Morphology and evolution of the oral shield in marsupial neonates including the newborn monito del monte (Dromiciops gliroides, Marsupialia Microbiotheria) pouch young

Abstract

Newborn marsupials can be arranged into three grades of developmental complexity based on their external form, as well as based on their organ systems and their cytology. The dasyurids are considered the least developed marsupials at birth, while didelphids and peramelids are intermediate, and macropods are the most developed. Currently there is still little information on caenolestid and microbiotherid development at birth. Developmental stages can be graded as G1, G2 and G3, with G1 being the least developed at birth, and G3 the most developed. Marsupials are also characterized by having an extremely developed craniofacial region at birth compared with placentals. However, the facial region is also observed to vary in development between different marsupial groups at birth. The oral shield is a morphological structure observed in the oral region of the head during late embryological development, which will diminish shortly after birth. Morphological variation of the oral shield is observed and can be arranged by developmental complexity from greatly developed, reduced to vestigial. In its most developed state, the lips are fused, forming together with the rhinarium, a flattened ring around the buccal opening. In this study, we examine the external oral shield morphology in different species of newborn marsupials (dasyurids, peramelids, macropods and didelphids), including the newborn monito del monte young (Dromiciops gliroides - the sole survivor of the order Microbiotheria). The adaptive value of the oral shield structure is reviewed, and we discuss if this structure may be influenced by developmental stage of newborn, pouch cover, species relatedness, or other reproductive features. We observe that the oral shield structure is present in most species of Marsupialia and appears to be exclusively present in this infraclass. It has never been described in Monotremata or Eutherians. It is present in unrelated taxa (e.g. didelphids, dasyurids and microbiotherids). We observe that a well-developed oral shield may be related to ultra altricial development at birth, large litter size (more than two), and is present in most species that lack a pouch in reproductive adult females or have a less prominent or less developed pouch with some exceptions. We try to explore the evolution of the oral shield structure using existing databases and our own observations to reconstruct likely ancestral character states that can then be used to estimate the evolutionary origin of this structure and if it was present in early mammals. We find that a simple to develop oral shield structure (type 2-3) may have been present in marsupial ancestors as well as in early therians, even though this structure is not present in the extant monotremes. This in turn may suggest that early marsupials may have had a very simple pouch or lacked a pouch as seen in some living marsupials, such as some dasyurids, didelphids and caenolestids. The study's results also suggest that different morphological stages of the oral shield and hindlimb development may be influenced by species size and reproductive strategy, and possibly by yet unknown species-specific adaptations.

Keywords: Dromiciops gliroides; marsupial; monotreme; newborn; oral shield.

Figure 1

All marsupial newborns show strong developed forelimbs with claws on the paws, while the hindlimbs are still poorly developed with some not even showing signs of the digits: (a) Eastern quoll; (b) Tasmanian devil; (c) numbat; (d) monito del monte; (e) grey four‐eyed opossum; (f) grey short‐tailed opossum; (g) Virginia opossum; (h) common opossum; (i) southern brown bandicoot; (j) brushtail possum; (k) red‐necked pademelon; (l) black‐striped wallaby; (m) common wallaroo; (n) koala; (o) Southern marsupial mole. [The figure was adapted from Schneider (2011) adding the monito del monte, numbat, grey four‐eyed opossum, red‐necked pademelon, black‐striped wallaby, common wallaroo and the drawings of the Tasmanian devil, common opossum and southern marsupial mole adapted from Hughes & Hall, 1988; Osman Hill, 1952; Wood Jones, 1921, respectively.]

Figure 2

Development of the oral shield. It may be extensively developed like in (a) the Eastern quoll with no difference apparent between the upper and lower mandible. Or extensive to reduced as in the (b) numbat and reduced in (c) the monito del monte, (d) the grey four‐eyed opossum, (e) the grey short‐tailed opossum and (f) the Virginia opossum, which show an oral shield‐like rhinarium structure with slightly visible lib faults. The oral shield is simple in the (g) Southern brown bandicoot and (h) the brushtail possum and vestigial in (i) the red‐necked pademelon, (j) the black‐striped wallaby, (k) koala and (l) Southern marsupial mole (LF, lip fold; N, naris; SM, sulcus medianus) (figure adapted from Schneider, 2011 and marsupial mole redrawn from Wood Jones, 1921).

