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The marsupial pouch: implications for reproductive success and mammalian evolution

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Australian Journal of Zoology
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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.
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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 specic niche. The production of undeveloped young with increased development in the pouch
(or counterpart) provides specic 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 diversication.
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 viparousor 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 specic 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 rst 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, placentalmammals
(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 810-week-old human embryo
or an 1112-day-old mouse embryo (Block 1960; Smith 2001).
Hence, much of the development that occurs in a mostly
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Australian Journal of Zoology, 2013, 61,4147 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 Coopers
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 specic 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 mothers fur
to propel itself from the mothers urogenital opening to a teat.
The mouth parts are also well developed and have a very
important role in fastening onto the mothers 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 specic 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 dirtypouch or clean and
pinkish for a cleanpouch.
Russell (1982b) also identied 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 identied 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 (Grifths 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). Specically, advantages were identied 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 nding 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 conditionshypothesis.
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 benecial 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
ushing 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 inuence 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 specic
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, nally, 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 23-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
diversication 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 marsupials 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,
ippers 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 inuenced 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 difcult to see how free-
hanging altricial young would survive in these types of situations.
The pouch, as a reproductive feature, ts Cases(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
inuenced by specic ecological traits such as mode of foraging
or predator avoidance. Researchers are frequently xed 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 rst 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 specic 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 diversication 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
Coopers 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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Handling Editor: Katherine Belov
The marsupial pouch Australian Journal of Zoology 47
www.publish.csiro.au/journals/ajz
... They grab their mother's fur to propel themselves from the cloaca towards a teat, and once they found it, they seal their mouth around it and remain strictly attached to it for the next few weeks (Russel 1982). Lungs are partially developed at birth, with a variable degree of development between species, which are complemented with partial gas exchange through the thin and moist skin (Russell 1982, Edwards & Deakin 2013. ...
... The morphology of the pouch of marsupials varies widely between taxa, notwithstanding, it offers the perfect moist environment for the developing young and it also provides physical and antimicrobial protection (Edwards & Deakin 2013). Not all species have an enclosed pouch with a forward-facing opening like a kangaroo. ...
... The mother has to select a 'safe' place to leave her litter away from predators and in insulated nest to minimise heat loss as young at this stage of development are highly ectothermic (Geiser 2003, Edwards & Deakin 2013. Tree cavities, hollow logs, burrows, soil crevices, tussock grass and other protected areas such as artificial nest boxes and human buildings can be used to build up a nest. ...
... Like other marsupials, koalas give birth after a short gestation period of 34-36 days to immunologically naïve, physiologically undeveloped young, which continue their development ex utero in the marsupium (herein pouch), sustained via lactation [10,14]. The maternal pouch is the primary site of immunological and physical development for marsupials, providing a humid, thermostable environment as well as protection from predation during lactation [14,15]. ...
... Like other marsupials, koalas give birth after a short gestation period of 34-36 days to immunologically naïve, physiologically undeveloped young, which continue their development ex utero in the marsupium (herein pouch), sustained via lactation [10,14]. The maternal pouch is the primary site of immunological and physical development for marsupials, providing a humid, thermostable environment as well as protection from predation during lactation [14,15]. However, the pouch is not sterile and has been demonstrated to harbour diverse communities of microorganisms including several pathogens, which may pose a risk to developing young [15][16][17][18][19][20]. ...
