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The marsupial pouch: implications for reproductive success
and mammalian evolution
Melanie J. Edwards
A
and Janine E. Deakin
A,B
A
Division of Evolution, Ecology and Genetics, Research School of Biology, The Australian National University,
Canberra, ACT 0200, Australia.
B
Corresponding author. Email: janine.deakin@anu.edu.au
Abstract. Extant mammals are divided into sub- and infraclasses that are distinguished by their mode of reproduction.
The monotremes lay eggs, the marsupials give birth to altricial young that typically develop in a pouch, and the eutherians
have prolonged in utero development, resulting in well developed young at birth. The three groups exhibit what appears to be
a nice progression of evolution towards the well developed newborn young of eutherian mammals. However, marsupials do
not represent a step in the progression of producing well developed young, but maintain a reproductive strategy that has
evolved to prosper in their specific niche. The production of undeveloped young with increased development in the pouch
(or counterpart) provides specific advantages to those species living in diverse environments. The evolution of this
reproductive strategy provides a clever solution to the uncertain and often adverse conditions encountered by many species,
and the survival of the developing young in a pouch containing potentially harmful microorganisms is truly remarkable.
In this review, we explore the unique features of the pouch, highlight the research questions that remain unanswered
regarding this unique marsupial attribute and discuss the advantages of the marsupial reproductive strategy and the potential
role of the pouch in mammalian diversification.
Received 3 September 2012, accepted 18 October 2012, published online 7 November 2012
Introduction
Many characteristics of reproduction are shared amongst the
vertebrates. However, there are also a countless number of
differences, demonstrating that different solutions have evolved
independently to solve the various problems of reproduction
(Lombardi 1998). The vertebrates not only display oviparous,
viviparous and ovoviviparous reproductive strategies, but
also exhibit extremely diverse developmental stages at birth,
including the production of precocial, altricial and highly
altricial offspring. The former two terms describe ‘well
developed’, or sighted, covered young and ‘undeveloped’,or
blind, naked young, respectively, while the latter term describes
the most extreme form of altriciality. Furthermore, each strategy
is not necessarily limited to a lineage, but is established in many
lineages throughout the subphylum. For example, the snakes
(suborder: Serpentes) include lineages of species that reproduce
by the various ‘viparous’or embryonic developmental strategies
(Pope 1956) and the birds (class: Aves), although all oviparous,
produce offspring that display a spectrum of altricial and precocial
developmental stages (Starck and Ricklefs 1998).
Not surprisingly, there are similar variances in the
reproductive strategies of mammals. All animals that produce
milk to meet the nutritional requirements of their young are
grouped into the class Mammalia and it is thought that lactation
provides a specific advantage to mammals, enabling them to
support the nutritional requirements of the young in any
environment where adults are able to survive (Pond 1984). The
extant mammals are divided into three major lineages that are
distinguished by their modes of reproduction. The monotremes
(or Prototheria –meaning ‘first beasts’) display a mixture of
reptilian and mammalian features, as they lay eggs yet feed
their young milk produced by mammary glands. Monotreme
hatchlings are highly altricial. In contrast, ‘placental’mammals
(or Eutheria –meaning ‘true beasts’) produce developed young
after a relatively long gestation time in which the developing
foetus relies on a placenta for the exchange of factors between
mother and foetus that are critical for survival, such as nutrients,
gases and immune compounds. The eutherian mammals produce
offspring varying from altricial to precocial; for example, even
within the Leporidae, there are altricial rabbits and precocial
hares (Trevathan 1987). The marsupials (or Metatheria –meaning
‘behind true beasts’) do not lay eggs but, like the monotremes,
they produce highly altricial young that complete most of their
development during a complex lactation phase rather than
throughout gestation. Marsupials are born at a stage of
development comparable to an 8–10-week-old human embryo
or an 11–12-day-old mouse embryo (Block 1960; Smith 2001).
Hence, much of the development that occurs in a mostly
Journal compilation CSIRO 2013 www.publish.csiro.au/journals/ajz
CSIRO PUBLISHING
Australian Journal of Zoology, 2013, 61,41–47 Review
http://dx.doi.org/10.1071/ZO12088
pathogen-free environment in eutherian mammals takes place
ex utero in marsupials and typically while the young are
permanently attached to a teat within a pouch.
