Reviews of Reproduction (2000) 5, 6–11

Maternal recognition of pregnancy in

Marilyn B. Renfree

Department of Zoology, University of Melbourne, Parkville, Victoria 3052,

Pregnancy in kangaroos and (macropodid marsupials) induces multiple unilateral responses in the reproductive system that override those related to proximity to the single corpus luteum on one ovary or to the follicle on the contralateral ovary. This situation is in contrast to most other non-macropodid marsupials, in which the responses are dependent on the corpus luteum. There is now good evidence that these unilateral responses in macropodids are controlled by the feto–placental unit acting locally to stimulate the endometrium and myometrium. Pregnancy also influences the duration of the oestrous cycle and maternal be- haviour. The stimuli responsible for these effects probably include paracrine, endocrine and mechanical stimuli resulting from uterine stretch. Taken together, these unilateral responses demonstrate that there is a refined maternal recognition of pregnancy in at least the macro- podid marsupials.

The concept of maternal recognition of pregnancy, as described unilateral responses of the pregnant uterus are now well by Short (1969) focused attention on the diverse ways by which defined, particularly for tammar wallabies, which have been the maternal organism first becomes aware of the presence of the subjects of the most detailed studies. an embryo in the uterus. The earliest maternal recognition may occur in the differential tubal transport of fertilized versus un- Pregnancy and the oestrous cycle fertilized eggs, as described by van Niekerk and Gerneke (1966) in horses, but the best studied response is the way in which the The duration of the oestrous cycle varies among lifespan and function of the corpus luteum is prolonged by species from 22 to 45 days, and the lifespan of the corpus the presence of an embryo: originally almost all attention was luteum is not prolonged by the presence of a conceptus, directed to this aspect of maternal recognition. However, ad- although in the bandicoot family, Peramelidae, the corpus vances in understanding of embryo–maternal interactions, luteum persists during lactation (for review, see Tyndale-Biscoe including the local responses of the uterus and the develop- and Renfree, 1987). There is no apparent unilaterally active mental changes in the embryo, have broadened the concept (but systemically inactive) luteolysin derived from the uterus of maternal recognition to include almost all aspects of the since hysterectomy has no effect on opossums or on the corpus ways by which pregnancy can redirect maternal physiology luteum of brushtail possums. The corpus luteum reaches (Heap, 1979). maximum size during the mid-luteal phase, and decreases in In many , the secretory activity of the corpus size toward the end of pregnancy. This pattern is mirrored by luteum is unaffected by pregnancy and, in mammals that have the proliferation and secretory activity of the endometrium. embryonic diapause, maternal recognition must be delayed. The histological changes in the gravid uterus during the fol- Marsupials (Table 1) provide examples of both of these strat- licular and luteal phases are similar to those of the non-gravid egies. The life of the corpus luteum is not extended by pregnancy uterus in monovular and polyovular species (Tyndale-Biscoe in most marsupials and because pregnancy is accommodated and Renfree, 1987). However, closer examination of the endo- within the oestrous cycle in all but one marsupial, these mam- metrial responses provided the first example of maternal rec- mals had been thought to lack any maternal recognition of preg- ognition of pregnancy in marsupials. nancy. Indeed, Hill and O’Donaghue (1913) coined the term ‘pseudopregnancy’ to describe the similarity of