Chapter 2 - Zebrafish Taxonomy and Phylogeny or - 2020 - The Zebrafish in Biomed PDF
Chapter 2 - Zebrafish Taxonomy and Phylogeny or - 2020 - The Zebrafish in Biomed PDF
Chapter 2 - Zebrafish Taxonomy and Phylogeny or - 2020 - The Zebrafish in Biomed PDF
2
Zebrafish Taxonomy and Phylogeny or
Taxonomy and Phylogeny
Braedan M. McCluskey1, Ingo Braasch2
1
Department of Biology, University of Virginia, Charlottesville, VA, United States of America;2Department of Integrative
Biology and Program in Ecology, Evolutionary Biology and Behavior, Michigan State University, East Lansing, MI,
United States of America
TABLE 2.1 Phylogenetic classification of zebrafish (Danio rerio). vertebrates as outgroups to gnathostomes. Cyclostomes
Classification below the gnathostome level is lack jaws and paired fins and feature many other
following Betancur et al. (2017). morphological as well as genomic differences, but also
Kingdom Metazoa (Animalia) important shared characteristics with the jawed verte-
brates. Thus, these jawless fish are central taxa in
Superphylum Deuterostomia
comparative studies to reconstruct ancestral conditions
Phylum Chordata during the early phase of vertebrate evolution and the
Subphylum Vertebrata evolutionary changes that led to the emergence of jawed
vertebrates (Nikitina, Bronner-Fraser, & Sauka-Spengler,
Infraphylum Gnathostomata
2009; Shimeld & Donoghue, 2012) (Fig. 2.1).
Megaclass Osteichthyes Gnathostomes are further subdivided into two main
(Euteleostome) groups: the cartilaginous fishes (Chondrichthyes),
Superclass Actinopterygii that is, sharks, skates, and chimeras, and the bony
Class Actinopteri
vertebrates (Euteleostome or Osteichthyes), to which
zebrafish and human belong (Pough & Janis, 2019)
Subclass Neopterygii (Fig. 2.1). Several cartilaginous fish species are being
Infraclass Teleostei used in developmental studies (reviewed in Onimaru,
Motone, Kiyatake, Nishida, & Kuraku, 2018) and the
Supercohort Clupeocephala
recent availability of chondrichthyan genomes (Hara
Cohort Otomorpha et al., 2018; Venkatesh et al., 2014) promises a rich future
Subcohort Ostariophysi for cartilaginous fishes as piscine model organisms for
Superorder Cypriniphysae
the investigation of gnathostome biology and outgroups
to bony vertebrates.
Order Cypriniformes Within bony vertebrates, the lineages leading to
Suborder Cyprinoidae zebrafish and human then parted around 400e450
million years ago, with the ray-finned fishes (Actino-
Family Danionidae
pterygii) that include zebrafish diverging from the
Genus Danio lobe-finned fishes (Sarcopterygii) that gave rise to the
Species Danio rerio tetrapods. Only three groups of lobe-finned fishes have
survived until today: the coelacanths and the lungfishes,
the latter of which are, in turn, the closest living relatives
Ray-finned fishes
LCEA
Bony vertebrates
Jawed vertebrates
Coelacanths
Lobe-finned
Vertebrates
Lungfishes
Chordates
VGD1/2 Tetrapods
Cartilaginous
fishes
Cyclostomes
Urochordates
Cephalochordates
FIGURE 2.1 Phylogeny of the vertebrate lineage. Zebrafish belongs to the ray-finned fishes, with their phylogeny further detailed in Fig. 2.2.
Reconstructing the last common euteleostome (i.e., bony vertebrate) ancestor (LCEA ¼ red dot) is essential for the comparison of ray-finned and
lobe-finned vertebrates, especially for the biomedical link of zebrafish to human. VGD1 and VGD2 indicate the likely occurrences of two rounds of
vertebrate genome duplication at the base of vertebrates. The timescales in Figs. 2.1 and 2.2 are based on data obtained from www.timetree.org.
