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Contents
.
.
Chapter 1
Introduction to Hox Modules in Evolution and
Development..........................................................................................1
Chapter 2
Multiple Layers of Complexity in the Regulation of the
Bithorax Complex of Drosophila.......................................................
.
15
Chapter 3
The Role of Hox Genes in the Origins and Diversification of
Beetle Horns........................................................................................ 53
Chapter 4
Duplication and Evolution of Hox Clusters in Chelicerata
(Arthropoda)........................................................................................ 77
Chapter 5
Structural Constraints in Hox Clusters: Lessons from Sharks
and Rays............................................................................................ 103
Chapter 6
.
Evolution of Cyclostome Hox Clusters............................................. 121
Chapter 7
Hox Genes in Echinoderms.............................................................. 141
vii
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viii
Contents
Chapter 8
Hox Genes in Mollusca..................................................................... 161
Chapter 9
The Evolution of Hox Genes in Spiralia........................................... 177
Index...................................................................................................................... 195
.
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1
Introduction to Hox
Modules in Evolution
and Development
CONTENTS
1.1 The Revolution of Evo-Devo............................................................................. 1
1.2 Homeotic Hox Homeobox Genes...................................................................... 2
1.3 A New Era of Wider Taxon-Sampling..............................................................4
1.4 Complex Regulatory Landscapes: Micromanagement and Collinearity........... 6
1.5 And There Is More............................................................................................ 8
1.6 Conclusion......................................................................................................... 8
References................................................................................................................... 9
1.1
THE REVOLUTION OF EVO-DEVO
The Hox genes are a renowned and hugely important subset of developmental control
genes in animals. The molecular characterisation of these genes began in the 1980s
and utterly transformed developmental biology, as well as rejuvenating the field of
evolutionary developmental biology (often abbreviated to evo-devo). A wealth of
research has accumulated since the early days of molecular biology, with the Hox
genes representing some of the best exemplars of the two sides of the evo-devo coin:
deep homology versus diversification. This book aims to capture some of the latest
developments in the field of Hox evo-devo research, illustrating the rich vein that
these genes have provided for deepening our understanding of the origins and diversification of huge swathes of the animal kingdom.
Hox genes are homeobox-containing genes; the homeobox is a distinctive nucleotide motif, typically of 180bp, that encodes a homeodomain, which in turn acts as a
sequence-specific DNA-binding motif. Hox proteins thus tend to act as transcription
factors. Few, if any, developmental gene pathways or regulatory networks do not
involve homeobox genes. Although the Hox genes are most renowned for their roles
in patterning the anterior-posterior axis of animals during embryogenesis (Akam,
1989; McGinnis and Krumlauf, 1992), the genes also have a multitude of activities
and effects beyond this anterior-posterior patterning role, with complex regulatory
landscapes facilitating activities in morphogenesis and organogenesis (Saurin et al.,
1
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2
Hox Modules in Evolution and Development
2018; Hajirnis and Mishra, 2021). As such, the Hox genes have had a major role in the
expansion and development of the field of evo-devo, following the discovery of the
homeobox in the Hox genes of the fruit fly, Drosophila melanogaster, and then
the rapid follow-on discoveries of conservation of the homeobox and homologous
Hox genes across almost the entire animal kingdom, including in humans (McGinnis,
1984a, b; Scott and Weiner, 1984; Hart et al., 1985; Levine et al., 1985; Boncinelli
et al., 1988; Duboule and Dollé, 1989; Graham et al., 1989; Gehring, 1994; Lewis,
1994; McGinnis, 1994). This widespread conservation of these homologous genes,
their action in comparable and often homologous developmental processes, and their
major roles in shaping animal body plans, with roles in generating both the similarities and differences between animal forms, has had a profound impact on biology
and our understanding of the evolution of animal diversity.
