interstitial tissue.The uterus was bicornuate and the lenticular placental disk was situated mesometrially in one horn. The interhaemal barrier of the placentallabyrinth was of the endotheliomonochorial type. There was a single layer of trophoblast cells. The cells of the maternal endothelium were largeand basophilic, contained abundant rough endoplasmic reticulum, and rested on an irregular basement membrane. Blunt projections of endo-metrium extended into the placental disk and clusters of large cells occurred between the endometrial stroma and labyrinth. At the marginsof the disk folds of trophoblast occurred and at the cranial end they formed an haemophagous region. The folds lateral to the disk includedsome peculiar tubular-appearing structures. There was a persistent yolk sac containing large endodermal cells around a largely collapsed lumen.Several features of placentation, such as the interhaemal barrier and the haemophagous region, are consistent with an association of Myzopo-didae with Emballonuridae. No support was found for alternative hypotheses that include Myzopodidae in the noctilionoid or vespertilionoid

lineages.Ó 2008 Elsevier Ltd. All rights reserved.

Keywords: Comparative placentation; Fetal membranes; Haemochorial placentation; Haemophagous region; Trophoblast

1. Introduction

Next to Rodentia, Chiroptera is the mammalian order withthe greatest number of species. The fossil record of bats is in-complete, but they seem to have undergone a rapid radiation in

the early Eocene coincident with an increase in plant diversityand a peak in insect abundance [1]. Perhaps this explains thegreat diversity in their placentation, which has been remarkedupon by several authors [2e 4]. Currently 18 families of batsare recognized in molecular and morphological studies [5e 8].

The sucker-footed bats, genus Myzopoda (Myzopodidae),are endemic to Madagascar. Their name is derived from

adhesive pads borne on the thumb and hind foot. Structureswith a similar function but different morphology are foundin the disc-winged bats, genus Thyroptera (Thyropteridae),a remarkable instance of convergent evolution [9]. Two spe-cies of Myzopoda are now recognized [10]. Myzopoda aurita

occurs in the humid eastern forests of Madagascar, whilst M.schliemanni occurs in the dry western forests of the island. Al-most nothing is known of reproduction in either species. Wehere present information on the female reproductive tractand denitive placentation of both species.

2. Materials and methods

The reproductive tract was studied in situ and the external genitalia exam-ined in four non-pregnant females, one of M . aurita and three of M . schlie-manni (Table 1). A pregnant uterus and both ovaries were taken from

* Corresponding author. Tel.: þ 45 6550 3716; fax: þ 45 6613 3479. E-mail address: [email protected] (A.M. Carter).

0143-4004/$ - see front matter Ó 2008 Elsevier Ltd. All rights reserved.

doi:10.1016/j.placenta.2008.02.009

Available online at www.sciencedirect.com

Placenta 29 (2008) 484 e 491

mailto:[email protected]

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a specimen of M. aurita that had been xed and then stored in 70% alcohol. Apregnant uterus and both ovaries of M . schliemanni were removed in the eldand xed in Karnovsky’s xative, i.e. 2.5% paraformaldehyde and 2.5% glu-taraldehyde in 0.1 M phosphate buffer.

After dissection to establish the gross morphology, the ovaries and portionsof the placenta and fetal membranes were removed and embedded in Aralditeepoxy resin for semi-thin sectioning. Tissues from M. schliemanni were rstprocessed for transmission electron microscopy (TEM) by postxation in2% osmium tetroxide prior to dehydration and embedding in plastic. A totalof 1 mm sections were stained with Azure B and examined by light micros-

copy, after which selected regions were thin-sectioned and examined by TEM.

3. Results

The external genitalia were characterized by a small clitoralpad and transverse orientation of the vulval opening. Theuterus was bicornuate. Pubic nipples were not present.

In both pregnant animals, the fetus and placenta were situ-ated in one horn of the bicornuate uterus, which was greatlyenlarged in the cranial direction. The corpus luteum was inthe ovary from the same side in one animal and in the ovaryof the opposite side in the other. None of the four ovaries

had more than a small amount of interstitial tissue, and the tis-sue present was conned to the hilus, suggesting that it was of embryonic origin.

