Neurobiology of Monotremes

Brain Evolution in Our Distant Mammalian Cousins

Ken Ashwell

• Publisher: CSIRO PUBLISHING
• Year: 2013
• Print ISBN: 9780643103115
• eBook ISBN: 9780643103160
• Topic: Scienze biologiche
• Subtopic: Evoluzione

Neurobiology of Monotremes brings together current information on the development, structure, function and behavioural ecology of the monotremes. The monotremes are an unusual and evolutionarily important group of mammals showing striking behavioural and physiological adaptations to their niches. They are the only mammals exhibiting electroreception (in the trigeminal sensory pathways) and the echidna shows distinctive olfactory specialisations.

The authors aim to close the current gap in knowledge between the genes and developmental biology of monotremes on the one hand, and the adult structure, function and ecology of monotremes on the other. They explore how the sequence 'embryonic structure › adult structure › behaviour' is achieved in monotremes and how this differs from other mammals.

The work also combines a detailed review of the neurobiology of monotremes with photographic and diagrammatic atlases of the sectioned adult brains and peripheral nervous system of the short-beaked echidna and platypus. Pairing of a detailed review of the field with the first published brain atlases of two of the three living monotremes will allow the reader to immediately relate key points in the text to features in the atlases and will extend a universal system of brain nomenclature developed in eutherian brain atlases by G Paxinos and colleagues to monotremes.

1

Classification and evolution of the monotremes

A. M. Musser

Summary

The higher taxon Monotremata includes the extant platypuses and echidnas as well as their extinct relatives. Living monotremes are highly specialised animals occupying distinct ecological niches, and are known only from Australia and New Guinea. Platypuses are semi-aquatic insectivores/carnivores, and echidnas are spine-covered, terrestrial insectivores. There has been extensive interest in and debate over monotreme origins since their discovery by western science in the late 1800s. Monotremes lay soft-shelled eggs from which the embryonic young hatch, in contrast to marsupial and placental mammals that bear live young. The many ‘primitive’ (plesiomorphic) features of monotremes occur in concert with unique specialisations, a phenomenon known as ‘mosaic evolution’. Monotreme taxonomy and classification have been confounded in part by this mosaic of features, and in part from a dearth of adequate comparative material. However, new discoveries of early mammals and near-mammals and development of cladistic methodologies for determining relationships have shed much-needed light on monotreme origins. Australosphenidans – recently discovered Mesozoic mammals from the Southern Hemisphere with tribosphenic-like teeth – may share a unique relationship with monotremes, and higher level classification schemes have followed based on this presumption, although the debate is far from resolved. Research into unique monotreme attributes – in particular, an electrosensory ability unknown in other mammals – will help science understand the success and longevity of this oldest of mammalian groups.

Introduction

Living monotremes include a single species of platypus, Ornithorhynchus anatinus (Ornithorhynchidae); and two genera of echidnas (Tachyglossidae) in four species: the long-beaked Zaglossus (three species) and the short-beaked Tachyglossus (a single species with several subspecies) (see below). Ornithorhynchus is a semi-aquatic insectivore/carnivore that feeds primarily on benthic invertebrates, restricted to the waterways of eastern Australia (including Tasmania but excluding northern Queensland). Echidnas are terrestrial insectivores, feeding on ants, termites and other soft-bodied invertebrates. The short-beaked echidna Tachyglossus aculeatus is found in all Australian states as well as in New Guinea, in areas with suitable habitat. Until very recently, long-beaked Zaglossus species were thought to have survived only in New Guinea, although mainland Australian Zaglossus fossil material is known from the Pleistocene and Holocene. A skin and skull of what appears to be an overlooked museum specimen of Zaglossus bruijnii, however, has been reported from a collection made in 1901 at Mount Anderson in the West Kimberley region of Western Australia; this remarkable find suggests that Zaglossus survived until at least the early 20th century in this isolated area of WA, and has raised hopes that Australian Zaglossus may still be extant (Helgen et al. 2012).

Monotremes are the only extant egg-laying mammals, pointing to origins deep within the mammalian tree. Features shared by monotremes and other living mammals include the presence of hair or fur, and the ability to produce milk to feed their young, suggesting that these attributes appeared early in mammalian evolution. Such features, however, may also have been present in the small, advanced cynodont reptiles that were the direct ancestors of mammals, and in the Late Triassic–Early Jurassic ‘mammaliaforms’ – early lineages of mammal-like taxa that lacked ‘advanced’ features of later therian mammals like marsupials and placentals.

