The unique paired retinal vascular pattern in marsupials: structural, functional and evolutionary perspectives based on observations in a range of species

Abstract

Background: In the few marsupial species studied to date that possess a retinal vasculature, the arterial and venous segments, down to the smallest calibre capillaries, have been shown to occur in pairs. This unique pattern of retinal vasculature has been described in only a few marsupial species. It is a pattern seen in the marsupial central nervous system (CNS) but not in other tissues in this group or in any tissues in eutherian mammals. The aim of the present study was to investigate the presence of retinal vessels in a range of non-eutherian mammalian species (marsupials and monotremes) and to determine if the pattern of paired vessels was a widespread phenomenon within this animal group.

Methods: Species studied included a monotreme, the short-billed echidna (Tachyglossus aculeatus) and a range of Australian marsupials, the honey possum (Tarispedidae rostratus), fat-tailed dunnart (Sminthopsis crassicaudata), grey-bellied dunnart (Sminthopsis griseoventer), numbat (Myrmecobius fasciatus), broad-footed marsupial mouse (Antechinus godmani) and the North American opossum (Didelphis virginiana). Eyes were fixed in glutaraldehyde or paraformaldehyde and retinae were embedded in resin for light and electron microscopic analysis.

Results: Examination revealed that in those species with retinal vessels (fat-tailed dunnart, grey-bellied dunnart, numbat, marsupial mouse, North American opossum) the pattern of vessels differs from the conventional plexus-like arrangement of mammalian retinal vasculature (i.e. anastomotic networks of capillaries between arterioles and venules). By contrast, in marsupials retinal vessels always occur in closely related pairs with the arteriolar limb usually situated on the vitread aspect. Vessels penetrate the retina and branch to form layers of paired capillaries as far as the outer nuclear layer in some species, which is considerably deeper than in normal mammalian holangiotic retinae. The capillaries form blind-ended hairpin loops and display classical morphological features of CNS capillaries. The vascular endothelium is supported by a distinct basal lamina that splits to envelop pericytes. The latter, although abundant, are invariably interposed between the two vessels that form each vascular unit.

Conclusion: The phylogenetic relations of this vascular pattern in the marsupial CNS and retina, and in the CNS of a few other classes of non-mammalian vertebrates, suggest that retinal vascularisation may have evolved independently in marsupial and eutherian mammals and that the former may have evolved from a common primitive mammal-like reptilian ancestor which possessed paired vasculature in the CNS. Eutherian mammals may have evolved from an ancestor with anastomotic networks in the CNS or this pattern may have evolved later in eutherian mammal evolutionary radiation. The possible functional and physiological significance of the paired vessels is discussed.