The placental disk was situated mesometrially and a col-lapsed yolk sac was situated beside the disk. In one specimenthe yolk sac was rod shaped and slightly longer than the disk (Fig. 1A); in the other it was attened and substantially longerthan the disk of the chorioallantoic placenta. Except for therelatively poor xation of the specimen of M . aurita , anda more compact yolk sac, the two placentae were similarand will be described together.

The discoidal placenta was approximately 7 Â 9 mm, beingelongated in the cranio-caudal direction. The umbilical cordwas situated closer to the caudal end than the centre of thedisk. There were two umbilical arteries and a single vein.The more cranial aspect of the disk had a pinkish area whichproved to be a small haemophagous region. A yolk sac duct joined the umbilical cord close to the surface of the placentaldisk.

The placental disk was a lenticular structure, superciallylobulated on the fetal surface where allantoic arteries accom-panied by a small amount of connective tissue extended intothe labyrinth (Figs. 1B and 2A). The junctional zone betweenthe labyrinth and the endometrium underlay most of the pla-cental disk, with the margins of the disk extending laterally

over the surface of the uterine luminal epithelium.

The underlying endometrium was irregular, with blunt projections extending into the placental disk (Figs. 1B and 2B).Between the less modied stroma of the endometrium andthe labyrinthine portion of the disk was a region of large cells.Some of these cells were clustered and others intercalated be-tween the clusters ( Fig. 2C,D). In a few regions, clearly decid-ualized stromal cells could be found towards the lessdecidualized endometrium.

The fetal side of the placental disk had numerous arteriesand venous sinuses. Extending down into the disk from thissurface were branches of the arteries, giving rise to the abun-dant small capillaries seen throughout the labyrinth ( Fig. 2A).Maternal vessels appeared to extend into the labyrinth fromsome of the endometrial projections ( Fig. 2B). Areas of con-uence of maternal placental capillaries into endometrial veinswere found near the junctional region ( Fig. 3A).

Within the labyrinth, the endothelial cells of the maternalcapillaries were cuboidal and strongly basophilic ( Fig. 3A).They were typically surrounded by a single layer of largepale cytotrophoblast cells ( Fig. 3B,C). The intercalated fetalvessels were unremarkable with normal squamous

endothelium.

Table 1Specimens of Myzopoda spp. examined

Species Museum Collection No. Description

Myzopoda aurita FMNH 184490 Pregnant femaleFMNH 92832 Non-pregnant female

Myzopoda schliemanni FMNH 185791 Subadult femaleFMNH 185792 Non-pregnant femaleFMNH 185794 Non-pregnant femaleFMNH 187610 Pregnant female

Abbreviation: FMNH, Field Museum of Natural History, Chicago.

Fig. 1. A. General view of the placental disk, elongated yolk sac and fetus. B.Section through the placental disk to show the endometrial projections (endoproj), labyrinth, and marginal folds. The fetal surface is lined by chorionicmesenchyme containing some prominent allantoic blood vessels. A segmentof the chorioallantoic membrane appears at far left. Much of the space be-tween the placenta and uterine wall is artefactual. Scale bars ¼ 2 mm (A),

0.85 mm (B). M. aurita (A); M. schliemanni (B).

485 A.M. Carter et al. / Placenta 29 (2008) 484 e 491



Examination of the ultrastructure of the labyrinth illus-trated that the maternal endothelial cells had abundant roughendoplasmic reticulum ( Figs. 4 and 5). Beneath these cellswas a thick but irregular basement membrane with occa-sional discontinuities where the trophoblast cells occasion-ally abutted the endothelium. The trophoblast cells thatsurrounded the maternal capillaries were large cells coupledby distinct junctions ( Fig. 5). They had a small amount of rough endoplasmic reticulum that had a distinct contentbut were not otherwise particularly rich in organelles. Thebasal lamina underlying the trophoblast was thinner andmore regular than that underlying the maternal endothelium.Although the fetal capillaries did not indent the trophoblast

surrounding maternal vessels, they were directly apposed to

the trophoblast with little or no intervening connectivetissue.

