Evolution of the brain and sensory systems of the kiwi

Abstract

Kiwi (Apteryx spp.) have evolved under unique evolutionary pressures and uniquely occupy a nocturnal, ground-dwelling niche. They share few traits with other birds: they have small eyes, an elongated bill, and several features more characteristic of mammals. Early anatomical studies described a number of unique features in the kiwi brain, but their relevance to the behaviour and ecology of the species was not clearly established. This study aims to describe the structure of the primary cranial sensory systems of kiwi and comment on the evolutionary pressures that may have shaped their current form. The external morphology and relatively large size of the brain of kiwi, in particular those of the telencephalon, contrast with those of other Palaeognaths. The relative size of the cerebral hemispheres is rivalled only by a handful of parrots and songbirds. This enlargement results from a differential enlargement of the nidopallium, mesopallium and, to a lesser extent, of the basal ganglia. In other birds these regions are associated with the integration of information, cognition and learning. Kiwi brain centres processing visual information were small, although the retina structure showed an adaptation to dim light. The olfactory and trigeminal systems associated with the bill were hypertrophied. The auditory system shows specialisations associated with an overrepresentation of high frequency coding areas that originates in the cochlea and is preserved throughout the auditory brainstem. In absolute terms, the upper frequency response limit, based on hair cell morphology, is estimated to be about 5 kHz, the lower limit to be about 500 Hz, with a slightly higher frequency range predicted from the morphology of central auditory structures. The organisation of both nucleus angularis (NA) and nucleus laminaris (NL) in kiwi suggest that the central auditory system has retained the ancestral organisation except for the morphological features associated with the overrepresentation of high frequencies. Overall, the brain and sensory structures of kiwi have evolved neural adaptations that accompany the very different behavioural strategies associated with the unique niche the birds occupy. A large telencephalic size and shift away from vision towards an increased reliance on olfactory, tactile and auditory cues constitute a collection of features that make kiwi unique among birds. These findings provide a unique glimpse of the evolutionary history that has led to this unusual design, in particular, and challenge many of our current views about the evolution of brains and encephalisation, in general.