Abstract

Bears produce the most altricial neonates of any placental mammal. We hypothesized that the transition from colostrum to mature milk in bears reflects a temporal and biochemical adaptation for altricial development and immune protection. Comparison of bear milks with milks of other eutherians yielded distinctive protein profiles. Proteomic and metabolomic analysis of serial milk samples collected from six giant pandas showed a prolonged transition from colostrum to main-phase lactation over approximately 30 days. Particularly striking are the persistence or sequential appearance of adaptive and innate immune factors. The endurance of immunoglobulin G suggests an unusual duration of trans-intestinal absorption of maternal antibodies, and is potentially relevant to the underdeveloped lymphoid system of giant panda neonates. Levels of certain milk oligosaccharides known to exert anti-microbial activities and/or that are conducive to the development of neonatal gut microbiomes underwent an almost complete changeover around days 20–30 postpartum, coincident with the maturation of the protein profile. A potential metabolic marker of starvation was detected, the prominence of which may reflect the natural postpartum period of anorexia in giant panda mothers. Early lactation in giant pandas, and possibly in other ursids, appears to be adapted for the unique requirements of unusually altricial eutherian neonates.

Highlights

  • The composition of mammalian milks and the duration of lactation vary dramatically from species to species, influenced by the ecology, evolutionary history, placental type and the developmental state of the neonate at birth [1,2,3]

  • Milks collected during mid-lactation from several species were analysed by 1D protein gel electrophoresis, which highlighted the considerable differences in protein profiles among species

  • Exploiting giant pandas as representing an extreme test case even among bears, we hypothesized that maturation of colostrum to mature milk would be prolonged compared with other eutherians

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Summary

Introduction

The composition of mammalian milks and the duration of lactation vary dramatically from species to species, influenced by the ecology, evolutionary history, placental type and the developmental state of the neonate at birth [1,2,3]. Certain milk proteins are only present early in lactation and disappear, to be replaced by others that disappear and are replaced in turn through the course of lactation [4,9,10]. Such dramatic and sustained changes in milk proteins do not occur in eutherian mammals, presumably because their neonates are at a significantly more advanced stage of development at birth. The composition of milk during this colostrum phase reflects the type of placenta characteristic of the species [1]

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