The unfortunate naming of these three groups of mammals –
Prototheria, Metatheria and Eutheria –may suggest that
monotremes and marsupials are evolutionary steps in the
progression to eutherians, but a closer examination of the unique
reproductive strategies adopted by each lineage shows that
their modes of reproduction simply provide alternative solutions
that have adapted under different conditions. The survival of
the highly altricial young of marsupials is truly remarkable.
Des Cooper demonstrated an interest in the uniqueness of the
marsupial reproductive strategy, and was particularly interested
in the survival of the altricial young in the pouch and even in
the development of the pouch itself. Without Des Cooper’s
contribution, we would know little about the marsupial pouch, as
the pouch has been largely overshadowed by another marsupial
reproductive trait –the production of highly altricial pouch
young. In this review we link highly altricial young to the
pouch and make a case for the pouch in the role of marsupial
reproductive success and mammalian evolution.
Highly altricial young
In comparison to the broad altricial to precocial spectrum
observed amongst different eutherian mammals at birth,
marsupials are born at a similar developmental stage, which
marks the minimum onset of functionality for specific tissues
(Hughes and Hall 1988). This stage of development can be
visually compared with the developmental stage of a bird embryo,
well before hatching, or to a eutherian mammal embryo in utero.
Particularly, the most visually noticeable characteristics are the
forelimbs, which the young uses to take hold of the mother’s fur
to propel itself from the mother’s urogenital opening to a teat.
The mouth parts are also well developed and have a very
important role in fastening onto the mother’s teat so the young can
remain attached to the mother and attain colostrum and milk.
Remarkably, the undeveloped characteristics of marsupials
outweigh the comparatively developed characteristics several-
fold at birth, with the undeveloped characteristics considered
unnecessary for survival at this time of development.
Not only is the marsupial young visually undeveloped, but
many general physiological processes essential for adult survival
also remain immature until sometime after parturition. For
example, the lungs are partly developed with partial gas exchange
occurring through the skin. The degree of development differs
between species; Julia Creek dunnarts (Sminthopsis douglasi),
under approximately seven days, exhibit gas exchange through
the skin which exceeds that through the lungs (Mortola et al.
1999), while the integument of the tammar wallaby (Macropus
eugenii) is responsible for ~33% of gas exchange at birth,
decreasing to 14% at six days post partum (MacFarlane et al.
2002).
Marsupial neonates are also ectothermic and exhibit a large
surface area to weight ratio, which can cause rapid heat loss.
However, the rate of heat loss reduces as the young develops.
When the thermogenic response is initiated, the response is
small and it is not until they are covered in body hair that the
development of thermogenesis is complete (Hulbert 1988).
Additionally, young are born with undeveloped immune tissue
(Deane and Cooper 1988). For example, tammar wallaby young
are not able to mount an adaptive immune response until 35 days
post partum (Old and Deane 2003) and the maturation of their
lymphoid tissue is determined to occur at ~90 days post partum
(Basden et al.1997).
The survival of highly altricial young appears to be a
phenomenon when compared with the reduced survival rates of
human neonates that are born prematurely. However, marsupials
have evolved to produce young at a highly altricial developmental
stage and exhibit specific traits that undoubtedly aid in the rearing
of such undeveloped young. In particular, the pouch resolves
many of the problems encountered by the production of highly
altricial newborn young.
The pouch
Pouches are located ventrally but vary markedly between
marsupial species; they can be shallow or deep and contain
varying numbers of teats between species (Tyndale-Biscoe
2005). Russell (1982b) described six different pouch types.
Figure 1shows a phylogeny of the pouch and the pouch
counterpart types for the major orders and suborders of
marsupials. In Type 1 the mammary area is not covered, but folds
of skin can develop in the breeding season; in Type 2 the
mammary area is partially covered; in Type 3 the mammary area is
covered and the teats are displayed in a circular arrangement with
the pouch opening in the centre; in Type 4 the mammary area is
covered and the teats are located in two pockets; in Type 5 the
mammary area is covered and the pouch opens to the anterior;
and in Type 6 the mammary area is covered and the pouch opens
Australidelphia
Dasyuromoprhia
Peramelemorphia
Notocyctemorphia
Paucituberculata
Didelphimorphia
Ameridelphia
Macropodiformes
Phalangeridae
Petauroidae
Diprotodontia
Vombatiformes
4
5
4
6
1
6
1
15
6
234
5
5
Fig. 1. A phylogeny showing different pouch types and pouch counterparts.