Article
Full-text available
Background: Captive koala breeding programmes are essential for long-term species management. However, breeding efficacy is frequently impacted by high neonatal mortality rates in otherwise healthy females. Loss of pouch young typically occurs during early lactation without prior complications during parturition and is often attributed to bacterial infection. While these infections are thought to originate from the maternal pouch, little is known about the microbial composition of koala pouches. As such, we characterised the koala pouch microbiome across the reproductive cycle and identified bacteria associated with mortality in a cohort of 39 captive animals housed at two facilities. Results: Using 16S rRNA gene amplicon sequencing, we observed significant changes in pouch bacterial composition and diversity between reproductive time points, with the lowest diversity observed following parturition (Shannon entropy - 2.46). Of the 39 koalas initially sampled, 17 were successfully bred, after which seven animals lost pouch young (overall mortality rate - 41.18%). Compared to successful breeder pouches, which were largely dominated by Muribaculaceae (phylum - Bacteroidetes), unsuccessful breeder pouches exhibited persistent Enterobacteriaceae (phylum - Proteobacteria) dominance from early lactation until mortality occurred. We identified two species, Pluralibacter gergoviae and Klebsiella pneumoniae, which were associated with poor reproductive outcomes. In vitro antibiotic susceptibility testing identified resistance in both isolates to several antibiotics commonly used in koalas, with the former being multidrug resistant. Conclusions: This study represents the first cultivation-independent characterisation of the koala pouch microbiota, and the first such investigation in marsupials associated with reproductive outcomes. Overall, our findings provide evidence that overgrowth of pathogenic organisms in the pouch during early development is associated with neonatal mortality in captive koalas. Our identification of previously unreported, multidrug resistant P. gergoviae strains linked to mortality also underscores the need for improved screening and monitoring procedures aimed at minimising neonatal mortality in future. Video Abstract.
... The marsupial pouch is an external abdominal fold of skin with a sphincter muscle enclosing the female's teats and mammary glands. In some marsupial species, the pouch is where the developing young will remain for up to 80% of the total lactation period 23 and provides protection by enclosing the young in a stable environment, free from predators and significant fluctuations in temperature and humidity 24 . The non-sterile pouch has been demonstrated to contain diverse microbial communities and bacteria that may be pathogenic to the developing young [25][26][27][28][29][30][31][32] . ...
Article
Full-text available
Wildlife harbour a diverse range of microorganisms that affect their health and development. Marsupials are born immunologically naïve and physiologically underdeveloped, with primary development occurring inside a pouch. Secretion of immunological compounds and antimicrobial peptides in the epithelial lining of the female’s pouch, pouch young skin, and through the milk, are thought to boost the neonate’s immune system and potentially alter the pouch skin microbiome. Here, using 16S rRNA amplicon sequencing, we characterised the Tasmanian devil pouch skin microbiome from 25 lactating and 30 non-lactating wild females to describe and compare across these reproductive stages. We found that the lactating pouch skin microbiome had significantly lower amplicon sequence variant richness and diversity than non-lactating pouches, however there was no overall dissimilarity in community structure between lactating and non-lactating pouches. The top five phyla were found to be consistent between both reproductive stages, with over 85% of the microbiome being comprised of Firmicutes, Proteobacteria, Fusobacteriota, Actinobacteriota, and Bacteroidota. The most abundant taxa remained consistent across all taxonomic ranks between lactating and non-lactating pouch types. This suggests that any potential immunological compounds or antimicrobial peptide secretions did not significantly influence the main community members. Of the more than 16,000 total identified amplicon sequence variants, 25 were recognised as differentially abundant between lactating and non-lactating pouches. It is proposed that the secretion of antimicrobial peptides in the pouch act to modulate these microbial communities. This study identifies candidate bacterial clades on which to test the activity of Tasmanian devil antimicrobial peptides and their role in pouch young protection, which in turn may lead to future therapeutic development for human diseases.
... The observation that the largest extinct Australian marsupial carnivore (Thylacoleo) is a vombatiform rather than a dasyurimorphian (the group that includes all extant carnivorous marsupials) presents additional circumstantial evidence that a well-developed pouch may be a prerequisite for large size. Although females of the largest extant dasyuromorphians (e.g., Dasyurus maculatus, Sarcophilus harissii) develop a posteriorly facing pouch during pregnancy, as did the thylacine (Thylacinus cynocephalus), the sickle-shaped dasyurimorphian pouch is much less extensive than the baglike pouch that characterizes the largest diprotodontians (Edwards & Deakin, 2013;Jones et al., 2001;Nowak, 1999;Rose et al., 2017;Tyndale-Biscoe, 2005). The challenges of supporting relatively large young may be sufficiently great that, even with a well-developed and/or posteriorly directed pouch, natural selection has only rarely favored the evolution of very large size among metatherians. ...
