AV06CH02_Teeling ARI 23 January 2018 7:16
Annual Review of Animal Biosciences
Bat Biology, Genomes, and the
Bat1K Project: To Generate
Chromosome-Level Genomes
for All Living Bat Species
Emma C. Teeling,
1
Sonja C. Vernes,
2,3
Liliana M. D
´
avalos,
4
David A. Ray,
5
M. Thomas P. Gilbert,
6,7
Eugene Myers,
8
and Bat1K Consortium
∗
1
School of Biology and Environmental Science, University College Dublin, Belfield, Dublin 4,
Ireland; email: emma.teeling@ucd.ie
2
Neurogenetics of Vocal Communication Group, Max Planck Institute for Psycholinguistics,
Nijmegen, 6500 AH, The Netherlands
3
Donders Centre for Cognitive Neuroimaging, Nijmegen, 6525 EN, The Netherlands
4
Department of Ecology and Evolution, Stony Brook University, Stony Brook, New York
11794-5245, USA
5
Department of Biological Sciences, Texas Tech University, Lubbock, Texas 79409, USA
6
Natural History Museum of Denmark, University of Copenhagen, 1350 Copenhagen, Denmark
7
University Museum, Norwegian University of Science and Technology, 7491 Trondheim,
Norway
8
Max Planck Institute for Molecular Cell Biology and Genetics, 01307 Dresden, Germany
∗
Full list of Bat1K Consortium members in Supplemental Appendix
Annu. Rev. Anim. Biosci. 2018. 6:23–46
First published as a Review in Advance on
November 20, 2017
The Annual Review of Animal Biosciences is online at
animal.annualreviews.org
https://doi.org/10.1146/annurev-animal-022516-
022811
Copyright
c
2018 by Annual Reviews.
All rights reserved
Keywords
echolocation, flight, longevity, immunity, ecosystem, mammals
Abstract
Bats are unique among mammals, possessing some of the rarest mammalian
adaptations, including true self-powered flight, laryngeal echolocation, ex-
ceptional longevity, unique immunity, contracted genomes, and vocal learn-
ing. They provide key ecosystem services, pollinating tropical plants, dis-
persing seeds, and controlling insect pest populations, thus driving healthy
ecosystems. They account for more than 20% of all living mammalian diver-
sity, and their crown-group evolutionary history dates back to the Eocene.
23
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ANNUAL
REVIEWS
Further
Supplemental Material
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Despite their great numbers and diversity, many s pecies are threatened and endangered. Here
we announce Bat1K, an initiative to sequence the genomes of all living bat species (n ∼ 1,300) to
chromosome-level assembly. The Bat1K genome consortium unites bat biologists (>148 mem-
bers as of writing), computational scientists, conservation organizations, genome technologists,
and any interested individuals committed to a better understanding of the genetic and evolution-
ary mechanisms that underlie the unique adaptations of bats. Our aim is to catalog the unique
genetic diversity present in all living bats to better understand the molecular basis of their unique
adaptations; uncover their evolutionary history; link genotype with phenotype; and ultimately
better understand, promote, and conserve bats. Here we review the unique adaptations of bats
and highlight how chromosome-level genome assemblies can uncover the molecular basis of these
traits. We present a novel sequencing and assembly strategy and review the striking societal and
scientific benefits that will result from the Bat1K initiative.
INTRODUCTION
Of all living mammals, bats are extraordinary given their unique and peculiar adaptations. From
the largest golden-capped fruitbat ( Acerodon jubatus), with a wingspan of ∼1.5 m and a weight of
∼1 kg, to the smallest, ∼2-g echolocating bumblebee bat (Craseonycteris thonglongyai ), the huge
diversity and extraordinary adaptive radiations in bat form and function have both fascinated and
terrified people for centuries (1–3). Bats account for ∼20% of all living mammals (>1,300 species)
and are found throughout the globe, absent only from the extreme polar regions. They are the
only mammals that can truly fly and likewise have uniquely evolved laryngeal echolocation, or
biosonar, which enables them to orient in complete darkness using sound alone (4–5). Using these
and other traits, they have evolved to thrive in diverse ecological niches and can feed on insects,
small mammals, fish, blood, nectar, fruit, and pollen (5). They perform key ecosystem services,
pollinating crop species in the tropics (e.g., bats pollinate the flowers of agave, making possible the
distillation of tequila), dispersing seeds, and feeding on crop pests throughout their range (6–9).
