Development of the Olfactory Pathways in Platypus and Echidna

Abstract

The two groups of living monotremes (platypus and echidnas) have remarkably different olfactory structures in the adult. The layers of the main olfactory bulb of the short-beaked echidna are extensively folded, whereas those of the platypus are not. Similarly, the surface area of the piriform cortex of the echidna is large and its lamination complex, whereas in the platypus it is small and simple. It has been argued that the modern echidnas are derived from a platypus-like ancestor, in which case the extensive olfactory specializations of the modern echidnas would have developed relatively recently in monotreme evolution. In this study, the development of the constituent structures of the olfactory pathway was studied in sectioned platypus and echidna embryos and post-hatchlings at the Museum für Naturkunde, Berlin, Germany. The aim was to determine whether the olfactory structures follow a similar maturational path in the two monotremes during embryonic and early post-hatching ages or whether they show very different developmental paths from the outset. The findings indicate that anatomical differences in the central olfactory system between the short-beaked echidna and the platypus begin to develop immediately before hatching, although details of differences in nasal cavity architecture emerge progressively during late post-hatching life. These findings are most consistent with the proposition that the two modern monotreme lineages have followed independent evolutionary paths from a less olfaction-specialized ancestor. The monotreme olfactory pathway does not appear to be sufficiently structurally mature at birth to allow olfaction-mediated behaviour, because central components of both the main and accessory olfactory system have not differentiated at the time of hatching.

Olfaction, navigation, and the origin of isocortex

“…In therians, however, vitellogenin genes have been pseudogenized (inactivated by nonsense mutations) at the expense of evolving more copies of casein genes (Brawand et al, 2008 ). In living monotremes the olfactory system has been reported not to be functional at birth (Ashwell, 2012 ), perhaps implying that the active compound eliciting preferential orientation to milk sources is associated with the acquisition of nipples in therian mammals, or that extant monotremes lost this capacity in their evolution. The latter is plausible considering that they have a poorly developed olfactory system, perhaps at the expense of an increased electrosensory sensitivity that aids them in searching for food (Ashwell, 2013 ).…”

Early development of the nervous system of the eutherian <i>Tupaia belangeri</i>

“…Thus, it turned out that, in newborn marsupials (Macropus eugenii), these pathways are usually too immature to support guidance to the pouch and nipple (Ashwell et al, 2008). Accordingly, at birth, the degree of maturity of these olfactory pathways is not high enough to allow olfaction-mediated behavior in platypus and echidnas, "two modern monotreme lineages that have followed independent evolutionary paths from a less olfaction-specialized ancestor" (Ashwell, 2012). Nevertheless, as in Tupaia belangeri, a terminal nerve including ganglia is present already prior to birth.…”

Sound production by the short‐beaked echidna (Tachyglossus aculeatus)

“…We provide here unequivocal evidence for vocalization by short‐beaked echidnas, describing five separate observations of echidnas producing sound and identifying four sound types. Two of these sounds (exhalations and wheezes) are likely inadvertent consequences of moving air through the respiratory system, possibly to facilitate olfaction which is an important sensory system for echidnas (Ashwell, 2012). The other two sounds were vocalizations (sounds other than by‐products of breathing or moving), that is, tones that can be described as a dove‐like ‘coo’ and a previously unreported lower frequency grunt.…”