Book
This volume presents an array of different case studies which take as primary material data sourced from the NOW (‘New and Old Worlds’) database of fossil mammals. The NOW database was one of the very first large paleobiological databases, and since 1996 it has been expanded from including mainly Neogene European land mammals to cover the entire Cenozoic at a global scale. In the last two decades the number of works that are based in the use of huge databases to explore ecological and evolutionary questions has increased exponentially, and even though the importance of big data in paleobiological research has been outlined in selected chapters of general works, no volume has appeared before this one which solely focuses on the databases as a primary source in reconstructing the past. The purpose of this book is to provide an illustrative volume showing the importance of big data in paleobiological research, and presenting a broad array of unpublished examples and case studies. The book is mainly aimed to professional palaeobiologists working with Cenozoic land mammals, but the scope of the book is broad enough to fit the interest for evolutionary biologists, paleoclimatologists and paleoecologists. The volume is divided in four parts. The first part includes two chapters on the development of large paleobiological databases, providing a first-hand account on the logic and the functioning of these databases. This is a much-needed perspective which is ignored by most researchers and users of such databases and, even if centered in the NOW database, the lessons that can be learned from this part can be extended to other examples. After this introductory part, the body of the book follows and is divided into three parts: patterns in regional faunas; large scale patterns and processes; and ecological, biogeographical and evolutionary patterns of key taxa. Each chapter is written by well-known specialists in the field, with some participation of members of the NOW advisory board. The array of selected mammal taxa ranges from carnivores, equids, ruminants and rodents to the genus Homo. The topics studied also include the diversification and radiation of major clades, large-scale paleobiogeographical patterns, the evolution of ecomorphological patterns and paleobiological problems such as evolution of body size or species longevity. In most cases the results are discussed in relation to protracted environmental or paleogeographic changes.
... The observation that the largest extinct Australian marsupial carnivore (Thylacoleo) is a vombatiform rather than a dasyurimorphian (the group that includes all extant carnivorous marsupials) presents additional circumstantial evidence that a well-developed pouch may be a prerequisite for large size. Although females of the largest extant dasyuromorphians (e.g., Dasyurus maculatus, Sarcophilus harissii) develop a posteriorly facing pouch during pregnancy, as did the thylacine (Thylacinus cynocephalus), the sickle-shaped dasyurimorphian pouch is much less extensive than the baglike pouch that characterizes the largest diprotodontians (Edwards & Deakin, 2013;Jones et al., 2001;Nowak, 1999;Rose et al., 2017;Tyndale-Biscoe, 2005). The challenges of supporting relatively large young may be sufficiently great that, even with a well-developed and/or posteriorly directed pouch, natural selection has only rarely favored the evolution of very large size among metatherians. ...
Chapter
Recent studies have demonstrated dramatic changes in North American rodent and lagomorph faunas through the Cenozoic, with open-habitat specialists (characterized by increased tooth crown height and adaptations for burrowing, jumping, or running) becoming common as open and arid habitats spread. These studies have primarily focused on continental scale analyses, but comparisons of regional and local scale changes are key to understanding how individual faunas changed over time and the roles exerted by topography and local climatic conditions on these faunal changes. Here, we use a database of all fossil rodents and lagomorphs in North America modified from NOW, MIOMAP, and FAUNMAP to compare faunas through time across nine distinct regions. Our analyses reveal asynchronous changes across the continent, with specialized dietary and locomotor adaptations in rodents and lagomorphs occurring earlier in relatively cool, arid regions at higher latitudes. Findings suggest topographic complexity and volcanic activity potentially drove aspects of ecomorphological evolution in rodents and lagomorphs. The attributes of open and arid-adapted taxa likely facilitated their spread from tectonically and volcanically active regions across the continent, as environmental conditions changed through the Cenozoic.KeywordsClimate changeHypsodontyMammal FaunasNorth AmericaRodentiaLagomorpha
... The observation that the largest extinct Australian marsupial carnivore (Thylacoleo) is a vombatiform rather than a dasyurimorphian (the group that includes all extant carnivorous marsupials) presents additional circumstantial evidence that a well-developed pouch may be a prerequisite for large size. Although females of the largest extant dasyuromorphians (e.g., Dasyurus maculatus, Sarcophilus harissii) develop a posteriorly facing pouch during pregnancy, as did the thylacine (Thylacinus cynocephalus), the sickle-shaped dasyurimorphian pouch is much less extensive than the baglike pouch that characterizes the largest diprotodontians (Edwards & Deakin, 2013;Jones et al., 2001;Nowak, 1999;Rose et al., 2017;Tyndale-Biscoe, 2005). The challenges of supporting relatively large young may be sufficiently great that, even with a well-developed and/or posteriorly directed pouch, natural selection has only rarely favored the evolution of very large size among metatherians. ...