1.2
HOMEOTIC HOX HOMEOBOX GENES
The name homeobox derives from the phenomenon of homeosis described by
William Bateson in his 1894 book Materials for the Study of Variation (reprinted
as Bateson, 1992), for which the Hox genes of D. melanogaster are the best-known
examples at the level of the genetics of such mutants. Homeosis entails one region
or part of the body being transformed into another. One way to think of this is that
things have not been deleted, duplicated, expanded or reduced, but instead the identity of something has changed such that its developmental fate becomes one that is
usually located in a different place in the body plan.
Some of the most famous homeotic mutants are Antennapedia, in which the
antennae are transformed into legs (Gehring, 1966), or the Ubx four-winged fly
(described in Chapter 2 by Karch and Maeda) in which the third thoracic segment
instead develops with the identity of the wing-bearing second thoracic segment. The
key feature of these types of mutants is that one region of the body is transformed
such that it develops as another part of the body – i.e. it is homeotically transformed
(Lewis, 1978, 1994). The genes effected by these mutations thus give particular
regions or parts of the body their ‘identity’ and are entwined with the concept of
positional information in embryogenesis, in this case in terms of a ‘Hox code’ –
whereby a particular combination of Hox proteins specify the identity of a region of
the body or a particular structure (Lewis, 1978; Wolpert, 1996). Thus, when the fly
homeotic genes of the Antennapedia and Bithorax complexes (ANT-C and BX-C,
respectively) were first cloned via the then pioneering techniques of genomic walking (Bender et al., 1983; Garber et al., 1983; Scott et al., 1983) and low stringency
DNA hybridisation, and their DNA sequences revealed to have a conserved motif
(McGinnis et al., 1984a, b; Scott and Weiner, 1984), it made perfect sense to call
the motif the homeobox. Despite repeated use of the term ‘Hox’ in the literature
interchangeably for homeobox, the Hox genes are in fact only a subset of homeoboxcontaining genes; being those genes that are orthologs of the genes of the fly and
mouse/human Hox gene clusters (Scott, 1992; Ferrier, 2016a) (Figure 1.1A). Thus,
whilst the human genome contains over 200 homeobox genes and arthropods like
D. melanogaster over 100 (Holland et al., 2007; Chipman et al., 2014), there are
only 39 human Hox genes and eight Hox genes in D. melanogaster (but with other
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Introduction to Hox Modules in Evolution and Development
3
FIGURE 1.1 The Hox gene clusters of the fly Drosophila melanogaster and human Homo
sapiens, and a phylogenetic tree highlighting the relationships of the taxa discussed in this
book. (A) The Hox clusters of the fly D. melanogaster and human, H. sapiens, highlighting the Hox genes and the Hox-derived genes (filled and empty triangles respectively),
and non-homeobox genes (rounded rectangles) for the fly and the four human clusters
resulting from the two rounds of Whole Genome Duplications (WGD) in early vertebrate
evolution, followed by various gene loss events (represented as ‘missing’ triangles along
the clusters). The different colours of the triangles represent the anterior, group 3, medial
and posterior categories of Hox genes, and their orientation represents the direction of
transcription for each gene. (B) A schematic phylogeny of selected taxa discussed in this
book. See Chapter 9 by Gasiorowski, Martín-Durán and Hejnol for further elaboration of
the spiralian clade.
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4
Hox Modules in Evolution and Development
homeobox-containing genes within the ANT-C part of the Hox cluster derived from
bona fide Hox genes, i.e. zerknüllt 1 and 2 and bicoid from Hox 3, and fushi tarazu
from a medial Hox gene perhaps with affinity to Lox5 or Hox6 of lophotrochozoans
or deuterostomes, respectively; Falciani et al., 1996; Telford, 2000) (Figure 1.1A).
It is these Hox genes and their orthologs across the animal kingdom that this book
focuses on (Figure 1.1B).