The folds at the lateral margins of the placental disk fre-quently had two layers of trophoblast ( Fig. 6A), and occa-sional masses of syncytiotrophoblast were found in thislocation. Some peculiar tubular-appearing structures werealso present ( Fig. 6A,B). These structures had an outer layerof cuboidal trophoblast cells and a tall inner layer of cells adjacent to maternal blood. The inner layer of cells showed ev-idence of fusion and had a band of heavy-staining material ina subapical position, which by TEM was amorphous and wasnot membrane-bound (not shown).

At the cranial end of the placenta were folds of columnar

trophoblast surrounding maternal blood ( Fig. 6C,D). Many

Fig. 2. A. Placental labyrinth showing large fetal artery entering from the surface and branching towards the endometrium. B. Part of the labyrinth and anendometrial projection containing sections of a maternal artery. C. Endometrium with clusters of large cells and a large maternal vessel (mv) surrounded bydecidualized stromal cells. D. Clusters of large cells interposed between the maternal vessel and the labyrinth. Scale bars ¼ 80 mm (A, B), 35 mm (C), 22 mm(D). M. schliemanni (A, C, D); M. aurita (B).




of the cells composing these trophoblast sacs contained in-gested erythrocytes. Other patches of columnar cells withingested erythrocytes were also found continuous withmore typical regions of the labyrinth at this end of the pla-centa and constituted part of the irregular haemophagousregion.

The chorioallantois extending peripherally from the placen-

tal disk had a simple single layer of trophoblast, was

vascularized, and was situated over a layer of low cuboidal lu-minal epithelial cells that had numerous large vacuoles(Fig. 7A). A few endometrial glands were found in some of the decidua basalis underlying the peripheral aspects of the

Fig. 3. A. Conuence of maternal vessels (mv) in the junctional regionbetween labyrinth and endometrium. B. Detail of the labyrinth showing thebasophilic endothelium of maternal capillaries (mat cap) and fetal capillaries(fet caps) with more squamous endothelium. C. Detail of the labyrinth show-ing maternal and fetal capillaries and the paler trophoblast cells (troph). Scalebars ¼ 54 mm (A), 13 mm (B, C). M. schliemanni .

Fig. 4. Placental labyrinth showing two maternal capillaries with enlargedcuboidal endothelial cells and each with a thick, irregular basement membrane(short arrows). There are occasional discontinuities in the basement membranewhere the trophoblast cells (troph) abut the endothelium. Note the fetal capil-lary at upper left. Scale bar ¼ 6.4 mm. M. schliemanni .

Fig. 5. Detail of the labyrinth showing maternal endothelial cells withabundant rough endoplasmatic reticulum (rer) and part of two trophoblastcells (troph) with few organelles but distinct junctions (short arrow). Notethe capillary at lower right (long arrow). Scale bar ¼ 3.0 mm. M. schliemanni .




disk, but the rest of the basal decidua and the parietal deciduawere remarkably free of such structures.

The largely collapsed yolk sac was similar to that seen inmany species of bats, including vespertilionids. The robust ba-sophilic endodermal cells lining the remnants of the yolk saccavity formed a continuous layer of cuboidal to columnar cells(Fig. 7B). Between these and the mesothelial cells was a smallamount of fetal connective tissue and numerous capillaries.The overlying mesothelial cells, rather than being squamous,formed a continuous cuboidal layer but were not as basophilicas the endothelial cells.

4. Discussion

The female genital tract and placentation of Myzopoda spp.share some characters with all bats, have one unique featureand fail to support either of the current hypotheses on the phy-logenetic position of Myzopodidae.

