Distinct Development of Peripheral Trigeminal Pathways in the Platypus <i>(Ornithorhynchus anatinus)</i> and Short-Beaked Echidna <i>(Tachyglossus aculeatus)</i>

Abstract

The extant monotremes (platypus and echidnas) are believed to all be capable of electroreception in the trigeminal pathways, although they differ significantly in the number and distribution of electroreceptors. It has been argued by some authors that electroreception was first developed in an aquatic environment and that echidnas are descended from a platypus-like ancestor that invaded an available terrestrial habitat. If this were the case, one would expect the developmental trajectories of the trigeminal pathways to be similar in the early stages of platypus and short-beaked echidna development, with structural divergence occurring later. We examined the development of the peripheral trigeminal pathway from snout skin to trigeminal ganglion in sectioned material in the Hill and Hubrecht collections to test for similarities and differences between the two during the development from egg to adulthood. Each monotreme showed a characteristic and different pattern of distribution of developing epidermal sensory gland specializations (electroreceptor primordia) from the time of hatching. The cross-sectional areas of the trigeminal divisions and the volume of the trigeminal ganglion itself were also very different between the two species at embryonic ages, and remained consistently different throughout post-hatching development. Our findings indicate that the trigeminal pathways in the short-beaked echidna and the platypus follow very different developmental trajectories from the earliest ages. These findings are more consistent with the notion that the platypus and echidna have both diverged from an ancestor with rudimentary electroreception and/or trigeminal specialization, rather than the contention that the echidna is derived from a platypus-like ancestor.

Quantitative Analysis of the Timing of Development of the Cerebellum and Precerebellar Nuclei in Monotremes, Metatherians, Rodents, and Humans

“…The 33 monotreme embryos, hatchlings, and juveniles (22 platypuses, Ornithorhynchus anatinus ; 11 short‐beaked echidnas, Tachyglossus aculeatus ) are held at the MfN or the AMNH and have been used in previous studies of the development of the monotreme nervous system and brainstem by our group (Ashwell, ; Ashwell et al, ; Ashwell and Hardman, ). The AMNH specimens had been kindly made available by Professor U. Zeller (previously of MfN).…”

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

“…The 31 monotreme embryos, hatchlings and juveniles (21 platypuses, Ornithorhynchus anatinus ; 10 short‐beaked echidnas, Tachyglossus aculeatus ) are held at the MfN or the AMNH and have been used in previous studies of the development of the monotreme nervous system and brainstem by our group (Ashwell and Hardman, ; Ashwell et al, ). The AMNH specimens had been kindly made available by Professor U Zeller, formerly of MfN.…”

Distinct Development of the Trigeminal Sensory Nuclei in Platypus and Echidna

“…Manger et al [1998b] have reported that electroreceptors begin to emerge on the surface of the platypus bill around 10 days after hatching, but they did not have the opportunity to examine sections of pre-hatching platypus. We recently showed that the peripheral trigeminal pathways of platypus and echidna are morphologically distinct from the earliest stages of the skin receptor, trigeminal nerve and ganglion differentiation, even before hatching [Ashwell et al, 2012]. In the case of the peripheral receptors, distinctive features of the two species emerge during the last third of incubation, but differences in the size of the trigeminal ganglion are evident even earlier, by the first third of incubation.…”