Bats and Viruses

A New Frontier of Emerging Infectious Diseases

Lin-Fa Wang, Christopher Cowled, Lin-Fa Wang, Christopher Cowled

• Publisher: Wiley-Blackwell
• Year: 2015
• ISBN:
  9781118818725
• Edition: 1
• Topic: Biological Sciences
• Subtopic: Microbiology & Molecular Biology
• Index: Biological Sciences

Approximately 75% of emerging infectious diseases are zoonoses, and the rate of emergence of zoonotic diseases is on the rise. Bats are being increasingly recognised as an important reservoir of zoonotic viruses of different families, including SARS coronavirus, Nipah virus, Hendra virus and Ebola virus. Understanding bats' role in emerging zoonotic diseases is crucial to this rapidly expanding area of research.

Bats and Viruses: A New Frontier of Emerging Infectious Diseases provides an updated overview of research focusing on bat biology and the role bats play as hosts of many major zoonotic viruses. The text covers bat biology, immunology, and genomics. Chapters also delve into the various major bat-borne virus families, including lyssaviruses, paramyxoviruses, coronaviruses, filoviruses and reoviruses, among others.

Edited by leaders in the field, Bats and Viruses: A New Frontier of Emerging Infectious Diseases is a timely, invaluable reference for bat researchers studying microbiology, virology and immunology, as well as infectious disease workers and epidemiologists, among others.

1
THE UNIQUENESS OF BATS

Paul A. Racey

Centre for Ecology and Conservation, University of Exeter, Cornwall Campus, Penryn, UK

1.1 INTRODUCTION

The aim of this chapter is to provide an overview of the distinctive features of bats, many of which are unique among mammals, and in particular to highlight features of their biology that may have some bearing on the high prevalence of viruses in this group (Luis et al., 2013).

Bats are the only mammals with the capacity for powered flight. The associated skeletal adaptations of elongated forelimb bones were fully developed in the first fossil bat Icaronycteris index 50 million years ago, discovered in the Green River formation in Wyoming, USA (Jepsen, 1966, 1970). Also evident were auditory bullae at the base of the cranium, indicating the presence of large cochlea, associated with echolocation, which enabled bats to fly in darkness. Flight and echolocation allowed bats to occupy and eventually dominate the nocturnal aerial feeding niche where they are relatively free of competitors and predators. Among the exceptions are caprimulgid birds (nightjars and goatsuckers), an Old World bat hawk and a New World bat falcon. Owls cannot match the flight agility of bats, although they are opportunist predators at roosts (Fenton & Fleming, 1976).

From the same Eocene fossil beds in Wyoming, Simmons et al. (2008) described Onychonycteris finneyi, of similar age to Icaronycteris index but more primitive, in that its limb bones are intermediate in proportion between terrestrial mammals and other Eocene bats. The cochlea is also smaller indicating that echolocation was either less well developed or absent, supporting the view that flight evolved before echolocation. However, in the absence of a more extensive fossil record, the evolutionary history of bats from a small terrestrial shrew-like early mammal of the Triassic to the fossil bats found 150 million years later is a matter of speculation. The most plausible hypothesis is that bats evolved from a species similar to modern day tree shrews, in which the limbs and digits became connected by folds of skin and the forelimbs became elongated to form an aerofoil (Smith, 1977; Hill & Smith, 1984). Jumping from branch to branch led to gliding and eventually to flapping flight.

With 1301–1331 species (January 2014, N.B Simmons, Pers. Comm.; Simmons, 2015) bats are the second largest order of mammals, and the number of species continues to rise as new ones are described or the taxonomy of particular genera is reviewed. Nevertheless, bats continue to account for about a fifth of all mammals because the same processes are happening in the largest order of mammals, the rodents, which has about twice as many species as bats. Bats are distributed throughout the world, with the exception of some isolated oceanic islands such as Tahiti and the polar regions, although they breed inside the Arctic Circle (Rydell, 1989). However, although there are twice as many bat species in the Old as in the New World, bats achieve their greatest species richness in South America (Hutson et al., 2001; Jones et al., 2009). Regardless of continent or scale, latitudinal gradients of richness are qualitatively similar and species number increases with decreasing latitude and decreases with increasing elevation (Willig et al., 2003). Family-level species richness varies greatly, from one and two species in the Craseonycteridae and Myzopodidae respectively to more than 300 species in the Vespertilionidae (Simmons & Conway, 2003).

Historically, bats were divided into two suborders: the Megachiroptera consisted of a single family, the Pteropodidae – Old World vegetarians with large eyes, which do not echolocate; and the Microchiroptera with 16 families of echolocating and mainly insectivorous bats. Recent phylogenetic analysis has revised the classification of bats, and two new suborders have replaced the old: The Yinpterochiroptera consisting of the Pteropodidae and five other families grouped within the superfamily Rhinolophoidea; and the Yangochiroptera, with three superfamilies – the Emballonuroidea, the Vespertilionoidea and the Noctilionoidea, comprising a total of 13 families (Teeling et al., 2005).

1.2 FLIGHT

The ability to glide by extending flaps of skin between the limbs has evolved several times among mammals, in the marsupial sugar gliders and flying phalangers of Australia and New Guinea, in placental mammals like flying squirrels and colugos of Asia, and anomalures of Africa. Bats are unique, however, in their capacity for powered flight. All forelimb bones in bats are elongated, although the ulna no longer extends to the wrist and is vestigial, so pronation and supination (turning about the elbow) is no longer possible nor desirable. Digit one – the thumb – is free and clawed and is important for climbing and grooming, and in some cases for aggression. Digits two and three are generally close together and form the rigid leading edge of the aerofoil. Digits four and five support the wing membrane or patagium, which consists of a double layer of skin, well provided with elastic tissue so that it can change shape in flight but retracts and folds at rest. The hind limbs are also elongated, attached to the patagium and involved in steering. They are generally joined to the tail by the interfemoral membrane which is sometimes used in prey capture. The overall flexibility of the wing means that some bats have a unique flying attribute – the ability to carry out stall turns – to rotate through 90° in their own body length.

In contrast to birds, where most power for flight comes from two muscles – the pectoralis and the supracoracoideus working antagonistically – flight in bats is powered by nine pairs of muscles, mainly abductors and adductors, concentrated towards the midline (in contrast to the situation in terrestrial mammals where the flexors and extensors of the limbs power locomotion). In birds the muscles that elevate and depress the wings are on the ventral surface, whereas in bats the elevators are dorsal and the depressors are ventral. The keel on the sternum of bats is much less prominent than in birds. The muscles responsible for opening and closing the wing are also situated in the proximal parts of the forelimb and their power is transmitted by extended tendons. The wing opens and closes in one plane and twisting is eliminated. The clavicle braces the shoulder joint against the axial skeleton, in contrast to the situation in birds where the coracoid provides a more rigid brace.

Although the hind limbs may be elongated, the pelvic girdle is reduced compared with the pectoral girdle, and the diameter of the birth canal is reduced. However, across the pubic symphysis, the interpubic ligament joins the pubic bones ventrally, and can expand to increase the diameter of the birth canal from 2 to 35 mm in Tadarida brasiliensis. This expansion is under the influence of the hormone relaxin (Crelin, 1969). The hind limbs have become rotated by 90° in many bats, although they have retained the ability for terrestrial locomotion, sometimes impressively so (Lawrence, 1969; Ris...