Comparative anatomy of neonates of the three major mammalian groups (monotremes, marsupials, placentals) and implications for the ancestral mammalian neonate morphotype

Abstract

The existing different modes of reproduction in monotremes, marsupials and placentals are the main source for our current understanding of the origin and evolution of the mammalian reproduction. The reproductive strategies and, in particular, the maturity states of the neonates differ remarkably between the three groups. Monotremes, for example, are the only extant mammals that lay eggs and incubate them for the last third of their embryonic development. In contrast, marsupials and placentals are viviparous and rely on intra-uterine development of the neonates via choriovitelline (mainly marsupials) and chorioallantoic (mainly placentals) placentae. The maturity of a newborn is closely linked to the parental care strategy once the neonate is born. The varying developmental degrees of neonates are the main focus of this study. Monotremes and marsupials produce highly altricial and nearly embryonic offspring. Placental mammals always give birth to more developed newborns with the widest range from altricial to precocial. The ability of a newborn to survive and grow in the environment it was born in depends highly on the degree of maturation of vital organs at the time of birth. Here, the anatomy of four neonates of the three major extant mammalian groups is compared. The basis for this study is histological and ultrastructural serial sections of a hatchling of Ornithorhynchus anatinus (Monotremata), and neonates of Monodelphis domestica (Marsupialia), Mesocricetus auratus (altricial Placentalia) and Macroscelides proboscideus (precocial Placentalia). Special attention was given to the developmental stages of the organs skin, lung, liver and kidney, which are considered crucial for the maintenance of vital functions. The state of the organs of newborn monotremes and marsupials are found to be able to support a minimum of vital functions outside the uterus. They are sufficient to survive, but without capacities for additional energetic challenges. The organs of the altricial placental neonate are further developed, able to support the maintenance of vital functions and short-term metabolic increase. The precocial placental newborn shows the most advanced state of organ development, to allow the maintenance of vital functions, stable thermoregulation and high energetic performance. The ancestral condition of a mammalian neonate is interpreted to be similar to the state of organ development found in the newborns of marsupials and monotremes. In comparison, the newborns of altricial and precocial placentals are derived from the ancestral state to a more mature developmental degree associated with advanced organ systems.

Evolution and Development of the Atrial Septum

“…Already Röse () proposed the secondary foramen was an adaptation to particular conditions of gestation and Runciman and colleagues (Runciman et al, ) suggested a role for the great duration of the eutherian mammal gestation. Marsupials almost invariably have shorter gestational period (12–38 days) than eutherians (16–660 days) (Ferner et al, ). Some reptiles have a gestation period of several months (Gregorovicova et al, ), but the work of the heart, cardiac output and metabolic rate of mammals is several times greater than in similarly sized reptiles (Jensen et al, ).…”

“…They also have fur and secrete milk from pores on the belly. Marsupials, like kangaroos, give birth to very immature offspring that complete most of the development in the mother's pouch (Ferner et al, ; Guernsey et al, ). Marsupials are considered a sister group to eutherian mammals (Song et al, ).…”

The embryo of the silky shrew opossum, Caenolestes fuliginosus (Tomes, 1863): First description of the embryo of Paucituberculata

“…The embryonic pulmonary development is different between C. fuliginosus and other American marsupials, but whether these differences persist at birth is unknown. Also, to compare the heart chambers at different stages among marsupial species would be of interest because its closure varies among groups (Ferner et al, 2017;Hughes & Hall, 1988). More samples and thorough anatomical and histological descriptions should help to solve some of the unsolved questions about the life history and evolution of these groups.…”

“…Although new methods to analyze the relative events in embryology were developed in recent years (Germain & Laurin, ; Werneburg, ), the lack of samples of many mammal species hinders comprehensive analyses (Werneburg et al, ; Werneburg & Sánchez‐Villagra, ). This is true for Paucituberculata, which remains absent from phylogenetic studies that include embryological traits (Ferner, Schultz, & Zeller, ; Freyer, Zeller, & Renfree, ; Werneburg et al, ; Zeller & Freyer, ). Its inclusion can potentially offer relevant information due to its basal position in the marsupial tree (Meredith et al, , but see Bininda‐Emonds et al, ).…”

Comparative skeletal anatomy of neonatal ursids and the extreme altriciality of the giant panda

“…Here we use micro-computed tomography (lCT) to visualize the skeletal anatomy of several ursid neonates and compare their skeletal maturity levels with those of other caniform outgroup neonates. Although skeletal anatomy has not been explicitly used to assess the relative altriciality of mammalian neonates (Ferner et al 2017), we suggest it is a useful measure of maturity as it is directly connected to the functional aspects of neonatal survival such as locomotion and suckling. lCT imaging offers a non-invasive, highresolution approach to capture the anatomical details of neonate skeletons (Hautier et al 2012;Roston et al 2013;Newton et al 2018).…”