the changes Endometrial responses in pregnancy that occurred in the uteri and mammary glands of unmated and mated female marsupials. Despite these superficial simi- As long ago as 1834, Richard Owen recorded that the endo- larities, it is now known that there are changes in maternal metrium of the gravid uterus of the Eastern grey kangaroo was physiology that are specific to pregnancy in marsupials. twice as thick as the endometrium of the contralateral, non- Marsupials offer certain advantages for the study of maternal gravid uterus. Almost 100 years later, Flynn (1930) described recognition of pregnancy because of their unusual reproductive marked histological differences between the gravid and non- anatomy. All marsupials possess two completely separate uteri, gravid uteri of Tasmanian . Both these observations each with a separate cervix but, in the monovular species, only were largely overlooked until the finding, in tammar wallabies, one of these two uteri becomes gravid, and ovulation usually that the wet weight of the endometrium of the gravid uterus was occurs from alternate ovaries, thus providing researchers consistently and significantly greater than that of the adjacent with an inbuilt ‘control’ uterus at all stages of pregnancy. In non-gravid uterus (Renfree, 1972). The proliferation of the macropodid marsupials (the kangaroos and wallabies) many endometrium is always greater in the uterus adjacent to © 2000 Journals of Reproduction and Fertility 1359-6004/2000 Downloaded from Bioscientifica.com at 09/29/2021 04:39:57PM via free access Unilateral responses in marsupial pregnancy 7 the corpus luteum, whether or not pregnancy occurs, but the Table 1. Maternal recognition of pregnancy in marsupials effect is enhanced in the second half of pregnancy compared with the oestrous cycle (Renfree, 1972; Renfree and Tyndale- Species with clear evidence of maternal recognition of pregnancy Biscoe, 1973; Tyndale-Biscoe, 1979). That this enhancement is Kangaroos and wallabies () dependent on the presence of the embryo or its fetal mem- Setonix brachyurus branes was unequivocally demonstrated by the transfer of the Tammar eugenii blastocyst to the uterus of a cyclic, non-pregnant , or to Bennett’s Macropus rufogriseus the uterus contralateral to the corpus luteum. In all cases, simi- Eastern grey kangaroo Macropus giganteus lar endometrial proliferation occurred in the gravid uterus, re- Western grey kangaroo Macropus fuliginosis gardless of its position relative to the corpus luteum (Fig. 1). Potorous tridactylus In in which blastocysts develop in both uteri, both Tasmanian Bettongia gaimardii sides had enhanced endometrial responses. In addition to these Species with some evidence of maternal recognition of pregnancy morphogenetic effects, the composition of the uterine se- cretions differs between the two uteri (Renfree, 1973a; Renfree Dasyurids (Dasyuridae) and Tyndale-Biscoe, 1973; Tyndale-Biscoe, 1979) and the rate Antechinus Antechinus agilis (stuartii) of protein synthesis is greater in the gravid uterus (Shaw Dunnart Sminthopsis macroura and Renfree, 1986). The synthesis of specific uterine secretions Species that apparently lack a maternal recognition of pregnancy (Renfree, 1973a) and growth factors, such as platelet-activating factor (PAF) (Kojima et al., 1993), are also likely to reflect Possums () these unilateral influences. Thus, the importance of the feto– Trichosurus vulpecula placental unit overrides the local effects of proximity to the American opossums (Didelphidae) corpus luteum. Virginia opossum Didelphis virginiana A similar endometrial response occurs in the potoroo (Shaw Grey short-tailed opossum Monodelphis domestica and Rose, 1979), the quokka (Wallace, 1981) and in Bennett’s wallaby (Walker and Rose, 1981). So far, these effects have Bandicoots (Peramelidae) been observed