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Structural and physiological changes in the female reproductive system underlie the origins of pregnancy in multiple vertebrate lineages. In mammals, the glandular portion of the lower reproductive tract has transformed into a structure specialized for supporting fetal development. These specializations range from relatively simple maternal nutrient provisioning in egg-laying monotremes to an elaborate suite of traits that support intimate maternal-fetal interactions in Eutherians. Among these traits are the maternal decidua and fetal component of the placenta, but there is considerable uncertainty about how these structures evolved. Previously, we showed that changes in uterine gene expression contributes to several evolutionary innovations during the origins of pregnancy (Mika et al., 2021b). Here, we reconstruct the evolution of entire transcriptomes (‘ancestral transcriptome reconstruction’) and show that maternal gene expression profiles are correlated with degree of placental invasion. These results indicate that an epitheliochorial-like placenta evolved early in the mammalian stem-lineage and that the ancestor of Eutherians had a hemochorial placenta, and suggest maternal control of placental invasiveness. These data resolve major transitions in the evolution of pregnancy and indicate that ancestral transcriptome reconstruction can be used to study the function of ancestral cell, tissue, and organ systems.

There are many different forms of nutrient provision in viviparous (live-bearing) species. The formation of a placenta is one method where the placenta functions to transfer nutrients from mother to fetus (placentotrophy), to transfer waste from the fetus to the mother, and to perform respiratory gas exchange. Despite having the same overarching function, there are different types of placentation within placentotrophic vertebrates, and many morphological changes occur in the uterus during pregnancy to facilitate formation of the placenta. These changes are regulated in complex ways but are controlled by similar hormonal mechanisms across species. This review describes current knowledge of the morphological and molecular changes to the uterine epithelium preceding implantation among mammals. Our aim is to identify the commonalities and constraints of these cellular changes to understand the evolution of placentation in mammals and to propose directions for future research. We compare and discuss the complex modifications to the ultrastructure of uterine epithelial cells (UEC) and show that there are similarities in the changes to the cytoskeleton and gross morphology of the UEC, especially of the apical and lateral plasma membrane of the cells during the formation of a placenta in all eutherians and marsupials studied to date. We conclude that further research is needed to understand the evolution of placentation among viviparous mammals, particularly concerning the level of placental invasiveness, hormonal control, and genetic underpinnings of pregnancy in marsupial taxa. Summary sentence There are many complex modifications to the ultrastructure of uterine epithelial cells during pregnancy with similarities in the changes to their gross morphology during the formation of a placenta in eutherians and marsupials studied to date. Graphical Abstract

Early pregnancy is a critical time for successful reproduction; up to half of human pregnancies fail before the development of the definitive chorioallantoic placenta. Unlike the situation in eutherian mammals, marsupial pregnancy is characterised by a long pre-implantation period prior to the development of the short-lived placenta, making them ideal models for study of the uterine environment promoting embryonic survival pre-implantation. Here we present a transcriptomic study of pre-implantation marsupial pregnancy, and identify differentially expressed genes in the Sminthopsis crassicaudata uterus involved in metabolism and biosynthesis, transport, immunity, tissue remodelling, and uterine receptivity. Interestingly, almost one quarter of the top 50 genes that are differentially upregulated in early pregnancy are putatively involved in histotrophy, highlighting the importance of nutrient transport to the conceptus prior to the development of the placenta. This work furthers our understanding of the mechanisms underlying survival of pre-implantation embryos in the earliest live bearing ancestors of mammals.

The seasonal changes in thermal physiology and torpor expression of many heterothermic mammals are controlled by photoperiod. As function at low body temperatures during torpor requires changes of tissue lipid composition, we tested for the first time whether and how fatty acids are affected by photoperiod acclimation in hamsters, Phodopus sungorus, a strongly photoperiodic species. We also examined changes in fatty acid composition in relation to those in morphology and thermal biology. Hamsters in short photoperiod had smaller reproductive organs and most had a reduced body mass in comparison to those in long photoperiod. Pelage colour of hamsters under short photoperiod was almost white while that of long photoperiod hamsters was grey-brown and black. Short photoperiod acclimation resulted in regular (28% of days) torpor use, whereas all hamsters in long photoperiod remained normothermic. The composition of total fatty acids differed between acclimation groups for brown adipose tissue (5 of 8 fatty acids), heart muscle (4 of 7 fatty acids) and leg muscle (3 of 11 fatty acids). Importantly, 54% of all fatty acids detected were correlated (r(2) = 0.60 to 0.87) with the minimum surface temperature of individuals, but the responses of tissues differed. While some of the compositional changes of fatty acids were consistent with a 'homeoviscous' response, this was not the case for all, including the sums of saturated and unsaturated fatty acids, which did not differ between acclimation groups. Our data identify a possible nexus between photoperiod acclimation, morphology, reproductive biology, thermal biology and fatty acid composition. They suggest that some of the changes in thermal physiology are linked to the composition of tissue and organ fatty acids.