1.3
A NEW ERA OF WIDER TAXON-SAMPLING
Our understanding of the function and regulation of Hox genes in Drosophila is
resolved to unprecedented detail, stemming from the elegant and thorough work in
genetics by Ed Lewis and colleagues, and flourishing still further with the impact
of developments in molecular techniques for the BX-C (as outlined by Karch and
Maeda in Chapter 2), and in parallel for the ANT-C (see (Denell, 1994) for a perspective on the early genetic studies of the ANT-C, which were later expanded
by the Kaufman lab and many others). This detailed knowledge of Drosophila
is complemented by the elegant and detailed work in vertebrates, particularly in
mice (e.g. Kmita and Duboule, 2003; Montavon et al., 2011; Nolte et al., 2013; Ahn
et al., 2014; Lonfat et al., 2014; Darbellay et al., 2019; Amandio et al., 2021). Whilst
there is clearly much more to be understood about Hox genes and their activities in
Drosophila and mice, the extent of the similarities and differences between these
so-called model species to other taxa is still largely an unresolved mystery. However,
we are now entering an era in which this mystery can be clarified, with techniques
becoming available that permit efficient exploration of molecular mechanisms without requiring the heroic efforts such as those exerted by Ed Lewis in unravelling the
genetics of a species, so that there is the possibility of exploring taxa largely driven
by their phylogenetic position or mode of development, instead of their amenability
to genetic approaches. The early description of the Hox genes as the Rosetta stone
for developmental biology (Slack, 1984) is even more apposite now than ever, with
the genes providing a rapid means to delve into the molecular mechanisms of how
animal form is constructed and how it evolved. This book thus comes at a time when
the field is rich with possibilities, and the authors here give a clear overview of where
the field is going.
Starting from the detailed mechanistic understanding of Hox gene regulation
and function that can be obtained in more ‘traditional’ study species like D. mela­
nogaster (see Karch and Maeda, Chapter 2), the power of wider taxon sampling
is clearly demonstrated in subsequent chapters. Moving progressively further away
from Drosophila, phylogenetically speaking, Zattara and Moczek (Chapter 3) use
other insects, the horn-bearing beetles, as a system to understand the evo-devo of
novel morphologies and evolvability – long-standing issues and debates in evolutionary biology that are now getting a new perspective from evo-devo and Hox studies
in particular. Beyond insects, Sharma (Chapter 4) uses the chelicerate arthropods
(i.e. spiders, mites, sea spiders and horseshoe crabs) to study the impacts of whole
genome duplication (WGD) and the importance of understanding the underlying
species phylogeny (which Hox genes can contribute to) in order to make accurate
and appropriate evolutionary inferences.
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Introduction to Hox Modules in Evolution and Development
5
These chelicerate WGDs are an intriguing case of a clade that has experienced
WGDs that have been a key factor in shaping the structure, organisation and content
of these genomes, with processes such as duplication-degeneration-complementation
(DDC) (Force et al., 1999) impacting the evolution of the regulation and function of
the developmental control genes (e.g. Schwager et al., 2017; Leite et al., 2018). Hox
genes have been and are proving to be key study systems to better understand the
impacts of gene duplication, via processes such as WGD, as a route to increased
genetic diversity and its interplay with developmental and morphological evolution.
The more well-known instance of WGD shaping the genomes of a large clade is
the case of the vertebrates. It is now well-established that the genomes of the gnathostome (jawed) vertebrates were shaped by two rounds of WGD (the 2R hypothesis) (Lamb, 2021; Nakatani et al., 2021), with further instances of additional WGD
in lineages such as the teleosts (i.e. the teleost 3R WGD; Amores et al., 1998; Taylor
et al., 2001; Aase-Remedios and Ferrier, 2021). Resolution of these 2R and 3R events
in gnathostomes has been significantly improved with non-teleost data such as that
from chondrichthyans (see Kuraku, Chapter 5), which now reveals the dynamics of
post-2R Hox evolution to unprecedented detail, including gene and cluster losses in
distinct lineages and unusual or distinctive divergences (e.g. HoxC genes), as well as
cryptic pan-vertebrate genes like Hox14 (Kuraku et al., 2016). Furthermore, a major
area of debate with regards to the 2R vertebrate events is how do the jawless cyclostome vertebrates (or agnathans) fit into the picture. Are they also descended from
the same 2R events that shaped the gnathostomes, or not? And if not, then did they
experience just one of the 2R events (i.e. cyclostomes diverged after 1R) or neither of
the 2R WGDs? Clearly, there are large numbers of paralogs in cyclostome genomes
and so they certainly did undergo large-scale duplications of some sort, but the difficulties that have been experienced over the years in reliably placing cyclostome
genes into molecular phylogenetic trees have contributed to a diversity of opinions
on how to interpret the data. The chapter of Pascual-Anaya and Böhmer (Chapter 6)
gives an update on the cyclostome field and the prominent role that Hox genes have
played in it. They provide a new hypothesis for the state of the last common ancestor
of vertebrates in terms of the array of Hox gene clusters that it possessed.
