Quantitative Analysis of the Maturation of the Main and Accessory Olfactory Systems in Monotremes and Metatherians in Comparison to Rodents and Humans.

We have used an unbiased statistical approach to compare the pace of development in the main and accessory olfactory systems in monotremes and metatherians with that in rodents and humans. We hypothesized that if metatherians and monotremes, which are born at small body size, use olfaction to locate the pouch and/or teat/milk field, then olfactory structures should reach structural maturity in metatherians and monotremes at a smaller size than eutherians like humans and rodents. The achievement of key structural milestones in the development of the main and accessory olfactory systems (11 and 7 milestones, respectively) was scored for 354 specimens and compared against a measure of general somatic growth (body length). We used a statistical approach adapted from Kaplan-Meier analysis to determine median body length at which structural milestones were achieved, and to test the differences for statistical significance (Braslow statistic). The laboratory mouse achieved most main olfactory milestones at a smaller body size than all the metatherians and the monotremes, although the dasyurids (which are born at only 5.0 mm) and mouse achieved accessory olfactory milestones at similar body length. All other metatherians and monotremes reached olfactory milestones at body lengths similar to or larger than the laboratory rat. We therefore reject the hypothesis that metatherians and monotremes as a group exhibit advanced development of the olfactory pathways relative to body size. The findings suggest that, if olfaction is used by metatherians and monotremes at birth, it is achieved with only a rudimentary system without structurally mature central components. Anat Rec, 301:1258-1275, 2018. © 2018 Wiley Periodicals, Inc.