I. Introduction
Zebrafish and Related Danio Species as an Evolutionary Model System 17
Teleost fishes are divided into three main lineages:
Zebrafish
Cypriniforms Danio genus the clupeocephalans that include zebrafish and most
Carps/Goldfish other fish model systems (see below); the osteoglosso-
Ostariophysans
Cyprininae morphs, which include, for example, arowana, African
Blind cavefish butterflyfish, and mormyrid electric fish; and the elopo-
Astyanax mexicanus
Livebearers
morphs to which eels and tarpons belong (Fig. 2.2). The
platyfish, swordtail, guppy interrelationships of these three major lineages have
Annual killifishes been difficult to resolve and are a matter of ongoing
e.g. Nothobranchius furzeri
investigation (Betancur et al., 2017).
Medaka
Clupeocephalans
Cichlids
species and the percomorphs with more than 14,000 spe-
Stickleback cies (Alfaro et al., 2009; Chakrabarty et al., 2017; Near
Gasterosteus aculeatus
et al., 2013). Ostariophysans include fishes as diverse
Antarctic icefish as catfishes, characins, electric knifefishes, and the cypri-
Teleosts Notothenioids
TGD niforms with zebrafish (Chakrabarty et al., 2017).
Pufferfishes
Neopterygians
Salmonids
Zebrafish and Related Danio Species as an
Osteoglossomorphs
bony tongues, mooneyes Evolutionary Model System
Elopomorphs
eels, tarpons Cypriniform and Danionid Relationships
Ray-finned Holostei Spotted gar
fishes Lepisosteus oculatus Zebrafish is surrounded by cypriniform biodiversity.
Acipenseriforms
Cypriniforms represent the largest group of freshwater
sturgeons, paddlefish fishes and besides minnows and suckers also includes spe-
Polypteriforms cies important for aquaculture, such as common carp and
bichirs, reedfish
grass carp, as well as many popular ornamental species,
400 300 200 100 0
million years ago
such as goldfish and rasboras (Stout et al., 2016).
The taxonomy of this diverse group has experienced
FIGURE 2.2 Phylogeny of the ray-finned fish lineage TGD in- numerous revisions as more species have been
dicates the occurrence of the Teleost Genome Duplication at the base of
teleosts. Black pin symbols show the occurrence of additional, lineage-
described and phylogenetic inference methods have
specific genome duplication events. shifted from morphological to molecular methods.
This change is particularly relevant to zebrafish, which
is referred to as Brachydanio rerio in much of the scientific
of the third group, the tetrapods that include us humans
literature from prior to 1995. Only recently have phylo-
(Pough & Janis, 2019) (Fig. 2.1).
genomic approaches proved sufficient to provide strong
With the advent of next-generation sequencing tech-
support for relationships between families within Cypri-
niques and the acquisition of large-scale genomic data
niformes and between species within Danio (McCluskey
across the tree of life, major strides have been made in
& Postlethwait, 2015; Stout et al., 2016). The most exten-
phylogenomics (i.e., the use of genome-wide sequence
sive molecular phylogenomic study of Danio to date
information to infer phylogenetic relationships) to
supports D. aesculapii as the closest relative of D. rerio
reconstruct the evolution of ray-finned fishes (e.g.,
(Fig. 2.3). Zebrafish is also closely related to D. kyathit
Betancur et al., 2013; Hughes et al., 2018; Near et al.,
with evidence of gene flow between those lineages
2012). Within the ray-finned fishes, the zebrafish belongs
during speciation (McCluskey & Postlethwait, 2015).
to their most species-rich clade, the teleost fishes (Teleos-
Relationships within Danio will be better resolved as
tei) (Fig. 2.2). With more than 25,000 species, teleosts
the diversity within this group is further described.
