Evolution and development of dual ingestion systems in mammals: notes on a new thesis and its clinical implications

Abstract

Traditionally, the development of oral feeding is viewed as a continuous, unitary process in which reflex-dominated sucking behavior gives rise to a more varied and volitional feeding behavior. In contrast, we consider the thesis that the infant develops two separable ingestive systems, one for suckling and one for feeding. First, we apply an evolutionary perspective, recognizing that suckling-feeding is a universal, mammalian developmental sequence. We find that in mammalian evolution, feeding systems in offspring were established prior to the evolution of lactation, and therefore suckling is a separable feature that was added to feeding. We next review an experimental literature that characterizes suckling and feeding as separable in terms of their topography, sensory controls, physiological controls, neural substrates, and experience-based development. Together, these considerations constitute a view of "dual ingestive systems." The thesis, then, is that suckling is not a simple precursor of feeding but is a complete behavior that emerges, forms, and then undergoes a dissolution that overlaps with the emergence of independent feeding. This thesis guides us to focus differently on the challenges of properly managing and facilitating oral ingestion in infants, especially those born preterm, prior to the developmental onset of suckling.

Figure 1

A simplified representation of some of the sequential, evolutionary radiations that appear from Amniota (I.) to Mammalia (II.) showing, for comparative purposes, the cladistic separation of the synapsids and saurosids as divergent subsets of Amniota. Along the dashed line, the diagram traces the trajectory from the Synapsida to the crown group, Mammalia, with select representatives of various radiating groups and species, shown by the light dashed lines. Bold horizontal lines depict the appearance and duration of each taxonomic group shown. The black triangle at the Jurassic-Cretaceous boundary denotes the end of the age of dinosaurs. The geological timescale and periods appear together at the bottom of the figure which was adapted with alterations from [10].

Figure 2

Developmental course of selected digestive elements of the mouth, stomach, pancreas, and intestine. Data were from [47, 50] and initially integrated in a discussion [51] that provides fuller reference information.

Figure 3

An idealized depiction of the coordinate development of suckling and feeding behavior which, together, comprise the development of oral ingestion. Note that the horizontal axis depicts an unspecified range of “developmental time” with vertical markers exemplifying a preterm birth and a term birth. The purpose of noting these events is to illustrate that the suckling system may not be functionally ready for the preterm infant, whereas it is prepared to be engaged at term.