only in macropodids. In monovular non- macropodids, such as the brushtail possum, both gravid and non-gravid uteri respond to a similar extent, although there is of the respective ovarian veins. Evidence to support this also a local effect of the adjacent corpus luteum in brushtail suggestion is provided by the differential concentrations of pro- possums (Von der Borsch, 1963; Curlewis and Stone, 1986). In gesterone (Towers et al., 1986; Kojima et al., 1993) and oestradiol polyovular species, such as opossums, both uteri are gravid, (Harder et al., 1984) sampled from the uterine branch of the but a few values from non-pregnant animals (Renfree, 1975; ovarian vein in tammar wallabies (sometimes labelled er- Fleming and Harder, 1981a,b) indicate an identical endometrial roneously the ‘utero–ovarian vein’) (Fig. 2). Similar unequal response during the oestrous cycle and pregnancy. Likewise, concentrations of progesterone and oestradiol occur in the left there is a similar pattern of histological changes in the gravid and right ovarian veins of brushtail possums (Curlewis et al., and non-gravid uteri in two species of polyovular, dasyurid 1985) but not of opossums (Harder and Fleming, 1981). marsupials, the dunnart and the antechinus (Cruz and Selwood, 1993, 1997), but there are distinct uterine differences in preg- Feto–placental influences nancy and non-pregnancy at some (dunnart) or at most (ante- chinus) time points. These differences may be due to direct Blastocyst development can be initiated experimentally during embryonic signals affecting the corpus luteum since these dif- seasonal quiescence in tammar wallabies with daily exogenous ferences are correlated with the rate of embryonic development progesterone injection, which also induces endometrial growth and with progesterone concentration. The results of further of both uteri for the duration of the treatment (Renfree and studies of these species will be awaited with interest. Tyndale-Biscoe, 1973). However, after the injections cease on day 10, only the uterus containing the developing embryo con- tinues to enlarge, while the non-gravid uterus reduces to a size Urogenital vasculature typical of the non-pregnant cycle. In these animals, the corpus The local effects of ovarian stimulation are possible because of luteum remains inactive, so the response of the gravid uterus the close association between the ovarian and uterine vascular after progesterone withdrawal must be due to the presence of supplies. The ovarian venous plexus is a fusion of many small the fetus or its placenta. The choriovitelline placenta, which veins draining the ovary, and the multiple uterine branches of is never invasive and only makes a chorio–epithelial interdigi- the ovarian artery almost completely surround the plexus. This tation with the uterine epithelium (Tyndale-Biscoe and Renfree, arrangement is similar in brushtail possums (Lee and O’Shea, 1987), appears to be responsible for this effect because some 1977) and tammar wallabies (Towers et al., 1986), and probably treated animals produced a vesicle that lacked any embryonic occurs in the potoroo (Shaw and Rose, 1979). There is no portal or vascular mesodermal tissue (Renfree and Tyndale-Biscoe, blood supply from the ovary to the uterus, but the proximity of 1973). These expanded vesicles, which consisted only of non- the branched uterine arterial supply to the ovarian drainage vascular yolk sac tissue (trophoblast plus endoderm), neverthe- provides an anatomical arrangement whereby hormones of less stimulated the endometrium and the uterine secretions as luteal or follicular origin can diffuse from the ovarian vein via in a normal pregnancy. These uterine responses on the gravid a countercurrent system into the arteries of the uterine branch side may be due to either uterine stretch, or to hormonal or