make up almost 50% of all living vertebrates (Helfman,
Collette, Facey, & Bowen, 2009; Nelson, 2006). Together
with their sister lineage, the holostean fishes that consist
The Emerging Danionid Model System
of bowfin and gars, teleosts are grouped into the Neo-
pterygii. More distantly, teleosts are related to the aci- The dozens of Danio species are phenotypically
penseriforms (sturgeons and paddlefishes) and the diverse, but all share the major advantages of zebrafish
polypteriforms (bichirs and reedfish), the earliest as a model vertebrate making danios ideal for
branching lineage among living ray-finned fishes studying interspecific evolution (Irion, Singh, &
(Betancur et al., 2013; Near et al., 2012) (Fig. 2.2). Nusslein-Volhard, 2016; Parichy, 2006). All danios have
I. Introduction
18 2. Zebrafish Phylogeny and Evolution
I. Introduction
Zebrafish and Its Relation to Other Fish Model Species 19
Importance of Genome Duplications for retention rate of TGD duplicates appears to be relatively
Zebrafish Evolution similar across teleosts, differences in terms of the specific
genes retained in duplicate within individual teleost lin-
At the genomic level, an important aspect of verte- eages have contributed to the genomic diversification of
brate evolution that needs to be considered in human- teleost lineages. Even if different teleost groups have
to-zebrafish comparisons is the role of three rounds of retained both TGD duplicates, lineage-specific diver-
whole-genome duplications (or polyploidizations) that gence in the functional roles among duplicates can be
have impacted the zebrafish and human lineages in observed (Braasch & Postlethwait, 2012).
several ways (Figs. 2.1 and 2.2). Polyploidizations are In addition to the TGD, the vertebrate lineage is
rare events in animals but have occurred comparatively derived from likely two additional, earlier ancient
frequently in fishes (Braasch & Postlethwait, 2012) rounds of whole-genome duplication at the base of
(Fig. 2.2). The amplification and diversification of verte- the vertebrate lineage, that occurred after their separa-
brate gene families imposed by the three vertebrate tion from nonvertebrate chordates. The evolutionary
genome duplications have led to complex scenarios of sequence of these Vertebrate Genome Duplications,
gene function evolution that sometimes are difficult to VGD1 and VGD2 (Fig. 2.1), remains a matter of ongoing
disentangle. debate (Sacerdot, Louis, Bon, Berthelot, & Roest Crol-
All living teleost species, including zebrafish, are lius, 2018; Smith et al., 2018). Differential loss of
derived from an ancestor that underwent a whole- VGD1/VGD2 gene duplicates after the divergence of
genome duplication event at the dawn of teleost evolu- the ray-finned and lobe-finned lineages has led to situ-
tion. This Teleost Genome Duplication (TGD) occurred ations in which no directly orthologous genes remain in
within the neopterygian lineage after the separation of the zebrafish and human genomes (Postlethwait, 2007).
teleosts from the holostean fishes (gars and bowfin), This can complicate the transition of genetic informa-
but before the divergence of the three major teleost line- tion from one system to the other. For example, the
ages of clupeocephalans, osteoglossomorphs, and elopo- intensively studied human stem cell factor POU5F1
morphs (Fig. 2.2) (reviewed in Braasch & Postlethwait, (OCT4) has no direct ortholog in the zebrafish genome
2012). For details on the genomic impacts of the TGD because of secondary loss from the ray-finned genome
see Postlethwait and Braasch (2019) in this volume. following VGD1/VGD2; its VGD1/VGD2 duplicate
Following the TGD, the teleost genome originally was Pou5f3, on the other hand, is present in the ray-
tetraploid, but it has secondarily returned to the diploid finned, and thus, zebrafish genome, while having
state through the process of rediploidization. Impor- been secondarily eliminated from the eutherian
tantly, depending on methods of TGD gene duplicate mammal and hence human genome (Frankenberg
inference, it has been estimated that between 1,200 and et al., 2014).
3,400 pairs of TGD gene duplicates have remained in In summary, a careful examination of gene family
the zebrafish genome (Howe et al., 2013; Pasquier history evolution is paramount for the transfer of genetic
et al., 2017; Roux, Liu, & Robinson-Rechavi, 2017). information between zebrafish and human. Gene orthol-
Thus, for a significant portion of human genes, there ogy predictions provided, for example, by the ZFIN and
will be two TGD-derived gene duplicates (also called Ensembl (www.ensembl.org) databases are good start-
co-orthologs or paralogs) in the zebrafish genome. This ing points for in-depth phylogenetic investigations of
can complicate comparisons between zebrafish and gene family relationships across vertebrates.
human as one may have to take two genomic regions
in the zebrafish into account, potentially harboring two
TGD co-orthologs of the gene under investigation. For
example, there are two sonic hedgehog (shh) genes present
Zebrafish and Its Relation to Other Fish
in the zebrafish genome, shha and shhb, that are co-ortho-
Model Species
logs to the single SHH gene in human.
