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

Abstract

Lactation 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.

Evolution of milk oligosaccharides and lactose: a hypothesis

“…We suggest that initially these oligosaccharides were biologically significant mainly as anti-microbial defense factors, along with other defense factors present in milk such as antibodies, lactoferrin and lysozyme. This scenario is consistent with the hypothesis that mammary glands and milk production evolved as the part of the innate immune system (Vorbach et al, 2006) and that the anti-microbial role of milk components evolved before their nutritional function (Blackburn et al, 1989).…”

Evolution of mammals: lactation helps mothers to cope with unreliable food supplies

“…Dall and I. L. Boyd 2053 unreliably from one foraging trip to the next (Lack 1968). Therefore, it is likely that there was strong selection for the transition from minimally nutritious proto-lacteal secretions, perhaps produced originally for their anti-microbial properties (Blackburn et al 1989), to fully-fledged milk production and consumption in the insectivorous mammal-like reptiles with extended maternal care (egg incubation and altricial young). Moreover, the metabolic demands of endothermy, once it evolved in the mammalian lineage, will have exacerbated the risk of running a negative energy budget, and hence the unreliability of food resources.…”

“…Of course the trade-off we explore here is unlikely to be solely responsible for the evident variation in the form and function of lactation across mammalian taxa. Once parental feeding from maternal reserves evolved in the mammalian lineage it is likely that other functional opportunities were created leading to the evolution of a wide range of mammalian traits and strategies (Pond 1977(Pond , 1998Hayssen et al 1985;Blackburn et al 1989;Hayssen 1993). For example, the nutritional quality of milk encourages very rapid postnatal growth, allowing the production of relatively small neonates and early maturation.…”

“…Moreover, the adoption of lactation as a mode of feeding young is thought to be related directly to the evolution of many other mammalian traits (Pond 1977(Pond , 1998Hayssen et al 1985;Blackburn et al 1989;Hayssen 1993). However, since Darwin, the evolution of lactation has troubled evolutionary biologists.…”

“…However, since Darwin, the evolution of lactation has troubled evolutionary biologists. It is a 'complex adaptation' with highly integrated components, including the morphological, physiological and behavioural aspects of milk production, ingestion and digestion (Blackburn et al 1989;Hayssen 1993). Indeed, early critics of Darwin's thesis targeted lactation as a problem for gradualist explanations (Mivart 1871), and the incipient stages in the evolution of milk production remain particularly difficult to explain (Blackburn et al 1989).…”