Figure 3

Newly hatched monotremes are at a similar stage of development as marsupial newborns of stage G3: while the hindlimbs are still paddle‐like the forelimbs are well developed and the forepaws exhibit claws. In contrast to marsupial young both echidna (left) and platypus (right) have an egg tooth (ET) and caruncle (C). Their mouth is already a slide‐like opening, which is possibly an adaptation to allow them to sip milk from the milk patch. Parts of the foetal membrane (FM) are still visible. (Echidna drawn after a photo in Griffiths, 1978 p. 242, already presented in Schneider, 2011; platypus adapted from a drawing in Hughes & Hall, 1998.)

Figure 4

While the adult numbat (a) has a thin and pointy muzzle, this is not the case in pouch young shown here (b–d) (all MA242 from Hill Collection). Even though the oral shield structure disappears the muzzle remains short, which is likely to be an adaptation to allow the young to stay securely attached to the teat. This may be especially important as female numbats do not possess a pouch.

Figure 5

Phylogenetic relationships of Dromiciops and extant marsupials with extinct species based on maximum parsimony analysis of the morphology‐only matrix. (a) Parsimony ancestral state reconstruction using MESQUITE software (Maddison & Maddison, 2015) demonstrating the prevalence of character 258 (oral shield) based on majority‐rule consensus of 100 trees. Consistency index = 0.36194416, tree length = 967, retention index = 0.634262. Character states are: (0): no oral shield; lips are separated and mouth can be open wide; (1): oral shield vestigial but lips still closed but clearly separated from the rhinarium; (2): oral shield simple; lips not swollen and rhinarium forming separate structure; (3): structure reduced compared with state 4, the lips becoming visible as folds of the skin, the lips are slightly swollen around the buccal opening and the rhinarium is well developed; (4): upper and lower lips form together with the rhinarium a flattened ring structure that surrounds the buccal opening. (b) Parsimony ancestral state reconstruction using MESQUITE software (Maddison & Maddison, 2015) demonstrating the prevalence of character 260 (Pouch type in mammary area) based on majority‐rule consensus of 100 trees. Consistency index = 0.36194416, tree length = 967, retention index = 0.634262. Character states are (0): in non‐breeding adults the mammary area has no covering fold of skin and the teats are exposed. Marginal, usually lateral, ridges of skin develop during the breeding season and the pouch may become deeper and evaginated. These lateral ridges of skin can be connected posteriorly. (1): Pouch consists of lateral folds of skin connected posteriorly; pouch opening anteriorly and covers the pouch young and teats. (2): The mammary area is completely covered by a fold of skin. The so‐formed deep pouch opens at its anterior margin. (3): The mammary area is completely covered by a fold of skin. The so‐formed deep pouch opens at its posterior margin and covers the pouch young and teats. (4): No pouch develops. No skin folds during breeding/reproductive season. The mammary area, as well as the pouch young that are attached to the teats are not covered by any skin folds during the first and second phase of lactation (Tyndale‐Biscoe, 2005). (5): Thin pouch‐like structure develops during reproductive period. Small invagination in the mammary area.

Figure 6

(a) Results of multiple correspondence analyses (MCA) using SPSS for species for which the categories: oral shield, pouch type, teat coverage, and number of young were known. The MCA included data from 22 species, including four American species (grey short‐tailed opossum, Virginia opossum, grey four‐eyed opossum, monito del monte) and 18 Australian species (tammar wallaby, eastern grey kangaroo, black‐striped wallaby, common wallaroo, red‐necked pademeleon, brush‐tailed rock wallaby, long‐nosed potoroo, musky rat kangaroo, koala, Southern hairy wombat, brushtail possum, Tasmanian devil, yellow‐footed antechinus, numbat, Southern brown bandicoot, Northern brown bandicoot, Eastern quoll, striped‐faced dunnart). The results can be grouped into the three stages G1, G2 and G3 of pouch young development. (b) Marsupial adult female head and body length (mm) vs. crl (crown rump length) of neonate young (mm). Orange circles represent G1 species, blue circles G2 and black G3. White filled circles with black outline are species in which the G group is unknown or n.a. (e.g. monotremes). The dark dotted line represents the average % of birth size of the adult size (4%). The light grey dotted line marks the 1%. Australian adult female length was taken from Van Dyck & Strahan (2008), Fadem et al. (1982) for grey short tailed opossum; Castro‐Arellano et al. (2000) for grey four‐eyed opossum and Marshall (1978) for monito del monte. Measurement of newborn honey possum taken from Oates et al. (2007).