Monotremes have their origins in the Mesozoic, the era comprised of the Triassic, Jurassic and Cretaceous periods. Mesozoic mammals or near-mammals, however, are almost always found as fragmentary fossils, often known only from small jaws and teeth (although this situation has dramatically improved over the past decade). Determining relationships from incomplete fossil taxa in order to understand monotreme phylogeny has been an ongoing exercise involving anatomists, palaeontologists and molecular biologists. To this writer, at least, it is a debate that has not yet been resolved.

Monotremes have traditionally been thought of as uniquely and quintessentially Australian (inclusive of New Guinea). However, a large ornithorhynchid species (Monotrematum americanum) is now known from the Paleocene of Patagonia in southern South America (Pascual et al. 1992a, b). This occurrence suggests an eastern Gondwanan distribution possibly from the late Mesozoic through earliest Cenozoic encompassing Australia, South America and, by inference, Antarctica (the land connection between Australia and Patagonia throughout much of this time period). Ornithorhynchids are therefore Gondwanan species with a relictual distribution in eastern Australia.

As we will see, the known evolutionary history of monotremes is lengthy, unique and in many ways surprising, extending back over 100 million years and encompassing at least three continents. Living monotremes are therefore relict species, and platypuses and echidnas may be but two long-separate branches of a larger, deeply rooted family tree.

Basic monotreme anatomy and physiology

The ‘primitive’ (plesiomorphic) features found in ornithorhynchids and tachyglossids have generated a great deal of debate over the place of monotremes in mammalian evolution, and whether monotremes are in fact fully mammalian as traditionally defined (see Musser 2006a, b for a review of relationship hypotheses). Egg-laying would almost certainly have been the plesiomorphic mammalian reproductive condition. Later therian mammals bore live young (e.g. altricial young in Marsupialia and well-developed young nourished by a placenta in Placentalia). The body temperature of monotremes is lower than that of therian mammals and may be variable, a physiological feature often cited as plesiomorphic and somewhat reptilian (e.g. Augee et al. 2006). Plesiomorphic osteological features include skull features such as paired pilae antoticae, which are ossifications in the skull floor along the sella turcica as in Sauropsida (among Mammalia, this is found only in monotremes); retention of a large septomaxilla, a bone of the snout found almost exclusively in pre-mammalian taxa; and absence of a bony auditory bulla. Plesiomorphic postcranial features include the retention of additional bones of the shoulder girdle in both monotremes (lost in therian mammals), the morphology of the humerus in living monotremes, and the archaic form of the femur in ornithorhynchids, almost identical to that of the pre-mammalian cynodont Tritylodon. The bones of the mammalian middle ear (malleus, incus and stapes), developed from the accessory jaw bones of pre-mammalian ancestors, were apparently not incorporated into the middle ear in early monotremes, which instead had a ‘pre-mammalian’ ear/jaw apparatus with at least some comparatively unreduced accessory jaw bones (Rich et al. 2005).

An unusual plesiomorphic feature once thought to be a monotreme autapomorphy is the presence of a crural (extratarsal) spur on the inner side of the ankle in both living monotreme families, comprised of an os calcaris and cornu calcaris (generally functional and venomous only in male Ornithorhynchus). Extratarsal spurs are found in some basal Mesozoic mammals, including eutriconodonts, symmetrodonts and multituberculates but not, as far as known, in either pre-mammalian Cynodontia or Theria (Hurum et al. 2006). The presence of ankle spurs may therefore be a basal mammalian feature – possibly a defence against such threats as dinosaurian predators – retained in monotremes but lost or never possessed in crown therians (Hurum et al. 2006).

Certain anatomical and physiological features of monotremes are highly sophisticated, relating to the great degree of specialisation in both living families and their ancestors. Perhaps the most remarkable specialisation is a sensory system incorporating both electroreceptors and mechanoreceptors in the skin of the beak or bill (e.g. Scheich et al. 1986; Pettigrew 1999). These sensory receptors need a moist environment in which to function optimally; the platypus operates in an aquatic environment, keeping the bill wet while feeding, whereas the tip of the beak in echidnas is kept moistened by mucus.

