ArticlePublisher preview availableLiterature Review

The nocturnal bottleneck and the evolution of activity patterns in mammals

Proceedings of the Royal Society B

August 2013
280(1765):20130508

DOI:10.1098/rspb.2013.0508

Source
PubMed

Authors:

Menno Gerkema

University of Groningen

Russell G Foster

University of Oxford

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In 1942, Walls described the concept of a 'nocturnal bottleneck' in placental mammals, where these species could survive only by avoiding daytime activity during times in which dinosaurs were the dominant taxon. Walls based this concept of a longer episode of nocturnality in early eutherian mammals by comparing the visual systems of reptiles, birds and all three extant taxa of the mammalian lineage, namely the monotremes, marsupials (now included in the metatherians) and placentals (included in the eutherians). This review describes the status of what has become known as the nocturnal bottleneck hypothesis, giving an overview of the chronobiological patterns of activity. We review the ecological plausibility that the activity patterns of (early) eutherian mammals were restricted to the night, based on arguments relating to endothermia, energy balance, foraging and predation, taking into account recent palaeontological information. We also assess genes, relating to light detection (visual and non-visual systems) and the photolyase DNA protection system that were lost in the eutherian mammalian lineage. Our conclusion presently is that arguments in favour of the nocturnal bottleneck hypothesis in eutherians prevail.

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Review

Cite this article: Gerkema MP, Davies WIL,

Foster RG, Menaker M, Hut RA. 2013 The

nocturnal bottleneck and the evolution of

activity patterns in mammals. Proc R Soc B

280: 20130508.

http://dx.doi.org/10.1098/rspb.2013.0508

Received: 25 February 2013

Accepted: 3 June 2013

Subject Areas:

behaviour, neuroscience, palaeontology

Keywords:

eutherian, bottleneck, activity, vision,

photolyases, endothermia

Author for correspondence:

Menno P. Gerkema

e-mail: m.p.gerkema@rug.nl

One contribution to a Special Feature ‘Animal

clocks: when science meets nature’.

The nocturnal bottleneck and the

evolution of activity patterns in mammals

Menno P. Gerkema1, Wayne I. L. Davies2,3, Russell G. Foster2,

Michael Menaker4and Roelof A. Hut1

Centre for Behaviour and Neuroscience, Department of Chronobiology, University of Groningen, Groningen,

The Netherlands

Nuffield Laboratory of Ophthalmology, University of Oxford, Oxford OX3 9DU, UK

School of Animal Biology, University of Western Australia, Perth, Western Australia 6009, Australia

Department of Biology, University of Virginia, Charlottesville, VA 22904 4328, USA

In 1942, Walls described the concept of a ‘nocturnal bottleneck’ in placental

mammals, where these species could survive only by avoiding daytime

activity during times in which dinosaurs were the dominant taxon. Walls

based this concept of a longer episode of nocturnality in early eutherian

mammals by comparing the visual systems of reptiles, birds and all three

extant taxa of the mammalian lineage, namely the monotremes, marsupials

(now included in the metatherians) and placentals (included in the euther-

ians). This review describes the status of what has become known as the

nocturnal bottleneck hypothesis, giving an overview of the chronobiological

patterns of activity. We review the ecological plausibility that the activity

patterns of (early) eutherian mammals were restricted to the night, based

on arguments relating to endothermia, energy balance, foraging and preda-

tion, taking into account recent palaeontological information. We also assess

genes, relating to light detection (visual and non-visual systems) and the

photolyase DNA protection system that were lost in the eutherian mamma-

lian lineage. Our conclusion presently is that arguments in favour of the

nocturnal bottleneck hypothesis in eutherians prevail.

A more likely view is that the placental mammals had an early history of strict

nocturnality.

...what was the retina like in these strictly nocturnal ‘bottle-neck’insectivores? [1, p. 687]

1. Introduction

A general view that early mammals were small insectivores, living on trees and

being only night active, has become commonplace in textbooks, with some

articles devoted specifically to vision [1,2], whereas others are more general

in nature [3,4]. Menaker and co-workers formulated a specific ‘nocturnal bottle-

neck hypothesis’ [5– 7], although some researchers have suggested the

involvement of a period of mesopia (medium-light levels) in the evolution of

eyes in response to light-restricted habitats [8], as observed in other species

(e.g. birds; [9]). The main focus of this review is the ‘nocturnal bottleneck’ con-

jecture that was inspired by the fact that mammals have only one (retinal)

photic input pathway to their circadian pacemaker system, whereas non-

mammalian species have several parallel retinal and extra-retinal circadian

photic input systems (e.g. hypothalamus, pineal gland, parietal eye). Further

evidence to support the hypothesis arose from consistent findings in mamma-

lian evolution, including the evolution of endothermia [3,10] and the adaptation

of photosensory systems (e.g. the loss of photoreceptor pigments: [7,8]).

The nocturnal bottleneck hypothesis suggests that early eutherian mammals

faced competition with diurnal reptiles (e.g. dinosaurs) during the Mesozoic

era: [1,6,11,12]. Thought to be mainly ectothermic, these reptiles would have

had to restrict their activity to the daytime because solar radiation was essential

to increase their body temperature to operational levels [13]. Predation pressure

and inter-species competition are thought to have stimulated the development

of endothermia, a major adaptive change that enabled early mammals to

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