Without bats, it is estimated that the United States would spend more than $3 billion a year on
pesticides alone (10). Bats are suspected reservoirs for some of the deadliest viral diseases [e.g.,
Ebola, SARS (severe acute respiratory syndrome), rabies, and MERS (Middle East respiratory
syndrome coronavirus); 11–14], but they appear to be asymptomatic and survive these infections.
This suggests that bats have evolved unique immune systems, and potentially the solution to
better tolerate these pathogens may lie in uncovering how bats limit their immunopathology
upon infection (15, 16). Bats also exhibit extraordinary longevity—they can live up to 10 times
longer than expected given their small body size and high metabolic rate (17). Only 19 mammal
species live proportionately longer than humans given their body size, and 18 are bats (17), with
Brandt’s bat (Myotis brandtii ) holding the reported record for bat longevity [>41 years, ∼7 g (18)].
Bats show few signs of senescence and low to negligible rates of cancer (11), suggesting they have
also evolved unique mechanisms to extend their health spans, rendering them excellent models
to study extended mammalian longevity and ageing (17). Bats face a variety of global threats that
threaten populations with regional or global extinction. The IUCN (International Union for
Conservation of Nature) Red List currently classifies 77 bat species as Critically Endangered or
Endangered and a further 184 as Vulnerable or Near Threatened due to significant population
declines from conservation threats. Lack of knowledge about bat species hampers our ability to
assess population stability in many cases; 222 bat species are considered Data Deficient by the
24 Teeling et al.
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IUCN, meaning that their status cannot yet be determined, and 105 newly identified species are
not yet listed (http://www.batcon.org).
The evolutionary history of bats has stimulated some of the most passionate debates in science,
some spanning decades, from the initial disbelief among the scientific community when Spallan-
zani discovered in 1794 that bats were using sound to orient in darkness (19–21); to heated debates
regarding whether the order was monophyletic and hence questioning if flight had a single origin
in mammals (e.g., the flying primate hypothesis; 22); to current debates over the convergent evo-
lution of laryngeal echolocation in bats and potential loss in the Old World fruit bats (for review,
see 23, 24). Molecular phylogenetic analyses have reclassified their position within the mam-
malian tree (25–27), refuting their position within Archonta (including Primates, Scandentia, and
Dermoptera) and placing them within Laurasiatheria (including Carnivora, Perissodactyla, Eu-
lipotyphla, Pholidota, and Cetartiodactyla); and reclassified familial and interordinal relationships
(Figure 1) (5, 23). Despite these advances, however, the sister taxon to bats remains unresolved (for
review, see 23). As a mammalian order, bats have an impoverished fossil record, with an estimated
>70% of fossil data missing (5, 28). There are astounding Lagerst
¨
atten Eocene fossils, but there
is limited fossil representation thereafter until the Pliocene (29), making it difficult to reconstruct
bat evolutionary history from fossils alone. Solving these outstanding evolutionary questions is
difficult, as convergent homoplastic characters, incomplete lineage sorting, and a fragmented fos-
sil record have limited phylogenetic reconstruction and obscured current understanding of the
evolution and basis of the unique adaptations in bats.
Animal genomes are increasingly revealing the genetic basis of environmental niche specializa-
tion and adaptation (30–33), and studying the molecular mechanisms r esponsible for this diversity
has allowed some of the greatest insights into t he functioning and evolution of our own genome
(32, 34, 35). Some of the most important challenges facing humanity into the next century are
biological. These include improving the well-being of our large and rapidly ageing human popu-
lations (36), preventing the spread of emergent infectious diseases ( 37), maintaining agricultural
productivity (10), and restoring natural ecosystems worldwide (38). These challenges will require a
range of approaches to overcome them, starting with understanding the intrinsic mechanisms that
make us vulnerable to disease and the ecological relationships underlying ecosystem maintenance
and resilience. To date, insights into these various health-related challenges have primarily come
from model organisms such as the fruit fly (Drosophila melanogaster) or the house mouse (Mus mus-
culus). Having been optimized to be reared and studied in labs, these organisms reproduce in great
numbers and live short lives, and thus are ideal experimental subjects. However, insights gained
from the behavior and responses of short-lived organisms do not always translate to those that live
longer, such as humans (17, 39, 40). Studying bats will enable us to address all of these challenges,
as many of their biological features mirror humans and their ecological roles both contribute to and
prevent the spread of infectious diseases, and structure functional ecosystems today and into the
future.
We announce Bat1K, a global effort to sequence and annotate chromosome-level genome as-
semblies of all living bat species. Prioritization of bat genomes is not just desirable but indispens-
able to confront the many challenges to human well-being, ecosystem function, and biodiversity
conservation we now face.