The electroreceptive system of the platypus is by far the most highly developed, and is critical to the navigational skills of the platypus as it finds its way through dark or turbid waterways. It is tempting to think of the extent of development of the electrosensory organs in ornithorhynchids as an ancient adaptation to the prolonged winter darkness of the southern polar regions during the early evolution of the group. This electro/mechanoreception is present but much less well-developed in the terrestrial tachyglossids, and receptors are concentrated at the tip of the beak.

The development of electroreception/mechanoreception is correlated with enlargement of the trigeminal nerve (5n), which passes to the bill or beak through foramina on the rostrum and via the mandibular canal (e.g. Manger 1994). The presence of an enlarged or hypertrophied mandibular canal is a key monotreme synapomorphy that may identify fossil taxa as either belonging within Monotremata (e.g. the Early Cretaceous Victorian monotreme Teinolophos trusleri, which has an enlarged mandibular canal: Rich et al. 2005) or excluded from Monotremata (e.g. the Early Cretaceous Kollikodon ritchiei from Lightning Ridge, New South Wales, which lacks an enlarged mandibular canal: Musser 2003, 2006a, b) (Fig. 1.1).

Monotreme evolution and diversification

Among extant monotremes, platypuses appear to be the older and more archaic type despite their aquatic specialisations. Ornithorhynchids have retained a greater number of plesiomorphic characters (see Musser 2006a, b), and their fossil history extends back to the earliest Paleocene (61–63 million years ago (mya)) (Pascual et al. 1992a, b). In addition, platypus-like monotremes are known from the Early Cretaceous of Australia (115–108 mya) (Archer et al. 1985). In contrast, the oldest echidna fossils are currently thought to be Miocene in age (no older than 15 million years old), and may in fact be much younger (see Musser 2006a, b).

Aquatic adaptations in Ornithorhynchus include a dorsoventrally flattened body, waterproof fur, webbed feet and a large bill comprised of soft skin richly imbued with mechano- and electroreceptors (Fig. 1.2a). Ornithorhynchus spends most of its waking hours foraging along the bottom of rivers, streams and lakes feeding on benthic invertebrates. Its habitat is generally limited to waterways, surrounding banks and river bottoms (platypuses may ...

Table of contents

• Cover
• Dedication
• Title Page
• Copyright
• Contents
• List of contributors
• Preface
• Acknowledgements
• 1 Classification and evolution of the monotremes (A. M. Musser)
• 2 Behaviour and ecology of monotremes (Stewart C. Nicol)
• 3 Embryology and post-hatching development of the monotremes (Ken W. S. Ashwell)
• 4 Overview of monotreme nervous system structure and evolution (Ken W. S. Ashwell)
• 5 Peripheral nervous system, spinal cord, brainstem and cerebellum (Ken W. S. Ashwell)
• 6 Diencephalon and deep telencephalic structures (Ken W. S. Ashwell)
• 7 Cerebral cortex and claustrum/endopiriform complex (Ken W. S. Ashwell)
• 8 Visual system (Ken W. S. Ashwell)
• 9 Somatosensory and electrosensory systems (Ken W. S. Ashwell and Craig D. Hardman)
• 10 Auditory and vestibular systems (Ken W. S. Ashwell)
• 11 Chemical senses: olfactory and gustatory systems (Ken W. S. Ashwell)
• 12 The hypothalamus, neuroendocrine interface and autonomic regulation (Ken W. S. Ashwell)
• 13 Monotremes and the evolution of sleep (Ken W. S. Ashwell)
• 14 Reflections: monotreme neurobiology in context (Ken W. S. Ashwell)
• 15 Atlas and tables of peripheral nervous system anatomy (Ken W. S. Ashwell and Anne M. Musser)
• 16 Atlas of the adult and developing brain and spinal cord of the short-beaked echidna (Tachyglossus aculeatus aculeatus) (Ken W. S. Ashwell and Craig D. Hardman)
• 17 Atlas of the adult and developing brain of the platypus (Ornithorhynchus anatinus) (Ken W. S. Ashwell and Craig D. Hardman)
• List of abbreviations used in brain and embryo atlas plates
• Index of brain and embryo atlas plates
• References
• Glossary
• Appendix tables and figures
• Index