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(a) (b) (c)

V V V CL V

F

Fig. 1. Diagrammatic representation of the response of the endometrium in tammar wallabies to the presence of an embryo relative to the location of the corpus luteum (CL) and developing follicle (F) on the contralateral ovary. (a) Normal unilateral pregnancy ipsilateral to the corpus luteum. (b) Double pregnancy after blastocyst transfer. (c) Unilateral pregnancy ipsilateral to the follicle after blastocyst transfer. V: vesicle with developing embryo. (Data from Renfree, 1972; Renfree and Tyndale-Biscoe, 1973.)

cytokine stimulation by the placenta (Renfree, 1972; Young and non-gravid endometrium before birth, in response to the local Renfree, 1979; Shaw, 1983). effects of follicular oestradiol from the ipsilateral ovary (Fig. 3). Although hormone production by the marsupial placenta The receptor for the oxytocic peptide mesotocin is also up- has not been well studied, and the tammar placenta has only regulated preferentially in late pregnancy in the gravid myo- incipient steroid synthetic activity (Heap et al., 1980), it is known metrium and downregulated in the non-gravid myometrium to have considerable capacity to synthesize prostaglandins (Parry et al., 1997; Sebastian et al., 1998). The increase in meso- (Shaw et al., 1999). The tammar placenta also expresses the tocin receptors in the gravid but not in the non-gravid myo- peptide relaxin (Parry and Renfree, 1999). The fetal fluids are metrium indicates that, at the end of gestation, there may be a also rich in prostaglandins (Shaw et al., 1999) and cortisol paracrine control of mesotocin receptors by the feto–placental (Ingram et al., 1999), and the placenta maintains high concen- unit (Fig. 3). This suggestion is supported by the demonstration trations of these hormones against a concentration gradient, as that neither uterus of non-pregnant animals shows these in- it does with the wide variety of amino acids, proteins and creases in mesotocin receptor concentrations (Siebel, Bathgate carbohydrates secreted into the fetal fluids (Renfree, 1973b). and Parry, 1999), highlighting this specific maternal recognition Clearly, the marsupial placenta has considerable endocrine and of pregnancy. paracrine capacity, and probably autocrine activity, much of which is as yet undefined. Myometrial responses Myometrial activity is quiescent during pregnancy in tammar Uterine receptors wallabies and, as the gravid myometrium grows, the gravid The fact that the endometrium of the non-gravid uterus de- myometrium, unlike the non-gravid myometrium, becomes in- creases in mass and secretory activity during the second half creasingly sensitive to oxytocin and prostaglandin (Tyndale- of pregnancy or the oestrous cycle, even though peripheral Biscoe and Renfree, 1987). In , isotonic contractile progesterone concentrations are at their highest, indicates activity also changes through the oestrous cycle, and pregnancy that there is a decreasing sensitivity to progesterone. It was influences uterine contractility. Myometrial activity in vivo suggested that the local stimulation of the gravid uterus has been recorded in tammar wallabies by electrouteromyogra- reverses sensitivity to progesterone by stimulating increased phy (Young and Renfree, 1979; Shaw, 1983). Activity remains progesterone receptor synthesis, but recent evidence does not low and cyclic in pregnant uteri at all stages of gestation, and support this hypothesis. There are differences in progesterone sensitivity increases in the gravid uterus in late pregnancy, but receptor concentration between the gravid and non-gravid by day 1 after birth both uteri are inactive and refractory uteri of quokkas (Owen et al., 1982) and tammar wallabies (Shaw, 1983). Since these effects differ between gravid and ad- (M. B. Renfree and D. R. Blanden, unpublished). However, jacent non-gravid uteri, they reflect a local rather than systemic both progesterone and oestradiol receptor concentrations are influence. Prostaglandin F2α concentrations increase sharply at downregulated after day 10 in early pregnancy, concomitant parturition. Myometrial responsiveness to the PGF2α analogue with the increase in progesterone in the peripheral plasma. Cloprostenol increases markedly towards the end of gestation, Another unilateral effect occurs at term, in that there is an in- but the myometrium is also refractory after birth. There is an crease in oestrogen receptor concentration in the endometrium increase in uterine PGF2α, PGE2 and 6-keto-PGF1 concentrations of the non-gravid uterus and immediately after birth, indicating at term, but these concentrations decrease markedly by day 1 that oestrogen receptors are upregulated selectively in the after birth (Shaw et al., 1999).

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(a) (a) 20 600 15

) 10 400 Ð1

5 (mg) 200 (ng ml wet weight

2 Endometrial 1

Plasma progesterone 0 0 0 5 10 15 20 25 30 23 24 25 26 27 28 29 (b)

(b) ) 1200 60 Ð1 800 50

receptors 400 ) β Ð1 2 40 (fmol mg E

in endometrium 0 30 0 5 10 15 20 25 30 (pg ml 20 (c)