Chapter
Sparassodonts in South America and hyaenodonts in Africa present an interesting test case for comparing the evolutionary trajectories of ecologically similar clades on once isolated continents. Despite being distantly related within Mammalia (sparassodonts are metatherians and hyaenodonts are eutherians), they share many adaptations for a carnivorous diet, including an entire molar row modified into carnassials. Using data from the NOW database, we find that both groups became increasingly carnivorous during the Cenozoic, though only hyaenodonts showed a corresponding increase in body size. This difference may be due to different reproductive strategies in the two groups. Further comparisons between these groups and comparisons with modern carnivorans are necessary to determine the degree to which parallels and differences in the evolutionary trajectories of all three are related to the number of pairs of carnassialized teeth (i.e., several versus only one) and the adaptability of the distal tooth row.KeywordsBody MassCarnivoryEndemismIsland ContinentHyaenodontaPaleobiologyMetatheriaSparassodonta
... The lungs are immature, so gas exchange takes place through the skin for some days. Inside the pouch, the humid environment may aid this integumental gas exchange [20]. ...
Article
Full-text available
We dissected carcasses of eight mature females, both parous and non-parous specimens, to study the macroscopic anatomy of the female reproductive system in the sugar glider. The genital system includes double organs, namely the right and left ones, which are completely separated. It includes two ovaries, two oviducts, two uteri and a vaginal complex. The uteri are fusiform-shaped and lack horns. The vaginal complex includes two lateral vaginae and a median vagina, also called the ‘birth canal’. The cranial end of both lateral vaginae partially fuses, forming an expansion named the vaginal sinus, which is divided into two parts by a longitudinal septum, one for each vagina, where the ipsilateral uterine cervix opens. The caudal end of the lateral vaginae opens into a medial and impar duct: the urogenital sinus that serves as a common passage for the reproductive and urinary systems. In non-pregnant females, only the lateral vaginae are present. In pregnant and recently parous females, a short median vagina extends from the caudal wall of the vaginal sinus to the cranial end of the urogenital sinus. In the ventral wall of this sinus, next to its caudal opening, there is a forked clitoris.
... In between these two developmental stages, there is a period of relative dormancy during which, by various means, the pollen is moved from the anther sac to the stigmatic surface, a process we call pollination (Raven et al. 1992). An analogous process is perhaps seen in marsupial animals where, after a period of development in the womb, the immature offspring must move to the marsupial pouch to continue its development (Edwards and Deakin 2013). Notice that in some angiosperm species pollination is done before the pollen grain has made its sperm, and even if the sperm are present during pollination they are often not yet sexually mature (Snell 2012;Sprunck et al. 2012;Williams et al. 2014;Liu and Wang 2021). ...