If we move deeper into the deuterostomes, beyond the vertebrates, we encounter
one of the most unusual body plans in the animal kingdom: that of the pentameral
echinoderms. Given the key role that the Hox genes play in patterning the anterior-­
posterior axis of bilaterian animals, many in the field of echinoderm evo-devo have
been focused on how these genes might pattern the pentameral body plan and hence
how such a novel morphology evolved. Omori and Irie (Chapter 7) provide an overview of the latest echinoderm Hox research, demonstrating the clear value of wide
taxon sampling and extending beyond what has historically been the major echinoderm study system of the purple sea urchin, Strongylocentrotus purpuratus, to obtain
a clear picture of what constitutes the echinoderm Hox complement and organisation
and how these genes are deployed during echinoderm development. Data from such
a wide selection of species, sampling from all of the extant echinoderm classes, has
clearly been essential to construct a more reliable picture of the ancestral state for
this intriguing phylum and facilitate more robust comparisons to other bilaterian
phyla. Wide taxon sampling is key.
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6
Hox Modules in Evolution and Development
Until relatively recently, a major part of the animal kingdom was largely neglected
in molecular evo-devo research, i.e. the phyla of the Lophotrochozoa/Spiralia.
Perhaps this was in large part due to the traditional study species in developmental
biology being from the Ecdysozoa and Deuterostomia (i.e. D. melanogaster as an
ecdysozoan and vertebrates like mice and zebrafish being deuterostomes). This relative neglect is now being rectified, as demonstrated by the chapters by Wollesen and
Wanninger, and Gasiorowski and colleagues (Chapters 8 and 9 respectively). As well
as providing insights into some of the most morphologically diverse phyla, such as
the molluscs, and the roles of Hox genes in shaping these body plans and the novelties they contain, this lophotrochozoan data is also proving valuable in shaping our
views on the links between Hox cluster organisation and the regulation of the genes.
Co-option as a major process in evo-devo (True and Carroll, 2002) is a common
theme in the Hox genes of these lophotrochozoan taxa, with Hox genes frequently
being redeployed from their pleisiomorphic ancestral roles in axial patterning into
apomorphies or evolutionary novelties. Pending functional genetic data, it is presumed that the Hox genes have an integral role in controlling at least some aspect
of the development of these evolutionary novelties. Thus, we come full circle in the
chapters of this book, with Hox roles in anterior-posterior patterning in insects like
the fruit fly alongside co-option into the evolution of novelties like beetle horns, to
Hox roles in both axial patterning and development of novelties in lophotrochozoans
like the molluscs, largely via the evolution of the regulation of the Hox genes.