Plasma oestradiol 10

) 1200

0 Ð1 23 24 25 26 27 28 29 800 Days after RPY 400 receptors 4 (fmol mg P

in endometrium 0 0 5 10 15 20 25 30 Fig. 2. Peripheral plasma (a) progesterone and (b) oestradiol con- (d) centrations ( ) compared with local concentrations in the plasma 3 of the uterine branch of ovarian vein ( , corpus luteum side; , follicle side) in tammar wallabies between days 23 and 29 of pregnancy after removal of the sucking pouch young. Birth nor- 2 protein) mally occurs 26–27 days after removal of the pouch young (RPY). Ð1 (Data from Hinds and Tyndale-Biscoe, 1982; Harder et al., 1984; Shaw and Renfree, 1984; Towers et al., 1986.) 1 Myometrial MT receptors

(pmol mg 0 0 5 10 15 20 25 30 Days after RPY Effects of pregnancy on the duration of the oestrous cycle

The duration of reproductive cycles in macropodids is affected Fig. 3. Unilateral responses to pregnancy in gravid (solid line) by the presence of the embryo and by preceding lactation. The and non-gravid (dashed line) uteri throughout pregnancy (days duration of gestation in the Eastern and Western species of after removal of pouch young (RPY) = days of pregnancy), show- grey kangaroos is 36 and 31 days, respectively, but the ges- ing endometrial wet weight, endometrial progesterone (P4), and β tation of Eastern grey females mated to Western grey males is oestradiol (E2 ) receptor concentrations and myometrial mesotocin intermediate at 34 days (for review, see Tyndale-Biscoe and (MT) receptor concentrations. (Data derived from Renfree, 1972; Renfree, 1987), reflecting the hybrid genotype of the fetuses. Renfree and Tyndale-Biscoe, 1973; Tyndale-Biscoe and Renfree, The duration of the oestrous cycle of female progeny was inter- 1987; Parry et al., 1997; Sebastian et al., 1998; M. B. Renfree and mediate between the parent species. In the agile wallaby, the D. R. Blanden, unpublished.) interval from one oestrus to the next is shorter in pregnant females than in non-pregnant females (Merchant, 1976), a phenomenon that has been confirmed in tammar (Merchant, Behavioural recognition of pregnancy 1979) and Bennett’s wallabies (Merchant and Calaby, 1981). These results are unequivocal demonstrations of maternal rec- In most marsupials, it is essential that the mother recognizes ognition of pregnancy. It is clear that the feto–placental unit the impending birth, to ensure that the tiny, altricial neonate is of macropodid marsupials is influencing ovarian function by able to reach the pouch or mammary area to complete its de- systemic signals, a characteristic that marsupials had been velopment. Most species studied so far achieve this by adopt- thought to lack. ing a specific birth posture. In macropodids, the birth posture