Central to understanding animal ecology is how prey cope with the interacting risks of starvation and predation. This tradeoff is modulated by the energy requirements of prey, yet relatively few studies have incorporated physiological mechanisms for energy savings when considering the behavioural response of prey to predation risk. In our study, we aimed to determine individual variation in behaviour, resting metabolism, body temperature and response to 24-h starvation within a captive population of fat-tailed dunnarts (Sminthopsis crassicaudata; 15-g insectivorous marsupials), and then, using semi-outdoor enclosures, test whether foraging effort and thermal energetics are adjusted in response to manipulation of ground cover, which for small mammals can simulate predation risk. We found that, under the low cover (high predation risk) treatment, dunnarts consumed less food and employed a greater daily reduction in body temperature between their active and rest phase. This result supports the hypothesis that rest-phase thermoregulatory energy savings are employed, even when food is available, if predation risk is perceived to increase the cost of foraging. Individuals exhibited correlated variation along two orthogonal axes incorporating the measured behavioural and metabolic variables, but these differences were not correlated with responses to starvation and predation risk. Our experiment demonstrates that flexibility in daily energy requirements provided by heterothermy can have important consequences for how small mammals respond to both starvation and predation risks. Such challenges are amplified in degraded habitat with introduced predators, making the capacity for heterothermy an even more important mechanism for survival.

Some mammals hibernate in response to harsh environments. Although hibernating mammals may metabolize proteins, the nitrogen metabolic pathways commonly activated during hibernation are not fully characterized. In contrast to the hypothesis of amino acid preservation, we found evidence of amino acid metabolism as three of five key enzymes, including phenylalanine hydroxylase (PAH), homogentisate 1,2-dioxygenase (HGD), fumarylacetoacetase (FAH), involved in phenylalanine and tyrosine catabolism were co-upregulated during hibernation in two distantly related species of bats, Myotis ricketti and Rhinolophus ferrumequinum. In addition, the levels of phenylalanine in the livers of these bats were significantly decreased during hibernation. Because phenylalanine and tyrosine are both glucogenic and ketogenic, these results indicate the role of this catabolic pathway in energy supply. Since any deficiency in the catabolism of these two amino acids can cause accumulations of toxic metabolites, these results also suggest the detoxification role of these enzymes during hibernation. A higher selective constraint on PAH, HPD, and HGD in hibernators than in non-hibernators was observed, and hibernators had more conserved amino acid residues in each of these enzymes than non-hibernators. These conserved amino acid residues are mostly located in positions critical for the structure and activity of the enzymes. Taken together, results of this work provide novel insights in nitrogen metabolism and removal of harmful metabolites during bat hibernation.

Marsupials have a slow rate of development and this allows a detailed examination of thermoregulatory developmental changes and stages. We quantified the cooling rates of marsupial dunnarts ( Sminthopsis crassicaudata ) at 40–56 days (d) old, and torpor and basking behaviour in animals given the option to bask in four age groups from 60 to 150 d. The development of thermoregulation was a continuum, but was characterised by three major thermoregulatory stages: (1) at 40 d, animals were unable to maintain a constant high body temperature during short-term cold exposure; (2) at 60 d, animals could maintain a high T b for the first part of the night at an ambient temperature of 15.0 ± 0.7 °C; later in the night, they entered an apparent torpor bout but could only rewarm passively when basking under a heat lamp; (3) from ~90 d, they expressed prolonged torpor bouts and were able to rewarm endogenously. Young newly weaned 60 d animals were able to avoid hypothermia by basking. In this case, basking was not an optional behavioural method of reducing the cost of rewarming from torpor, but was essential for thermoregulation independent of the nest temperature. Results from our study suggest that basking is a crucial behavioural trait that permits young marsupials and perhaps other juvenile altricial mammals to overcome the developmental stage between poikilothermy early in development and full endothermy later in life.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Erythroblastic islands are multicellular clusters in which a central macrophage supports the development and maturation of red blood cell (erythroid) progenitors. These clusters play crucial roles in the pathogenesis observed in animal models of hematological disorders. The precise structure and function of erythroblastic islands is poorly understood. Here, we have combined scanning electron microscopy and immuno-gold labeling of surface proteins to develop a better understanding of the ultrastructure of these multicellular clusters. The erythroid-specific surface antigen Ter-119 and the transferrin receptor CD71 exhibited distinct patterns of protein sorting during erythroid cell maturation as detected by immuno-gold labeling. During electron microscopy analysis we observed two distinct classes of erythroblastic islands. The islands varied in size and morphology, and the number and type of erythroid cells interacting with the central macrophage. Assessment of femoral marrow isolated from a cavid rodent species (guinea pig, Cavis porcellus) and a marsupial carnivore species (fat-tailed dunnarts, Sminthopsis crassicaudata) showed that while the morphology of the central macrophage varied, two different types of erythroblastic islands were consistently identifiable. Our findings suggest that these two classes of erythroblastic islands are conserved in mammalian evolution and may play distinct roles in red blood cell production.

Many animals consume foods that vary in all 3 macronutrients: carbohydrates, lipid, and protein. Yet most studies of diet regulation only consider pairs of nutrients (protein and carbohydrate or protein and lipid). Diet regulation also extends beyond nutrient and energy intake to include sources of energy expenditure, such as changes in activity level. We used a right-angled mixture triangle design to quantify the 3-dimensional intake target of fat-tailed dunnarts, Sminthopsis crassicaudata, and to test the consequences of free choice for energy intake, weight gain, and activity level relative to a standard maintenance diet. Dunnarts consistently preferred a relatively high-lipid, low-protein, and low-carbohydrate diet in 3 separate feeding experiments. Dunnarts also consumed a higher total energy intake during choice relative to no-choice periods. However, the weight of dunnarts was not consistently higher at the end of choice relative to no-choice periods, which is likely because dunnarts increased their activity level during periods of choice and decreased their activity when on no-choice diets. This shows that increases in the intake of lipid, which is an important component in the diet of dunnarts, does not necessarily lead to increases in weight gain because these animals can adjust energy expenditure to balance their energy budget. These results have important implications for the design of diets for animals in captivity and demonstrate that consideration of both energy intake and expenditure are needed for a more comprehensive and integrative understanding of diet regulation by animals.