The origins of lactation and the evolution of milk: a review with new hypotheses

Abstract

ABSTRACTLactation is central to mammalian reproduction, and an understanding of the origins of lactation is necessary to comprehend the early evolution of the Class Mammalia. In modern mammals, lactation is a staggeringly complex phenomenon involving morphological, physiological, biochemical, ecological, and behavioural adaptations. Because such a complex web of adaptations could not have arisen de novo, lactation must have begun as a much simpler process. Hypotheses regarding the original adaptive value of proto‐lacteal secretions invoke thermoregulatory, antibiotic, behavioural or nutritive functions. In this review, we evaluate each of these hypotheses and attempt to reconstruct the origins of lactation in the light of current concepts of the biology of early mammals and their ancestors, the origin of mammary glands, the evolution of extravitelline nutrient provision, and the physiology and biochemistry of milk synthesis and secretion. Drawing upon empirical evidence and theoretical considerations, we present a gradualistic scenario involving the following steps. First, incubation of eggs was aided by development of a vascularized abdominal incubation patch. Secondly, anti‐microbial secretions from cutaneous glands of the incubation patch enhanced survival of eggs or offspring. At this stage, these secretions could have supplemented vitelline nutrients (in much the same way as oviductal secretions do in monotremes), perhaps facultatively. Subsequently, hypertrophy and specialization of cutaneous glands accompanied the controlled production of a copious, nutritious secretion, which eventually evolved into a primary source of energy for development and growth of the offspring. We outline important events in the evolution of milk, and suggest studies likely to provide indirect tests of the evolutionary hypotheses discussed.