Downloaded from Bioscientifica.com at 09/29/2021 04:39:57PM via free access 10 M. B. Renfree is characterized by the female sitting or resting against a tree Harder JD, Hinds LA, Horn CA and Tyndale-Biscoe CH (1984) Oestradiol or support with the tail passed forward between her legs. in follicular fluid and in utero–ovarian venous and peripheral plasma during parturition and post-partum oestrus in the tammar, Macropus The female licks her pouch and urogenital opening especially eugenii. Journal of Reproduction and Fertility 72 551–558 vigorously in the minute immediately preceding birth (Renfree Heap RB (1979) Introduction. In Maternal Recognition of Pregnancy Ciba et al., 1989). This behaviour is now known to be under the influ- Foundation Symposium 64 1–2 ence of prostaglandins (Shaw, 1990; Hinds et al., 1990), and even Heap RB, Renfree MB and Burton RD (1980) Steroid metabolism in vitro of males treated with the prostaglandin analogue Cloprostenol the yolk sac placenta and endometrium of the , Macropus eugenii. Journal of Endocrinology 87 339–349 will adopt the birth posture and lick their scrotum (Shaw, 1990). Hill JP and O’Donaghue CH (1913) The reproductive cycle in the marsupial Oxytocin, if given in pharmacological doses, can also induce Dasyurus viverrinus. Quarterly Journal of Microscopical Science 59 133–174 adoption of the birth position in the potoroo, bettong, bandi- Hinds LA and Tyndale-Biscoe CH (1982) Plasma progesterone levels in coot and the grey short-tailed opossum (Rose and McFadyen, the pregnant and non-pregnant tammar, Macropus eugenii. Journal of Endocrinology 93 99–107 1997; Rose and Fadem, 1999). Hinds LA, Tyndale-Biscoe CH, Shaw G, Fletcher TP and Renfree MB (1990) Effects of prostaglandin and prolactin on luteolysis and parturient behaviour in the non-pregnant tammar, Macropus eugenii. Journal of Conclusions Reproduction and Fertility 88 325–333 Numerous unilateral effects are imposed by the anatomy of the Ingram J, Shaw G and Renfree MB (1999) Cortisol in the fetal fluids of the tammar in the late gestation Biology of Reproduction 60 651–655 marsupial reproductive tract and, in monovular species, by Kojima T, Hinds LA, Muller WJ, O’Neill C and Tyndale-Biscoe CH (1993) the proximity of the corpus luteum of pregnancy or the de- Production and secretion of progesterone in vitro and presence of platelet veloping follicle. These effects can be over-ridden by paracrine activating factor (PAF) in early pregnancy of the marsupial, Macropus and endocrine signals from the feto–placental unit, and some of eugenii. Reproduction, Fertility and Development 5 15–25 Lee CS and O’Shea JD (1977) Observations on the vasculature of the repro- these responses may also be due to local physical reactions to ductive tract in some Australian marsupials Journal of Morphology 154 the presence of a developing fetus. The vascular anatomy of the 95–114 reproductive tract allows preferential unilateral delivery of *Merchant JC (1976) Breeding biology of the agile wallaby, Macropus agilis these signals regardless of their origin. However, the feto– (Gould) (Marsupialia: Macropodidae), in captivity Australian Wildlife placental unit in marsupials, as in all other mammals, can re- Research 3 93–103 Merchant JC (1979) The effect of pregnancy on the interval between one direct maternal physiology to ensure the success of pregnancy oestrus and the next in the tammar wallaby, Macropus eugenii. Journal of and parturition. Macropodid marsupials have a refined maternal Reproduction and Fertility 56 459–463 recognition of pregnancy, which is manifest by unilateral re- Merchant JC and Calaby JH (1981) Reproductive biology of the red-necked sponses within the female reproductive tract. wallaby (Macropus ruefogriseus banksianus) and Bennett’s wallaby (M. r. rufogriseus) in captivity Journal of Zoology London 194 203–217 Owen FJ, Cake MH and Bradshaw SD (1982) Characterization and proper- The author thanks R. V. Short and G. Shaw for helpful comments ties of a progesterone receptor in the uterus of the quokka (Setonix and discussion of the manuscript and L. J. Parry for permission to brachyurus) Journal of Endocrinology 93 17–24 quote her unpublished results. The author is also grateful to G. Shaw Parry LJ and Renfree MB (1999) Onset of relaxin gene expression in the for assistance with the diagrams. tammar wallaby placenta Biology of Reproduction Supplement 60 25 Parry LJ, Bathgate RAD, Shaw G, Renfree MB and Ivell R (1997) Differential regulation of uterine oxytocic receptors during pregnancy in References a marsupial Biology of Reproduction 56 200–207 *Renfree MB (1972) Influence of the embryo on the marsupial uterus Nature Key references are indicated by asterisks. 240 475–477 Cruz YP and Selwood L (1993) Uterine histology of the dasyurid marsupial, Renfree MB (1973a) Proteins in the uterine secretions of the marsupial Antechinus stuartii: relationship with differentiation of the embryo Journal Macropus eugenii. Developmental Biology 32 41–49 of Reproduction and Fertility 99 237–242 Renfree MB (1973b) The composition of fetal fluids of the marsupial Cruz YP and Selwood L (1997) Histological differences between gravid and Macropus eugenii. 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