Since their fixation in the teleost genome, TGD dupli- Zebrafish is the most commonly used fish species in
cates will have diverged in function in often complex biomedical research, but it is important to remember
that zebrafish is just one of tens of thousands of teleost
patterns, following evolutionary fates such as subfunc-
fish species. It, therefore, provides a snapshot of the
tionalization (the distribution of ancestral gene
tremendous genotypic and phenotypic biodiversity of
functions among duplicates) and neofunctionalization
teleosts, and comparisons to other phylogenetically
(emergence of novel gene functions) (Force et al.,
1999). Comparing zebrafish to other teleosts, one will diverse fish models are essential to inform the evolution
further find differences in terms of TGD duplicate reten- of zebrafish in relation to the teleost, ray-finned, and
tion and loss among species. Although the overall bony vertebrate ancestors.
I. Introduction
20 2. Zebrafish Phylogeny and Evolution
I. Introduction
References 21
emerged as the most popular annual killifish species in lineages. Due to its “unduplicated” nature with regard
aging research as it represents the most short-lived to the TGD and its comparatively slow rates of genomic
known vertebrate with a few months of lifespan and and morphological evolution, gar provides important
sexual maturity within a few weeks after hatching reference points for the transition of biomedically
(Cellerino, Valenzano, & Reichard, 2016; Platzer & relevant morphological and genomic information across
Englert, 2016). bony vertebrates and to link zebrafish to human biology
Cichlids: With several thousand species, cichlids are (Braasch et al., 2015, 2016). This has helped, for example,
a prime example for adaptive radiations and phenotypic to clarify the evolution of joint development in bony
diversification (Salzburger, 2018) that feature complex vertebrates, enabling to then develop an arthritis model
social behaviors (Fernald, 2017) and trophic adaptations in zebrafish (Askary et al., 2016).
of the jaw apparatus, which can be used to model hu-
man craniofacial diseases (Powder & Albertson, 2016).
Again, comparative functional analyses using zebrafish Conclusion and Outlook
have been instrumental in enlightening the underlying
genetic basis of such biomedically relevant phenotypes Zebrafish is a unique representative of ray-finned
(Cooper, Wirgau, Sweet, & Albertson, 2013; Powder, teleost fish biodiversity that diverged from human
Cousin, McLinden, & Albertson, 2014). more than 400 million years ago. While being a powerful
Sticklebacks: Three-spined stickleback (Gasterosteus model system to study vertebrate biology and human
aculeatus) and related species are major model organ- disease, it is important to keep in mind that zebrafish
isms for evolutionary and ecological genetics (Peichel neither is a “prototypic” fish that stopped evolving after
& Marques, 2017). Studies on the genetic basis of pheno- separation from the human lineage nor that findings in
typic differences among stickleback populations, for zebrafish are necessarily generalizable across fish
example, in the pigmentary and skeletal systems, found lineages.
parallels to phenotypic diversity among human popula- A meaningful utilization of the zebrafish model in
tions, yet also pointed to human-specific changes during biomedical research, therefore, calls, on the one hand,
vertebrate evolution, respectively (Indjeian et al., 2016; for the detailed elucidation of shared and divergent
Miller et al., 2007). Furthermore, sticklebacks often serve characteristics of zebrafish and human at both the
as percomorph comparators to zebrafish in phenotypic and genetic levelsdas exemplified by the
developmental-genetic studies (e.g., Askary et al., information provided in the chapters of this volume.
2016; Jovelin et al., 2007). On the other hand, the inclusion of information from
Antarctic icefish: Notothenioid icefish are uniquely the phylogenetically expanding swarm of fish model
adapted to the extreme cold of Antarctic waters: they systems will put zebrafish research into an enriched
possess antifreeze proteins, many species are character- evolutionary context. With the relentless technical
ized by reduced bone formation, and they lack improvements for its investigation, zebrafish will
functional hemoglobin and red blood cells. Thus, they continue to lead the charge in illuminating the
can serve as models for human diseases, such as osteo- genotype-to-phenotype map in the fish world.
penia and osteoporosis and anemia (Albertson et al.,
2009). Due to their unique ecology, Antarctic icefish are
difficult to study in captivity, and thus, zebrafish have
been used for example to functionally investigate genes
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I. Introduction
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I. Introduction