Article
Full-text available
The two-sex model makes the assumption that there are only two sexual reproductive states: male and female. However, in land plants (embryophytes) the application of this model to the alternation of generations life cycle requires the subtle redefinition of several common terms related to sexual reproduction, which seems to obscure aspects of one or the other plant generation: For instance, the homosporous sporophytic plant is treated as being asexual, and the gametophytes of angiosperms treated like mere gametes. In contrast, the proposal is made that the sporophytes of homosporous plants are indeed sexual reproductive organisms, as are the gametophytes of heterosporous plants. This view requires the expansion of the number of sexual reproductive states we accept for these plant species; therefore, a three-sex model for homosporous plants and a four-sex model for heterosporous plants are described and then contrasted with the current two-sex model. These new models allow the use of sexual reproductive terms in a manner largely similar to that seen in animals, and may better accommodate the plant alternation of generations life cycle than does the current plant two-sex model. These new models may also help stimulate new lines of research, and examples of how they might alter our view of events in the flower, and may lead to new questions about sexual determination and differentiation, are presented. Thus it is suggested that land plant species have more than merely two sexual reproductive states and that recognition of this may promote our study and understanding of them.
... The absence of infants could be related to the observation time, which did not coincide with the birth season, or it could be due to technical factors of observation. This could relate to the behavior and the marsupial reproductive system, as it is known that the marsupials giving birth to altricial young that typically develop in a pouch (Edwards and Deakin 2012). In addition, it was found that cuscus would move into hiding and then stay still when they were disturbed by the presence of humans, this is similar to the research of Repi et al. (2019) of A. melanotis in Salibabu island and Nugraha and Mustari (2017) of Ailurops ursinus in Tanjung Peropa, Southeast Sulawesi, Indonesia. ...
Article
Full-text available
The Talaud bear cuscus (Ailurops melanotis) has been reported from Sangihe (the largest island in the Sangihe Island group) and Salibabu (within the Talaud Islands). As an endemic species of Indonesia, this species is rare and there is no certainty regarding its precise geographic distribution or population size. This research aimed to estimate population density and provide the first preliminary data on its geographical distribution, as well as general description of its habitat. Our research shows that A. melanotis occurs on three islands: Salibabu Island, Nusa Island, and Bukide Island, and probably also exists in the Sahandaruman mountain on Sangihe Island. Our population surveys estimate, population density on each island as: Salibabu: 3.69 ± 2.54 ind/km 2 , with an estimated total population of 28.95 individuals, Nusa Island: was 12.31 ± 2.58 ind/km 2 , with an estimated population of 19.08 individuals, and Bukide Island: 7.17 ± 1.79/km 2 , with an estimated population of 10.40 individuals. Information regarding population is a key guiding factor in conservation efforts, where population size is related to extinction risk (threat status) and its geographical distribution, this can help to determine conservation priorities for species or habitats.
... In between these two developmental stages there is a period of relative dormancy during which, by various means, this male gametophyte is moved from the anther sac to the stigmatic surface, and it is this movement which we call pollination (Raven et al., 1992). An analogous process is perhaps seen in marsupial animals where, after a period of development in the womb, the immature offspring must move to the marsupial pouch to continue its development (Edwards and Deakin, 2013). Notice that in some angiosperm species pollination is sometimes done before the pollen grain has made its sperm, and even if the sperm are present during pollination they are often not yet sexually mature (Snell, 2012;Sprunck et al., 2012). ...
Preprint
The current plant two-sex model makes the assumption that there are only two sexual reproductive states: male and female. However, the application of this model to the plant alternation of generations requires the subtle redefinition of several common terms related to sexual reproduction, which also seems to obscure aspects of one or the other plant generation: For instance, the homosporous sporophytic plant is treated as being “asexual,” and the gametophytes of angiosperms treated like mere gametes. In contrast, the proposal is made that the sporophytes of homosporous plants are indeed sexual reproductive organisms, as are the gametophytes of heterosporous plants. This view requires the expansion of the number of sexual reproductive states we accept for plants, therefore a three-sex model for homosporous plants and a four-sex model for heterosporous plants are described and then contrasted with the current two-sex model. These new models allow the use of sexual reproductive terms in a manner largely similar to that seen in animals, and may better accommodate the plant alternation of generations life cycle than does the current plant two-sex model. These new three-sex and four-sex models may also help stimulate new lines of research, and examples of how they might alter our view of the flower, and may lead to new perspectives in terms of sexual determination, are presented. Thus it is suggested that plants have more than merely two sexual reproductive states, and that recognition of this may promote our study and understanding of plants.