1.4 COMPLEX REGULATORY LANDSCAPES: MICROMANAGEMENT
AND COLLINEARITY
One of the early stumbling blocks to the widespread adoption of ideas on roles for
Hox gene changes in evolution was the perception that mutation of these genes would
always have dramatic impacts, usually early in embryogenesis, that would lead to
large changes that would almost always be detrimental (akin to the idea of hopeful
monsters attributed to Goldschmidt, 1940). With the current much deeper understanding of the complexities and modularity of the regulation of the Hox genes and
their roles in development, it is clear that we no longer have to hypothesise hopeful
monsters. Instead, Hox genes can be viewed as micro-managers rather than master
control genes – hopeful monsters are not necessarily impossible, but are certainly
not required for Hox changes to have significant roles in evo-devo (Akam, 1998a,
b). The micro-manager idea was stimulated by research on Hox gene regulation and
pleiotropy, emphasising the importance both of modular regulatory elements and the
highly dynamic expression of Hox genes in time and space, as well as the abundance
of target genes, all of which can accumulate multiple small changes over the vast
periods of evolutionary time to sum to apparently saltational changes when comparing extant taxa that diverged many millions of years ago (Akam, 1998a, b; Buffry
and McGregor, 2022). In time, the detailed understanding of Hox gene regulation
and function that we possess for D. melanogaster will be extended across the animal
kingdom, providing even greater explanatory power to Hox genes and evo-devo.
Hox gene regulation also provides one of the major phenomena that the Hox
genes are renowned for: Collinearity. This entails the order of the genes along the
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Introduction to Hox Modules in Evolution and Development
7
chromosome corresponding to the order that the genes are expressed along the
anterior-posterior axis, both in terms of their domains of expression (spatial collinearity) and the sequence in which they are activated (temporal collinearity – with
anterior acting genes expressed first, through to posterior genes being activated last)
(Von Allmen et al., 1996; Ferrier and Minguillón, 2003; Deschamps and Duboule,
2017; Krumlauf, 2018; Duboule, 2022). Nevertheless, it is clear that there are many
cases of Hox genes not being clustered (Lemons and McGinnis, 2006; Monteiro
and Ferrier, 2006), and a range of types of Hox gene organisation are recognised
(Duboule, 2007). A potentially unifying principle behind the organisation of the
Hox genes presumably relates to how these genes are regulated, following the abundant evidence for various long-range regulatory processes and phenomena such as
topologically associating domains (TADs) (Acemel et al., 2016; Duboule, 2022),
shared enhancers (Sharpe et al., 1998; Kmita and Duboule, 2003; Ahn et al., 2014;
Miller and Posakony, 2020; and see Chapter 2 by Karch and Maeda), intermingled
enhancers (Shippy et al., 2008), chromatin modulation (Chambeyron and Bickmore,
2004; Chambeyron et al., 2005), insulator/boundary elements and collinearity of
enhancers (see Chapter 2 by Karch and Maeda), all of these things creating regulatory landscapes over Hox clusters at least in some taxa. From views on collinearity being focused on the overall spatial and temporal activation of the genes, with
the pre-­eminence of temporal collinearity being viewed as the major process or
mechanism(s) constraining the Hox genes in intact, ordered clusters in the genome
(e.g. Duboule, 1994; Von Allmen et al., 1996; Ferrier and Holland, 2002; Ferrier
and Minguillón, 2003; Monteiro and Ferrier, 2006; Deschamps and Duboule, 2017;
Pascual-Anaya et al., 2018; Duboule, 2022), the lophotrochozoan data has been
responsible for stimulating more nuanced views, such as sub-cluster temporal collinearity (Wang et al., 2017; Ferrier, 2019; see Chapter 9 by Gasiorowski et al.). Once
again wider taxon sampling has been key.
We are still quite some way from having a clear overview of collinearity, in terms
of what it actually constitutes, how it is achieved, and the diversity or universality of
mechanisms and processes that are under its umbrella. But we now have a clearer
prospect for resolving the issue(s) than ever before, with the rapid developments in
genome sequencing and functional genetics, all driven by the essential requirement
for wide taxon sampling, as clearly demonstrated in this book. This will go handin-hand with the continued development and refinement of the key techniques that
are integral to this science. Functional genetics in diverse species that do not have
a history of or amenability to classical genetic approaches was opened up by the
various approaches to RNA interference (RNAi) and is now experiencing a further
revolution with the application of the CRISPR/Cas technique (see the discussions
in Chapters 3 and 4 by Zattarra and Moczek, and Sharma, respectively). Genome
and transcriptome sequencing became more affordable, and hence feasible, with the
advent of so-called next-gen sequencing, and these rapid technical developments
have continued with the invention and wide application of such techniques as longmolecule sequencing and Hi-C sequencing to produce much better genome sequence
assemblies, often now to the level of whole chromosome resolution. This degree of
resolution is essential for robustly identifying linkage and clustering of genes like
the Hox genes and the genomic context that they evolved and function in (Pollard
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8
Hox Modules in Evolution and Development
and Holland, 2000; Garcia-Fernàndez, 2005; Butts et al., 2008; Ferrier, 2016a).