The presence of a cellular trophoblast layer in an endothe-liomonochorial placental relationship is found in other batssuch as Natalus (Natalidae) and Saccopteryx (Emballonuridae)[3] and also in the kangaroo rat Dipodomys [11] and Africanelephant Loxodonta [12]. Both endotheliochorial placentaewith cellular trophoblast and those with syncytial trophoblastshow regions where maternal endothelium and trophoblastcontact one another through a variably thick basement

membrane. The situation in Myzopoda , however, is relatively

simple in showing short blunt contacts. The presence of such contacts in all endotheliochorial placentae suggests that

such regions function in information signaling between mater-nal and fetal organisms. The trophoblast layer in Myzopodawas not indented by the fetal capillaries, as is usually foundin later stages of placentation in other species with endothelio-chorial placentae.

The structure of the margins of the placental disk was quiteinteresting. Only in the cranial region did peripheral tropho-blast folds develop haemophagous areas. In the rest of thedisk, some of the folds had two layers of trophoblast whichfor the most part were closely apposed but in other areasformed tubular-appearing structures that had a unique innersyncytiotrophoblast layer often encompassing maternal blood.Such structures have not been described in any other bat, andtheir functional signicance is not apparent. A developmentalseries might provide better clues both as to their possible func-tion and as to whether or not the placental labyrinth per se wasinitially endotheliodichorial before becoming endotheliomo-nochorial as occurs in Natalus and Saccopteryx [3].

The general pattern of maternal blood entering fromprojections into the placenta and returning to regions be-tween such projections and that of fetal blood branchingoff arteries extending well into the placenta to return viacapillaries to the fetal surface suggests only partial counter-current ow. The pattern could be studied better by vascularcasts to determine the denitive relationships of maternal and

fetal vessels.

Fig. 6. A. Folds of bilaminar trophoblast at the margin of the placental disk (arrow). Several tubular structures are formed from some of these folds. A section of theperipheral allantois is at lower left. B. Parts of two tubular structures from the margin of the disk. They are surrounded by a thin connective tissue containing fetalcapillaries. There is then an outer layer of cuboidal trophoblast cells (outer troph) and an inner cell layer (inner troph) that includes a band of darkly stainingmaterial. The lumen of each tube contains maternal blood, slightly shrunken away from the trophoblast surface. C. Cranial folds encompassing maternal bloodwith patches of columnar trophoblast cells that contain ingested erythrocytes (haemophagous cells). D. Detail of a haemophagous region showing columnar tro-phoblast cells with ingested erythrocytes. Scale bars ¼ 140 mm (A), 13 mm (B), 54 mm (C), 34 mm (D). M. schliemanni .




4.1. Phylogenetic implications

There is general agreement to recognize four superfamiliesof microbats [1,6,8,13] . These are currently Rhinolophoidea,Emballonuroidea, Noctilionoidea and Vespertilionoidea.Recent phylogenies based on DNA sequence analysis place Myzopoda either in Noctilionoidea [1] or Vespertilionoidea[6]. However, alternative topologies, including an associationof Myzopoda with Emballonuridae and Nycteridae, cannotbe rejected on the basis of molecular data [6].

Noctilionoidea is well supported in cladistic analyses of de-velopmental data [14,15] . Two of the character transforma-tions supporting this group are orientation of the vulva in ananterior-posterior direction and enlargement of the clitoris[15,16] . Like most other bats, Myzopoda has transverse orien-tation of the vulva and a small clitoral pad. Five additionalcharacters that support Noctilionoidea are concerned withearly development. They include development to the blasto-cyst stage within the Fallopian tube, features of implantation,

and amniogenesis by cavitation [15]. Thus, it would be

necessary to have a developmental series of Myzopoda in orderto complete the comparison.

Abundant interstitial gland tissue is a consistent feature of Vespertilionoidea [15] although it also occurs in Thyroptera[17], placed in the Noctilionoidea. In contrast, interstitialgland tissue was quite sparse in Myzopoda .

Emballonuridae is supported by two derived characterconditions: the absence of an allantoic vesicle at all stagesof development and the presence of a haemophagous regionwithin the placenta [15]. Myzopoda had no allantoic vesicleat the stage examined but it is not known whether it isalways absent or is lost in the course of gestation as occursin most other bats [15]. Haemophagous regions are com-prised of columnar trophoblast with the ability to engulf ma-ternal erythrocytes and free their contained iron for use bythe fetus [18]. They are a feature of placentation in manymammals [18], but among bats are seen only in Myzopodaand in Emballonuridae, where they have been found in sixdifferent genera [19].