Chapter
The traditional view of the relationship of marsupials is that of Huxley (1880), who held that Metatheria represent a stage of evolutionary development between the Prototheria (for example, platypus and spiny anteater) and the Eutheria (placental mammals). Huxley’s view implies that the living mammals thus represent three groups which evolved one from another, in the sequence Prototheria — Metatheria — Eutheria. It is this background against which features of marsupial anatomy and physiology may be interpreted as primitive in comparison with placental equivalents; thus several authors (for example, Lillegraven, 1969; Sharman, 1970) see certain aspects of marsupial reproductive biology as primitive, restrictive or inefficient when compared with similar features of placental reproduction.
Chapter
The development of a complex multicellular adult mammal from a single cell is as wondrous and awesome as the evolution of mammals themselves from simple single cell organisms. The parallels between the ontogeny of organisms and their phylogeny have long been recognized and were originally expressed by Haeckel as “ontogeny recapitulates phylogeny”. This doctrine initially generated considerable discussion and although it is not now generally accepted, it is obvious that there is some relationship between the two. For example, much phylogenetic change is the result of changes in developmental rates and timing (Gould 1977).
Chapter
Marsupials are born in a very immature state. Many of the developmental processes that occur in utero in eutherian mammals take place during pouch life in marsupials. The timetable of the development of their physiological systems is strongly affected by the need to meet the challenges of the external world at a very early stage. Marsupial pouch young therefore offer convenient experimental systems for addressing biomedical questions, which are much harder to tackle using their less accessible eutherian equivalents.
Article
The lactational strategy adopted by marsupials is very different to that of eutherian mammals, in terms of the developmental changes in the composition of the milk during lactation and the hormonal profile associated with these changes. Most studies have focused on the dramatic changes in carbohydrate and fat in the milk with surprisingly little attention being directed to the control of the milk proteins. Studies presented in this chapter have focused on the mechanism of control of two critical stages of the lactation cycle in Macropus eugenii (see Fig.1.1); firstly, the transition from Phase 1 to Phase 2 as lactation is initiated (lactogenesis) and secondly, the transition from Phase 2 to Phase 3 with the accompanying changes in the qualitative and quantitative synthesis of milk These questions have been addressed using a mammary gland explant culture system in an attempt to equate what is known about the hormonal changes in the peripheral circulation at these times with the capacity of the mammary gland to synthesize specific milk proteins. In addition, and just as importantly, the value of the mammary gland of M. eugenii as an unique experimental model to assess questions of fundamental importance in biology will be discussed.
Chapter
Gametogenesis is the sequence of events that occur as germ cells, or gonocytes, of the sex cell line form gametes. This complex process occurs within the gonadal tissues. The general process of gametogenesis is divisible into two main phases; a gonial phase and a gametogenic phase. These phases can be distinguished by the mode of cell division that gamete precursors undergo. During the gonial phase, cells of the germ cell line within the gonad undergo successive mitotic divisions and establish a population of gonial cells. In males, this phase is referred to as the spermatogonial phase during which spermatogonial cells are produced. In females of most vertebrates, the gonial phase occurs very early in the life cycle and establishes a population of oogonia within the ovary. During the subsequent gametogenic phase of both males and females, descendents of these gonial cells undergo meiotic divisions and are transformed into mature gametes.
Chapter
This is the first re-appraisal in 50 years of concepts of development made in birds. This book is a case study in evolutionary diversification of life histories. Although birds have a rather uniform body plan and physiology, they exhibit marked variation in development type, parental care, and rate of growth. Altricial birds are fully dependent on their parents for warmth and nutrition and begin posthatching life in a more or less embryonic condition. At the other extreme, such superprecocial species as the megapodes are independent of all parental care from hatching, and the neonate, able to fly, resembles an adult bird. This book thus attempts to present an integrative perspective of organism biology, ecology, and evolution.