Understanding the significance of Hox gene organisation goes hand-in-hand with
understanding how the genes are expressed (in time and space) and what developmental functions this expression is entwined with. This is exemplified throughout
the chapters of this book.
1.5
AND THERE IS MORE
We have not been able to capture all of the research that is ongoing in the area of
Hox gene evo-devo and could easily fill another book (or more) with Hox research in
other taxa, impacting further evolutionary and developmental concepts and biological processes.
We could have included other parts of the animal kingdom, such as non-­bilaterians
(including sea anemones and jellyfish) to help understand the evolutionary transition between the diploblasts and triploblasts (or radially symmetrical and bilaterian
animals, depending on one’s perspective) (DuBuc et al., 2018; He et al., 2018). Or
even more basal lineages in the animal phylogeny, such as sponges (Porifera) and
comb jellies (Ctenophora) to understand the origin of the Hox genes themselves,
relative to other homeobox gene families (Mendivil Ramos et al., 2012; Fortunato
et al., 2014; Ferrier, 2016b). Also, the gnathostome vertebrates (such as the various
jawed fish) have been the source for important research on Hox paralog evolution
(or ohnolog evolution – ohnolog being the name given to paralogs produced from
WGD, in tribute to Susumo Ohno who first hypothesised a major role for WGD in
chordate evolution; Ohno, 1970; Wolfe, 2000) and morphological innovations such
as the paired appendages and digits, appendage positions, or varied vertebral transitions, to name but a few (Burke et al., 1995; Mallo, 2018; Moreau et al., 2019; Meyer
et al., 2021). We could also have explored the diversity of examples of evolution via
changes to Hox regulation versus changes to protein-coding sequences, as a major
route to exploring the debates about the relative balance of such changes in evo-devo
and how the gene regulatory networks (GRNs) containing Hox genes evolve (e.g.
Greer et al., 2000; Ronshaugen et al., 2002; Liu et al., 2019; Allais-Bonnet et al.,
2021; Lynch and Wagner, 2021). Also on a regulatory theme, research on the Hox
cluster of D. melanogaster was pioneering in discovering activities of non-coding
RNA genes (Sànchez-Herrero and Akam, 1989), which has blossomed into roles
for microRNAs, long non-coding RNAs and antisense RNA transcripts, with Hox
examples often leading the way for our understanding of how these ‘RNA’ genes
work (De Kumar and Krumlauf, 2016) (also see Chapters 2 and 5 by Karch and
Maeda, and Kuraku, respectively). This book is clearly to be viewed as a selective
sample of Hox evo-devo research.
1.6
CONCLUSION
A core theme of this book and Hox research is the comparative method. The power
of the comparative method is intrinsic to understanding fundamental aspects of
biology, such as pattern formation, cell fate determination, morphogenesis, GRNs,
homology and the origins of form in both ontogenesis and evolutionary time, and so
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Introduction to Hox Modules in Evolution and Development
9
how evolution has produced the incredible biodiversity that we see around us today
(as well as everything that has existed in the past and is now extinct). The scope and
power of this comparative method combined with the revolution of Hox genes cannot
be underestimated. Hox genes are now firmly established as fundamental elements in
two major traditional branches of biology, Developmental Biology and Evolutionary
Biology, and offer one of the most fertile and powerful integrated overlaps of the
two, which is now firmly established as the field of Evo-Devo. Hox gene research has
been truly revolutionary and shows every indication of continuing to be so.
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