A neuroanatomical evaluation of cholinergic,catecholaminergic, serotonergic and orexinergic neural systems in mammals pertaining to the phylogenetic affinities of the Chiroptera
Date
2015
Authors
Calvey, Tanya
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Abstract
One of the few remaining mysteries in mammalian phylogeny is the issue of Chiropteran
phylogeny. In order to further investigate the diphyletic hypothesis that states that
Megachiroptera evolved from primate-like gliders and that Microchiroptera evolved from
insectivores, the cholinergic, catecholaminergic, serotonergic and orexinergic systems were
analyzed in, not only five insectivores (Crocidura cyanea, Crocidura olivieri, Sylvisorex ollula,
Paraechinus aethiopicus and Atelerix frontalis) and three prosimian primates (Galagoides
demidoff, Perodicticus potto and Lemur catta), but in species from other orders of interest
including the Afrotheria (Potamogale velox, Amblysomus hottentotus and Petrodromus
tetradactylus), Lagomorpha (Lepus capensis) and Scandentia (Tupaia belangeri). Brains of the
mammals were coronally sectioned and immunohistochemically stained with antibodies against
cholineacetyltransferase, tyrosine hydroxylase, serotonin and orexin-A. The presence or absence
of 93 nuclei within these neuromodulatory systems was entered into modern cladistics software
for analysis of the 13 studied species, as well as an additional 40 previously studied mammals.
The majority of nuclei revealed in the current study were similar among the species investigated
and to mammals generally, but certain differences in the nuclear complement highlighted
potential phylogenetic interrelationships. The Afrotherian, A. hottentotus, presented unusual
cholinergic interneurons in the cerebral cortex, hippocampus, olfactory bulb and amygdala, and
exhibited an unusual foreshortening of the brain, such that a major mesencephalic flexure in the
brainstem was evident. The Afrotherian, P. tetradactylus, lacked the catecholaminergic A15d
nucleus as in a previously studied member of Macroscelididae. The three Insectivoran shrews
lacked the cholinergic parabigeminal and Edinger-Westphal nuclei, had a mediodorsal arch of
the cholinergic laterodorsal tegmental nucleus, lacked the catecholaminergic A4 and A15d nuclei
and presented an incipient ventral division of the substantia nigra which is identical to previously
studied Microchiroptera. All three prosimians presented a central compact division of
catecholaminergic locus coeruleus (A6c) surrounded by a shell of less densely packed (A6d)
tyrosine hydroxylase immunopositive neurons. This combination of compact and diffuse
divisions of the locus coeruleus complex is only found in primates and Megachiropterans of all
the mammalian species studied to date. T. belangeri of the Scandentia contained ChAT+ neurons
within the nucleus of the trapezoid body as well as the superior olivary nuclear complex, which
has not been described in any mammal studied to date. L. capensis of the Lagomorpha presented
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the rodent specific rostral dorsal midline medullary nucleus (C3), while T. belangeri was lacking
both the ventral and dorsal divisions of the anterior hypothalamic group (A15v and A15d), and
both species were lacking the primate/Megachiropteran specific compact portion of the locus
coeruleus. Our neuroanatomical analysis suggests a phylogenetic relationship between the
Soricidae (shrews) and the Microchiropterans, supports the phylogenetic grouping of primates
with Megachiropterans, confirms previous molecular evidence of the relationship between
lagomorphs and rodents within the super-order Glires, and suggests that primates are
phylogenetically closer to Megachiroptera than to any members of the Euarchontoglires. The
cladistic analysis confirmed the neuroanatomical analysis with the most parsimonious tree
placing Megachiroptera into the Euarchontoglires as a sister group to primates and the
Microchiroptera next to Soricidae within the Laurasiatheria.