Central to the success of Bat1K is wide involvement from bat researchers across diverse research
areas. This article aims to provide information to the scientific community about the Bat1K effort;
to encourage participation; to set standards for tissue collection and vouchering, assembly quality,
and data release; and to outline the major research endeavors that we anticipate will benefit from
Bat1K.
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Bat1K Project 25
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Y
inpterochiroptera
Yangochiroptera
102030405060 0
Cenozoic
Millions of years ago
Paleogene Neogene
Nycteridae
Emballonuridae
Phyllostomidae
Mormoopidae*
Noctilionidae
Furipteridae
Thyropteridae
Mystacinidae
Myzopodidae
Vespertilionidae*
Natalidae
Pteropodidae*
Rhinolophidae*
Megadermatidae*
Craseonycteridae
Rhinopomatidae
Miniopteridae*
Molossidae
Rhinonycteridae
Hipposideridae*
Cistugidae
Figure 1
Molecular consensus on bat familial relationships and divergence times (23). Asterisks indicate bat families
with genomes available in the National Center for Biotechnology Information. Those species are listed in
Table 2. Bat artwork created by Fiona Reid.
26 Teeling et al.
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KEY AREAS OF IMPACT
The study of bats and their genomes is likely to have widespread impacts on a range of diverse
scientific fields. Below we outline some key areas of study.
Model for Healthy Ageing
Unlike most lab animals, bats are excellent models for understanding human senescence and
ageing and to discover the means to improve health into old age. Although there are some merits
to mechanistic hypotheses of ageing (e.g., that life span should be inversely related to metabolic
rates, as the latter contribute to the accumulation of intracellular debris leading to ageing), the best-
supported theory of ageing is evolutionary and linked to life history (41). According to this theory,
if adults in a population experience high extrinsic mortality (e.g., from predation), natural selection
will favor short-term reproductive success over long-term survival and maintenance, resulting in
rapid senescence after reproduction, past the age at which most individuals would have died in a
natural population (42). The survivorship and life history of house mice reflect this pattern, with
intrinsic mortality and morbidity rising sharply past one year of age, even under highly favorable
lab conditions. Conversely, populations with low extrinsic mortality will experience continued
selection throughout longer lifetimes, favoring slow senescence and resulting in longer, healthier
lifetimes. Because bats are both nocturnal and capable of active flight, they have escaped the
attention of most predators. This in turn has led them to evolve the relatively unusual vertebrate
combination of long life spans with small bodies (17, 40, 43). As long-lived mammals, in some cases
living >41 years, bats offer clues regarding the mechanisms for maintaining high function across
internal systems over a long life span, longer than any similar-sized mouse can live (17, 44, 45).
Natural selection over millions of generations for continued health and reproduction through-
out a long lifetime has equipped bats with excellent cellular and system-wide mechanisms of main-
tenance (45). This is particularly impressive considering that the high metabolic rates characteristic
of bats are expected to produce reactive oxygen species, typically causing chronic inflammation
and hastening senescence (46). However, the maintenance of function alone is not enough, as cells
and tissues need constant repair over the course of a multiyear life span. Studies focused on bats
have identified suites of cellular repair mechanisms that potentially evolved to support the unusual
longevity of bats (11, 40, 44, 45). These genes and variants can be readily compared with human
genes to discover specific features that would enable a healthy old age (11, 44, 45).
Model for Enhanced Disease Resistance
Bats have enhanced immune function, coupled with a potentially modulated inflammatory re-
sponse (11, 16, 47). This holds considerable potential for addressing some of the worst conse-
quences of senescence of humans. Inflammatory disorders associated with autoimmune diseases
are among the fastest growing causes of disease worldwide, particularly in ageing populations (48).
The ability to modulate inappropriate inflammation in response to stressors without impairing
immune function could improve the lives of millions. Hence, detailed exploration of the genomic
mechanisms of gene expression in wild bats could hold the key to improving health conditions
worldwide (16). High-quality bat genomes will drive a better understanding of molecular bases
underlying the resistance/tolerance of European bats to white-nose syndrome (49), which could
ultimately be used to inform future bat conservation and management efforts within the United
States. White-nose syndrome is a deadly fungal disease recently introduced to North America
from Europe (50) that has decimated US bat populations, particularly of little brown bats (Myotis
lucifugus) and tricolored bats (Perimyotis subflavus), and is responsible for an estimated 5–6 million
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Bat1K Project 27
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