Monotreme Reproductive Biology and Behavior

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Monotreme Reproductive Biology and Behavior


Monotremes are mammals that are oviparous, or egg-laying. There are only 3 extant species of monotremes: the playtpus and two species of echidna. Their reproductive systems are highly specialized to facilitate both the production of eggs and milk. The male tract is quite simple. The female tract has qualities similar to those of birds, though female echidnas also possess pouches. The monotreme egg is also very specialized and somewhat similar to a reptile egg. Platypuses and echidnas have very different behaviors when it comes to mating, but their genetics are quite similar. Monotremes possess a few large chromosomes and several unpaired microchromosomes. The descendants of the first radiation of mammals, monotremes have characteristics of both placentals and marsupials, while still retaining characteristics of reptiles and birds in a combination all their own.

Introduction

At first glance platypuses seem to be an amalgamation of mammals, birds, and everything in between. In fact, their reproduction biology also has much in common with a variety of animals—reptiles, birds, placentals and marsupial mammals. Platypuses belong to a group of animals called monotremes. These egg-laying mammals have been a mystery to researchers since their discovery by Westerners over 200 years ago. The first specimens of platypuses brought back to England were thought to be hoaxes similar to mermaids (Moyal, 2001). Found only in and around Australia, there are only three living species of monotremes: the platypus (Ornithorhynchus anatinus) and two species of echidnas (Tachyglossus aculeatus, and Zaglossus bruijni).

The word “monotreme” is Greek for “one-hole,” referring to the cloaca that is the exit for the urinary, reproductive, and excretory systems (Dawson, 1983). The creatures are oviparous--the females lay eggs that develop outside of her body. This paper will explain the background of the animals, the anatomy of the tract and egg, breeding behavior, and genetics behind this unique reproductive system. It will pay special attention to the similarities of the monotreme reproductive system to those of animals we are more familiar with.

Background

Monotremes are crepuscular animals only found in Australia and New Guinea.

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The platypus, or duck-bill, is an aquatic animal that feeds largely from fresh-water bottoms. It weighs up to 2.35 kg and may be up to 0.56 m long. Its external features include a duck-bill shaped snout, a flat and broad tail, and webbed limbs. This amphibious creature is rarely observed on land except when burrowing a nest. Burrell, as early at 1927, suggested the possibility of a ‘sixth sense’ in the platypus bill. In fact, platypuses do possess a system of electroreception, and echidnas may also possess a similar sense (Dawson, 1983).

The echidna or spiny anteater (Tachyglossus aculeatus) is a terrestrial animal, usually from 3 to 5 kg. It has a pointed snout, and a mouth containing no teeth. Its long, sticky tongue can extend 18 cm and is used to catch ants and termites, as well as masticate food.

The second echidna species, the long-beaked echidna (Zaglossus bruijni), is found mainly in the mountains of New Guinea. It is up to 1 m in length and is usually less than 10 kg. It also has long spines, but its downward curving snout contrasts it with T. aculeatus. The long-beaked echidna eats mainly earthworms, and it is considered a delicacy in New Guinea (Dawson, 1983).

Reproductive anatomy and physiology

The reproductive tracts of male echidnas and platypus are similar to those of placental mammals. One exception is that male monotremes have no scrotum; their testes are within the abdominal cavity near the kidneys. The tract leads from the testes to the epididymis to the vas deferens, which join the urethra just before the ureters. A pair of bulbouretheral glands and small prostate glands produce seminal fluid. The urethra ends in the penis, which is located in a prepupital sack in the urogenital sinus when not erect. The males possess a set a poison spurs on their back legs, which were once thought to hold the female during copulation, but this idea has been disproven since they would effectively kill the female (Dawson, 1983).

Female reproductive systems of platypus and echidnas are quite different from each other and placental mammals. They contain paired ovaries that resemble those of reptiles or birds. In the platypus, both ovaries are present, but only the left ovary is functional. This is similar to birds, whose right ovary and oviduct regress, while the left ovary is functional (Brant, 2003). Echidnas have two functional ovaries, but generally only one egg develops at a time. The reproductive infundibulum directs the egg to an oviduct. This is also the site of sperm storage and fertilization (Griffiths, 1968). The egg is transported through the oviduct to one of the paired uteri. The egg then enters the single urogenital sinus, then the cloaca, along with the urine and feces (Dawson, 1983). Unlike platypus, echidnas possess a separate pouch where they incubate their eggs and nurse their young. There are two areolae found on the anterior wall of the pouch. Its temperature can be 2 degrees higher than the mother’s core temperature (Griffiths, 1968).

Interestingly, in platypus “the existence of mammary glands was doubted for some 30 years after the animals were discovered” (Dawson, 1983). The mammary glands of monotremes are indeed quite simple. The duct system is similar to that of placental mammals, but the areolas, where the milk emerges, is hidden by fur and there are no teats. The glands regress in the non-breeding season (Dawson, 1983).