Dark and light circles represent teats that are located exteriorly and interiorly,
respectively. Solid and dotted lines represent the pouch opening and covered
areas, respectively. Pouch types and diagrams are reported from Russell
(1982b) and Tyndale-Biscoe and Renfree (1987).
42 Australian Journal of Zoology M. J. Edwards and J. E. Deakin
to the posterior. Figure 2shows external and internal images of
a tammar wallaby pouch (Type 5), with and without a pouch
young and with different degrees of pouch cleanliness (also
known as ‘pouch grot’), as described by Sharman and Calaby
(1964) as brown to black scale for a ‘dirty’pouch or clean and
pinkish for a ‘clean’pouch.
Russell (1982b) also identified three different patterns of
parental care that are associated with different pouch types.
Pattern A describes species with small pouches and large litters,
whereby the mother leaves the young at an early developmental
stage (with little fur, their eyes closed and no thermoregulation) in
a nest after a period of teat attachment. Pattern B describes species
with well developed pouches and fewer young, whereby the
young remain in the pouch and are then left in a nest at a later
developmental stage (when they are well furred, their eyes are
open and they can thermoregulate). Pattern C describes species
with large pouches and typically only one young, whereby the
young remain in the pouch, as in Pattern B, and then leave the
pouch but continue to follow the mother at foot. Gemmell et al.
(2002) describes different methods, correlating to different pouch
types, for newborn young to travel from the urogenital opening
to the pouch; young may either climb upward to the pouch (e.g.
the forward-facing pouch (Type 5) of the brushtail possum
(Trichosurus vulpecula)) or the mother may place her urogenital
opening above the pouch so the newborn can move down to the
pouch (e.g. the backward-facing pouch (Type 6) of the bandicoot
(Isoodon macrourus)).
Remarkably, there are still so many questions about the
pouch that remain unanswered. Foremost of these is the trigger
for pouch development. The pouch is not under hormonal control,
but is thought to be under the control of a locus on the X
chromosome, along with the scrotum and mammary glands
(Shaw et al.1989; Watson and Cooper 1995; Watson et al.1997).
The role of chemical protection in the pouch is also relatively
unknown, although four genes for the antimicrobial peptide
cathelicidin are expressed in tammar wallaby pouch skin (Wang
et al.2011). A haematoxylin and eosin stain of the pouch skin
taken from within the tammar wallaby pouch also shows a very
large active apocrine gland (Fig. 3); these are usually found in the
axillary and genital areas (Morimoto and Saga 1995). Large sweat
glands have also been identified in the red kangaroo (Macropus
rufus) and brushtail possum pouches, suggesting that there may
be active secretions into the pouch (Kubota et al.1989; Old et al.
2005). Further work, possibly linking the glands to antimicrobial
or mucosal activity needs to be completed (Edwards et al.2011).
Although the pouch or marsupium gives the marsupials their
name, not all marsupials have pouches. Instead, the position of
their reproductive and excretory organs distinguishes them from
the monotremes and the eutherians (Cooper and Hope 1989;
Tyndale-Biscoe 2005). Species without a pouch instead form a
tissue between the teat and the young so the young stay attached
and do not become separated from the mother. To support the
young the ilio marsupialis muscle passes through the mammary
gland and up each teat (Griffiths and Slater 1988). It is surprising
that a pouch is not associated with all marsupials as many
challenges that are presented by producing highly altricial young
appear to be overcome by the pouch. As a pouch is not necessary
for the production of highly altricial young, below we examine the
role of the pouch in reproduction and ultimately in mammalian
evolution.
Implications of the pouch for reproductive success
and mammalian evolution
The production of highly altricial young, and not the pouch, is
usually the focus of discussion for marsupial reproduction. In the
(a)(c)
(b)(d)
Fig. 2. An external view of a closed tammar wallaby (Macropus eugenii) pouch (a), a pouch
young inside the pouch (b), and two images of an internal view of a tammar wallaby
pouch without a pouch young (cand d). An elongated teat is evident in (c) and (d) and one pouch
displays a large amount of ‘pouch grot’(c).