Endotheliochorial placentation, with retention of thematernal capillary endothelium in late pregnancy, is anotherconsistent feature of Emballonuridae [15]. In noctilionoidsand most vespertilionoids the minimum interhaemal barrierat term is haemochorial, although the placenta is endothelio-chorial in Natalus , which is assigned to Vespertilionoidea [4].For mammals as a whole, this particular character has provendifcult to resolve by cladistic analysis [20]. It can be re-solved for bats only under the assumption of acceleratedcharacter transformation, but endothelial placentation thenappears as a character transformation on the lineage of Em-ballonuroidea [15] .

Thus none of the characters we have examined offersupport for inclusion of Myzopoda in Noctilionoidea [1] orVespertilionoidea [6] (Table 2 ). There is, however, somesupport for an alternative scenario that includes Myzopodawith Emballonuridae and Nycteridae [6]. This includesthe nature of the interhaemal barrier and the presence of a haemophagous region. To further examine this hypothesiswe would need to examine a full developmental series of Myzopoda . In addition a study of placentation in Nycteridaeis greatly overdue.

Little is known about the reproductive biology of Myzo- poda spp. The two pregnant specimens were caught in Sep-tember and October. Each bore a single embryo, as do mostbats. Both embryos were in the left horn but in one the corpusluteum was found in the right ovary. Asymmetry of the repro-ductive tract, usually with the right side dominant, is commonin bats and may be an ancient feature [21], but the characterconditions are quite variable [15].

In conclusion, we have studied denitive placentation in Myzopoda and describe some tubular structures of unknownfunction that are unique to the genus. Several features of pla-centation, especially the interhaemal barrier, which is endothe-liomonochorial, and the presence of a haemophagous regionare coherent with an association of Myzopodidae with Embal-lonuridae. No support was found for alternative hypotheses

that include the Myzopodidae in Noctilionoidea or

Fig. 7. A. Chorioallantois peripheral to the disk. Above is chorionic mesodermwith fetal capillaries. A single layer of basophilic trophoblast cells is apposedto the uterine epithelial cells (ut epithelium), which appear vacuolated. Bloodvessels (bv) are seen in the endometrial stroma. B. Portion of the yolk sac. Theendoderm adjacent to the collapsed lumen comprises large, columnar, baso-philic cells. The connective tissue between the endoderm and the pale cuboidalmesothelial cells is sparse but well vascularised. Scale bars ¼ 13 mm (A),34 mm (B). M. schliemanni .




Vespertilionoidea. Further studies including early develop-mental stages might throw light on the phylogenetic afnitiesof this interesting family.

Acknowledgements

We thank Dr. Thomas N. Blankenship for stimulating dis-cussions. The nancial support of The Carlsberg Foundationis gratefully acknowledged (AMC). Fieldwork associatedwith the collection of these specimens was supported by grantsfrom the John D. and Catherine T. MacArthur Foundation,Volkswagen Foundation and Benecia Foundation (SMG).We are grateful to the Malagasy authorities for permits to con-duct these eld programs.

References

[1] Teeling EC, Springer MS, Madsen O, Bates P, O’Brien SJ, Murphy WJ.A molecular phylogeny for bats illuminates biogeography and the fossilrecord. Science 2005;307:580 e 4.

[2] Gopalakrishna A, Karim KB. Female genital anatomy and the morpho-genesis of foetal membranes of Chiroptera and their bearing on the phy-logenetic relationships of the group. In: Srivastava US, editor. GoldenJubilee Commemoration, Volume 1980. Naya Prokash, Calcutta: TheNational Academy of Sciences; 1980. p. 379 e 428.

[3] Enders AC, Blankenship TN, Lantz KC, Enders SS. Morphological var-iation in the interhemal areas of chorioallantoic placentae. In: Carter A,Dantzer V, Jansson T, editors. The maternal fetal interface. vol. 12.Trophoblast Research; 1998. p. 1 e 19.