Hormones such as estrogens in females and androgens in males influence the reproductive systems of monotremes, like all mammals. The testes have a distinct seasonal variation which coincides with the reproductive cycle of the female (Dawson, 1983). Testis size begins to increase in May and testosterone concentrations peak in June/July, slightly before ovulation in females. The hormone progesterone controls the female’s ovulation. In wild platypus, progesterone concentrations remain low until late July and begin to increase in August--inducing ovulation. This also corresponds to the maximum weights of ovarian and uterine tissue. Levels remain elevated through September and are back to normal by November, with most egg-laying in October (Handasyde, McDonald, Evans, 1992). Other female hormones include prolactin which stimulates milk production. Oxytocin in placental females functions in milk letdown, and in reptiles it has an antidiuretic function. Predictably, the oxytocin secreted from the monotreme pituitary gland is similar to that secreted by placental mammals (Griffiths, 1968).

Development of the egg and embryo

The small, leathery monotreme eggs have some characteristics similar to those of reptiles or birds and others that are completely unique. The development of the follicles containing oocytes (i.e. ova or eggs) is broken into 3 stages. In the first stage, the oocytes are c. 0.01 mm in diameter and contain a nucleus with several nucleoli. They are found in the ovarian cortex. The outer covering, the zona pellucida, consists of a single layer of cubiodal cells. This surrounds a thin striate layer which surrounds the egg membrane.

At the second stage of oogenesis, egg size is about 0.4 mm in diameter and the zona pellucida has greatly increased in thickness. Fat droplets are beginning to form, which will be used in yolk primordia growth. The third stage includes development until the full-grown oocyte size of 3.9 mm. In this stage, the latebra is a thin stalk that connects the yolk center to the germinal disk (location of the nucleus on the yolk where the embryo will develop) and has much in common with that of reptiles. The zona pellucida and egg membrane are now very thin, but the egg is surrounded by an epithelium two cells deep. Complete maturation of the ovum involves the formation of a maturation spindle at the germinal disk and the first cellular division, resulting in polar bodies. The mature monotreme follicle is more similar to mammals than reptiles in that it secretes follicular fluid (Griffiths, 1968).

When the egg leaves the ovary, it is 10 times smaller than a hen’s egg at this stage, but 25 times the size of a placental egg. At this point the egg contains a yolk enclosed by two primary membranes, along with the embryo. Secondary membranes arise from the ovarian follicle cells and tertiary membranes are added in the oviduct and uterus. The majority of the nutrients in the egg come from the oviduct. The egg continues to grow in size in the uterus due to a unique eggshell which allows for expansion. The final shell layer is added once the egg has reached about 15 x 17mm in size. The egg spends about 28 days in the uterus, and only 10 days in external incubation (Dawson, 1983). In contrast, a chicken egg spends about 1 day in the tract and 21 days in external incubation (Brant, 2003).

This incubation period is also divided into 3 distinct phases. In the first stage, the embryo has no functional organs and the yolk sac aids respiration. The digits appear in the middle phase. In the terminal phase, the embryo reaches c. 9mm in length and an egg tooth appears (Manger, Hall, Pettigrew, 2004).

Breeding Behavior

Studies have shown that social breeding behavior in platypus is quite complicated, perhaps explaining why there have only been two recorded platypus births in captivity. In the wild, Grant and Griffiths (1992) found that females do not breed their first year, but can breed as early as their second year of life. Some females do not breed in consecutive years. The study suggests that mainly the resident established females in an area do most of the breeding. Pre-mating behavior generally includes increased bodily contact, following and circling, and the male biting the female’s tail. Mating in platypuses involves the male approaching the female from behind and curling his tail beneath her with his chest resting on her back (Holland and Jackson, 2002).

Twenty-eight days after mating, platypuses first dig burrows in which to lay their eggs. The platypus lays between 1 and 3 eggs, usually 2, while on her back. “A sticky mucoid substance covers the eggs so that they adhere together and to the underfur of the abdomen”. The platypus does not have a pouch and the eggs are held between the tail and the abdomen for 10 days. The female normally eats almost half of its body weight in food every night, but for brief periods of time while she lays and incubates her eggs, the platypus does not leave its nest. It is thought that the female lives off fat deposits in its tail during this time. After several days, the female begins to eat 90-100% of its weight in food daily and this continues throughout the lactation period (Manger, Hall, Pettigrew, 2004). Platypuses are suckled for 3 to 4 months after hatching or until they are about 30 cm long (Dawson, 1983).

In the wild, the echidna breeding season lasts 2-3 months in the early spring. With their long and numerous spines, they mate very carefully “venter to venter with head to head or with heads pointing in opposite directions and only the cloacal apertures in contact” (Griffiths, 1968).