The marsupial pouch Australian Journal of Zoology 43
past, the notion that eutherian reproduction has a fundamental
evolutionary advantage over marsupial reproduction was
explored (Müller from Lillegraven 1975); however, Kirsch
(1977a) highlighted that we should not be asking why marsupials
lack a complex gestation, but asking whether a long gestation is
necessary? Kirsch (1977a,1977b), Parker (1977) and Low (1978)
discussed that the difference between the reproductive strategies
of marsupials and eutherians amounted from different selective
environments. The support for the production of highly altricial
young included that marsupials could terminate their investment
in reproduction in response to unfavourable conditions (such as
irregular drought episodes: Kirsch 1977a,1977b; Parker 1977;
Low 1978). Specifically, advantages were identified in terms of
reproductive value and effort, and for marsupials these included:
rapid birth (which reduced vigilance time), low cost associated
with the foetus in terms of risk and energy (such as reduced
vulnerability to predation and increased ability to forage), ability
to resorb reproductive material, and low cost of the uterus when
compared with finding or building a nest (Kirsch 1977a,1977b;
Parker 1977; Low 1978). However, Russell (1982b,1982a), Lee
and Cockburn (1985) and Cockburn (1989) examined the
marsupial strategy further using additional examples of marsupial
species and provided a comprehensive discussion that pointed to
discrepancies in the ‘unfavourable conditions’hypothesis.
Hopson (1973) proposed that the fundamental components
of mammalian reproduction are selection for endothermy and
small body size. As metabolic rate increases as body size
decreases (creating an energetic dilemma), Hopson (1973)
suggested that there is selection for the production of ectothermic
young with low metabolic rate and increased parental care,
including adaptations for creating warmth. Case (1978) presented
a slightly different hypothesis to Hopson, and proposed that
smaller young have a lower energetic requirement than larger
young. Thus, parental costs are greater after birth and can
be shared between parents, particularly when brooding and
foraging cannot co-occur. Furthermore, the mammary gland and
attachment to the teat increased maternal care and reduced
the need for paternal care. Case (1978) also suggested that
reproductive characteristics are shaped by aspects of a species’
niche and habitat. For example, it may be beneficial for those
species that spend a large amount of time and energy searching for
food to produce small embryos as larger embryos may hinder their
ability to forage.
Mostly, the pouch is disregarded in discussions on the
marsupial reproduction strategy, although Hopson (1973) stated
that pouches helped with trends to produce altricial young. It is
likely that researchers question the role that the pouch has in the
discussion of marsupial reproduction, as some marsupial species
lack a pouch. However, when present, the pouch plays a major
role in reproduction, thus it is necessary to examine the pouch
explicitly.
The pouch has more than one role in the reproduction of
many marsupial species and the large variation of pouches seen
within the marsupials is likely to correspond to the varying levels
of importance of the role of the pouch. First, direct physical
protection from the external environment is provided by the
pouch (Russell 1982b). In birds and monotremes, physical
protection comes from the egg, while protection for eutherian
mammals, at a comparable developmental stage, comes from the
uterus and integument of the mother. The pouch may also provide
protection on a chemical level, as pouch washes (obtained by
flushing pouches with sterile water) contain proteins with
antimicrobial activity and display antimicrobial activity when
they are subjected to bacteria (Bobek and Deane 2001;
Ambatipudi et al.2007,2008; Edwards et al.2012). Second, the
pouch may influence the humidity of the direct environment of
the young (Kubota et al.1989), which may aid in integumental
gas exchange. Chemical protection and humidity control could
come from secretions within the pouch (Kubota et al.1989),
or from the mother licking the pouch and depositing saliva
(Charlick et al.1981). Third, as the pouch is associated with the
mother, direct contact between the mother and young allows the
young to develop at a constant temperature that is comparable to
that of the adult, thus resolving the issues of ectothermy in the
developing young (Hulbert 1988). The ability to open and close
the pouch may also provide an air-conditioning effect (Kubota
et al.1989). If a pouch provides a constant environment specific
to the requirements of the young for protection, humidity, and
warmth, it may have an increased chance of surviving and
reproducing. For example, if the mother moves into or even
through an environment in which conditions are unfavourable to
the young, the pouch will keep the direct environment of the
young constant.
Fourth, the pouch may make young inconspicuous to
predators so that mothers may not be targeted while foraging,
and, finally, the pouch evolved in unison with mammary glands.
Although the pouch is always associated with mammary glands,
the mammary glands are not always associated with a pouch
(Shaw et al.1989). Mammary glands provide the young with
100 µm
Lumen
MC
SC
Fig. 3. An 8-mm section of a pouch skin biopsy stained with haematoxylin
and eosin, taken from within the tammar wallaby (Macropus eugenii) pouch
with a 2–3-day-old pouch young. An apocrine gland is evident with an
extremely large lumen surrounded by secretory cells (SC) and myoepithelial
cells (MC).