[4] Badwaik NK, Rasweiler 4th JJ. Pregnancy. In: Crichton EG, Krutzch PH,editors. Reproductive biology of bats. San Diego: Academic Press; 2000.p. 221e 93.

[5] Jones KE, Purvis A, MacLarnon A, Bininda-Emonds OR, Simmons NB.A phylogenetic supertree of the bats (Mammalia: Chiroptera). Biol RevCamb Philos Soc 2002;77:223 e 59.

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Springer MS, Teeling EC. A family matter: conclusive resolution of the taxonomic position of the long-ngered bats, Miniopterus. MolBiol Evol 2007;24:1553 e 61.

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Table 2Comparison of reproductive tract and placentation in Family Myzopodidae with Superfamilies Noctilionoidea, Vespertilionoidea and Emballonuroidea

Character a Myzopodidae Noctilionoidea Vespertilionoidea Emballonuroidea

Vulva (1) Transverse orientation Anter ior-posterior orientation Transverse or ientation Transverse orientationClitoris (2) Small clitoral pad Elongated clioris Small clitoris Small clitorisUterine morphology (3) Bicornuate Bicornuate with evolutionary

transformation to simplex uterusBicornuate Unresolved: bicornuate or

duplex uterusOvarian interstitial

gland tissue (4)Sparse Sparse Abundant Sparse

Denitive yolk sac (16) Partially inverted Partially inverted Partially inverted Gland-like withreduced lumen

Allantoic vesicle (17) Absent in lategestation

Absent in late gestation Unresolved: absent in lategestation or rudimentarythroughout

Rudimentary throughoutgestation

Location of denitiveplacenta (18)

Mesometrial Lateral to mesometrial withseveral evolutionary transformations

Facing uterotubal junctionwith evolutionary transformationto antimesometrial

Lateral to mesometrial

Gross form of placenta (19) Single disc Single disc Single disc with evolutionarytransformations to double disc

Single disc

Overall structure of placenta Labyrinthine Labyrinthine Labyrinthine LabyrinthineInterhaemal barrier (20) Endotheliochorial Haemochorial Haemochorial with evolutionary

transformation to endotheliochorialin Natalus

Endotheliochorial

Type of trophoblast inbarrier (21)

One layer of cytotrophoblast

Two layers: syncytio- andcytotrophoblast

Unresolved One layer of cyto- orsyncytio-trophoblast

Intrasyncytial membrane Not applicable Present Present Not applicableNumber of umbilical

vesselsTwo arteries andone vein

Two arteries and one vein Two arteries and one vein Two arteries and one vein

Haemophagous regions (22) Present Absent Absent PresentEndometrial stroma Decidua present Decidua present Decidua present Decidua presentNumber of offspring (23) One One One with transformation

to two or moreOne

Pubic nipples (25) Absent Absent Absent Absenta Numbers in brackets refer to characters in Carter and Mess [15] . Unnumbered characters were not phylogenetically informative in that study.




[13] Smith JD. Chiropteran evolution. In: Baker RJ, Jones JK, Carter DC, ed-itors. Biology of bats of the new world family phyllostomatidae, Part I.Lubbock: Texas Tech Press; 1976. p. 49 e 69.

[14] Luckett WP. The use of fetal membrane data in assessing chiropteranphylogeny. In: Wilson DE, Gardner AL, editors. Proceedings Fifth Inter-national Bat Research Conference. Lubbock: Texas Tech Press; 1980.p. 245e 65.

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Thyroptera tricolor spix (Microchiroptera: Thyropteridae). Am J Anat1980;159:209 e 43.

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[19] WimsattWA,GopalakrishnaA. Occurrence of a placental hematoma in theprimitive sheath-tailed bats (Emballonuridae), with observations on itsstructure, development and histochemistry. Am J Anat 1958;103:35 e 67.

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[21] Wimsatt WA. Reproductive asymmetry and unilateral pregnancy in Chi-roptera. J Reprod Fertil 1979;56:345 e 57.


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