Gestation time is about 23 days (Holland and Jackson, 2002). A single egg is deposited in the pouch, where it is loosely held and incubated for 10 days. It has been found that the cloaca can be everted up to 1.25cm, suggesting that if the female echidna is allowed to curl up, she can directly deposit the egg in the posterior end of the pouch. After hatching, the young hold onto numerous hairs on the pouch interior (Griffiths, 1968). They suck from the areolae in the pouch but are not fixed to them as in marsupials (Manger, Hall, Pettigrew, 2004). Echidnas carry their young in this way for about 55 days, or until spines develop, and suckle them until about 7 months of age (Dawson, 1983).

Genetics and Evolution

Platypus and echidnas are in the Class Mammalia and the subclass Monotremata. They are thought to have diverged from other mammals some 180 mya. Biochemical evidence does not support a closer relationship of monotremes to either marsupials or placentals (Dawson, 1983). They are closely related to “prototherians” from the first radiation of mammals.

Monotremes have a unique chromosomal setup. They have a genome size similar to placentals—about 3 billion base pairs and 70,000 genes, but have relatively large and few chromosomes (Marshall-Graves, 1996). All 3 species have 6 large pairs of autosomes; however, echidna gender is determined by a multiple sex chromosome system: X1X1X2X2 for female and X1X2Y for male. Platypus have a XX/XY system similar to humans and other mammals. The monotreme Y chromosome is quite large and shares a region of homology with the X chromosome, unlike placental sex chromosomes (Watson and Marshall-Graves, 1992). Another oddity is the existence of several unpaired “microchromosomes” that form a chain during meiosis—typical of plants but unheard of in other mammals. While the genome of monotremes is unique, it is also highly conserved. Platypus and echidna diverged about 70 mya, but have almost identical karyotypes (Marshall-Graves, 1996).

Monotremes have been around longer than all other extant mammals, and the adaptive advantage of reproductive system is beginning to be understood. For example, the “low body temperatures of about 32 degrees C, may mitigate against a selective pressure for the evolution of the scrotum” which keeps other mammals’ testes at a reduced temperature and may allow the female to store sperm for an extended amount of time (Dawson, 1983).

Conclusion

The monotreme has a unique reproductive system among mammals. The male reproductive tract is similar to that of placentals, while the female tract is more similar to those of birds and reptiles. All three species lay eggs, while the echidna possesses a pouch in which to incubate and nurse its young. Monotreme mating rituals can be complicated or even dangerous. The genetics behind monotreme chromosomes and evolution also differs greatly from most other mammals. A study of their reproductive systems give insight into how these creatures are much like other animals and how in some ways monotremes will always exist in a category all to themselves.

Literature Cited

Brant, George. 2003. AnS 214 lab manual. Welch Ave. Trading Post and Copyworks.

Dawson, Terence J. 1983. Monotremes and Marsupials: the Other Mammals. Southampton (GB): The Camelot Press Ltd.

Grant, T.R. and Griffiths, M. 1992. Aspects of lactation and determination of sex ratios and longetivity in a free-ranging population of platypuses (Ornithorhynchus anatinus) in the Shoalhaven River, NSW. Platypus and Echidnas. M. L. Augee, ed. Sydney: The Royal Zoological Society of NSW.

Griffiths, Mervyn. 1968. Echidnas. Oxford: Pergamon Press Ltd.

Handasyde, K.A., McDonald, I.R, and Evans, B.K. 1992. Seasonal changes in plasma concentrations of progesterone in free-ranging platypus (Ornithorhynchus anatinus). Platypus and Echidnas. M. L. Augee, ed. Sydney: The Royal Zoological Society of NSW.

Holland, Norm and Jackson, Stephen M. 2002. Reproductive behaviour and food consumption associated with the captive breeding of platypus (Ornithorhynchus anatinus). Journal of Zoology 256: 279-288. London: The Zoological Society of London.

Manger, Paul R., Hall, Leslie S., and Pettigrew, John D. 2004. Development of the external features of the platypus (Ornithorhynchus anatinus). Philosophical Transactions: Biological Sciences 353: 1115-1125. The Royal Society.

Marshall-Graves, Jennifer A. 1996. Mammals that break the rules: genetics of marsupials and monotremes. Annual Review of Genetics 30: 233-228.

Moyal, Ann. 2001. Platypus. Washington, D.C.: Smithsonian Institution Press.

Watson, Jaclyn M. and Marshall-Graves, Jennifer A. 1992. Clues about the Evolution of Mammalian Sex Chromosomes from Monotreme Gene Mapping. Platypus and Echidnas. M. L. Augee, ed. Sydney: The Royal Zoological Society of NSW.


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