44 Australian Journal of Zoology M. J. Edwards and J. E. Deakin
essential nutrients and also pass on immune compounds to the
developing animal (Deane et al.1990; Young et al.1997). In
contrast to eutherian mammals, the supply of marsupial milk is
multifaceted, as milk production occurs over three or four phases,
which are associated with major periods of growth (Nicholas
1988; Joss et al.2009).
It is clear that the pouch supports the undeveloped marsupial;
however, the pouch also presents potential challenges. For
example, the young must travel from the urogenital opening to the
pouch before latching onto a teat. Additionally, the pouch is a non-
sterile environment containing a range of bacteria that have the
potential to harm the young (Yadav et al.1972; Charlick et al.
1981; Old and Deane 1998; Deakin and Cooper 2004; Chhour
et al.2010).
The pouch not only provides insight into marsupial
reproduction but may also shed light on mammalian
diversification and evolution. Currently, the mammalian lineages
are dominated by eutherian mammals, even though marsupials
have been evolving for the same period (Bininda-Emonds et al.
2007). Müller (from Lillegraven 1975), Cooper and Steppan
(2010), and Kelly and Sears (2011) suggested that the
reproductive strategy of marsupials has contributed to limiting
the marsupial’s evolutionary potential when compared with
eutherian mammals. The limitation comes from the need for
developed forelimbs to travel from the urogenital opening to
the teat, which may pose a functional constraint on the forelimb,
limiting its morphological evolution. In other words, the
marsupials must retain their forelimbs and cannot evolve wings,
flippers or hooves, which have evolved in the eutherian clade.
Kirsch (1977b) found the hypothesis unconvincing as claws in
some marsupial species are deciduous.
Whether or not the forelimb of the marsupial has limited the
evolutionary potential of the marsupials, we suggest that the
pouch has positively influenced the range of extant marsupial
species. The pouch provides a practical explanation that supports
the movement of marsupials into niches that are not supported
by free-hanging highly altricial young. For example, the water
opossum (Chironectes minimus) has a strongly developed pouch
muscle, the pars pudenda, which allows the pouch to close
effectively enough to help protect the young from water (Enders
1937). The marsupial mole (Notoryctes typhlops) and other
burrowing species have posterior-opening pouches that protect
the young from sand and soil entering the pouch while they are
burrowing (Johnson 1995). It is also likely that the pouch provides
increased protection in jumping and gliding species (genus:
Macropus and Petaurus) when the mother lands on successive
trees or hops though scrubland, as it is difficult to see how free-
hanging altricial young would survive in these types of situations.
The pouch, as a reproductive feature, fits Case’s(1978)
hypothesis, as it may be shaped by attributes of niche and habitat.
Although we only provide examples of how a pouch might
promote reproductive success in clearly different environments, it
is likely that the presence or type of pouch is also going to be
influenced by specific ecological traits such as mode of foraging
or predator avoidance. Researchers are frequently fixed on
explaining why there are not as many marsupials as there are
eutherian mammals; perhaps turning the question around to ask
why are there as many marsupials as there are, is just as interesting
in evolutionary terms.
Conclusion
The marsupials, often referred to as Metatheria (or halfway
mammals), have sometimes been thought of as being an
intermediate group between the egg-laying monotremes, often
referred to as Prototheria (or first mammals), and the
comparatively more highly developed eutherians (or true
mammals). However, it is important to remember that marsupials
do not represent a step in the evolution of producing well
developed young, but maintain an alternative mode of
reproduction compared with the eutherian strategy that has
evolved to prosper in their specific niche (Graves et al.1989).
Much emphasis has been placed on the production of highly
altricial young in the marsupial reproduction strategy, while the
pouch is often disregarded. However, the pouch plays an
extremely important role in the reproductive success of those
species that have them. Additionally, the pouch may have played
an important role in the diversification and evolution of mammals
by supporting the movement of marsupials into niches that are not
supported by free-hanging highly altricial young.
Many of the examples presented in this review came from Des
Cooper’s research; we are indebted to him for his contribution to
marsupial biology.
Acknowledgements
JED is supported by an Australian Research Council Future Fellowship.
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