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Published in final edited form as:

Dev Biol. 2017 July 15; 427(2): 241–250. doi:10.1016/j.ydbio.2016.11.008.

Pigeonetics takes flight: evolution, development, and genetics of

intraspecific variation
Eric T. Domyan1,* and Michael D. Shapiro2,*
1Department of Biology, Utah Valley University, Orem, UT
2Department of Biology, University of Utah, Salt Lake City, UT
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Abstract
Intensive artificial selection over thousands of years has produced hundreds of varieties of
domestic pigeon. As Charles Darwin observed, the morphological differences among breeds can
rise to the magnitude of variation typically observed among different species. Nevertheless,
different pigeon varieties are interfertile, thereby enabling forward genetic and genomic
approaches to identify genes that underlie derived traits. Building on classical genetic studies of
pigeon variation, recent molecular investigations find a spectrum of coding and regulatory alleles
controlling derived traits, including plumage color, feather growth polarity, and limb identity.
Developmental and genetic analyses of pigeons are revealing the molecular basis of variation in a
classic example of extreme intraspecific diversity, and have the potential to nominate genes that
control variation among other birds and vertebrates in general.
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Keywords
pigeon; genetics; pigmentation; feather; limb development; evolution

Introduction
“In the late summer or early autumn of 1859, Whitwell Elwin, editor of the respected British
journal the Quarterly Review, was sent an advance copy of a new book by the naturalist
Charles Darwin. Elwin… agreed that it had merit, but feared that the subject matter was too
narrow to attract a wide audience. He urged Darwin to write a book about pigeons instead.
‘Everyone is interested in pigeons,’ he observed helpfully.” (Bryson, 2003)
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Fortunately, Darwin did not follow Elwin’s advice, and On the Origin of Species by Means
of Natural Selection remains one of the most important volumes in the history of human
thought. Yet Darwin was indeed a pigeon aficionado and immersed himself in the pigeon
societies of London. His observations of the myriad breeds, as well as associations with
“eminent fanciers” (Darwin, 1859, p. 20), had a profound influence on how he chose to
communicate his ideas about how selection works (Baptista et al., 2009; Montgomerie,
2009; Secord, 1981; Theunissen, 2012). “Believing that it is always best to study some

*
Author for correspondence during review: Michael D. Shapiro, shapiro@biology.utah.edu, (801) 581-5690.
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special group, I have, after deliberation, taken up domestic pigeons… The diversity of the
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breeds is something astonishing,” he wrote in the Origin (Darwin, 1859). In Variation of

Animals and Plants under Domestication, he dedicated two chapters to this species, and
singled out pigeons in his Introduction to the two-volume set: “I have selected this case,
because, as we shall hereafter see, the materials are better than in any other; and one case
fully described will in fact illustrate all others” (Darwin, 1868, p. 1). Darwin noted that
based on morphology alone, a taxonomist might classify unique pigeon breeds as completely
different genera (see Fig. 1 for representative breeds, many of which were familiar to
Darwin), yet he also observed that all breeds, no matter how morphologically or
behaviorally divergent, could be interbred to produce viable offspring (Darwin, 1859;
Darwin, 1868). Therefore, he concluded, different breeds did not represent different species,
but were instead diverse descendants of Columba livia, the wild rock pigeon.

The rock pigeon was likely domesticated at least 5000 years ago in the Middle East and/or
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Mediterranean region, making it one of the oldest avian domesticates, and also the most
phenotypically diverse (Hansell, 1998; Levi, 1986; Price, 2002). Their feral descendants are
often disdained in urban environments (Jerolmack, 2008) by the very humans that create
ideal cliff-like habitats for them, provide them with plentiful food year-round, and are
largely responsible for their nearly worldwide distribution. Yet pigeons have also assumed
the roles of sacred religious symbols and war heroes (Hansell, 1998), and they are important
model organisms for research in parasitology, behavior, physiology, psychology,
neuroscience, microbiology, and other disciplines (Abs, 1983; Blaisdell and Cook, 2005;
Fagot and Cook, 2006; Harbison et al., 2009; Klopfleisch et al., 2006; Lauwers et al., 2013;
Mehlhorn and Rehkamper, 2009; Ros et al., 2011; Wagner et al., 2007). Here, we review the
motivation and recent progress towards understanding the genetic and developmental
mechanisms controlling pigeon diversity, including some of the same traits that struck
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“Darwin’s fancy” (Montgomerie, 2009).

Pigeon genetics: then and now

Shortly after the re-discovery of Mendel’s work, scientists began investigating the genetic
basis of trait variation in a large variety of organisms, of which today’s canonical model
organisms (e.g., mouse, chicken, fruit fly) represent only a subset. Indeed, the genetic basis
of trait variation in pigeon was studied by a number of researchers including W. Christie and
C. Wriedt (Norway), L. Cole (University of Wisconsin), W.M. Levi (Palmetto Pigeon Plant,
South Carolina), W.F. Hollander (Iowa State University), and even the renowned Drosophila
geneticist T.H. Morgan (Columbia University) (Christie and Wriedt, 1927; Cole, 1912;
Hollander, 1937, 1983; Levi, 1965, 1986; Morgan, 1911). These studies provided case
examples of such genetic phenomena as dominance, sex-linkage, sex differences in
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recombination frequency, and genetic mosaicism (Cole, 1912; Cole and Kelley, 1919;
Hollander and Cole, 1940). Among the hobbyist community, an interest in pigeon genetics
has continued to the present day, and results of experimental crosses are reported on citizen
scientist websites and in newsletters. In academic circles, however, pigeon genetics grew out
of favor in the mid-20th Century, perhaps in part due to the development of molecular
genetic tools for a limited set of model genetic organisms. A notable exception to this trend
was W.F. Hollander, who continued to study pigeon genetics professionally and as a

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hobbyist until his passing in 2004 (Hollander, 1983; Hollander and Mangile, 1994). Sell
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(1994, 2012) provides outstanding and current summaries of most known genetic variants.

In more recent years, technological advances and precipitous price drops in next-generation
sequencing have allowed biologists to revisit many of the early, classical pigeon genetic
experiments, this time employing modern genomic, genetic, and developmental biology
techniques. The rock pigeon now has a high-quality reference genome, additional re-
sequenced genomes representing a wide variety of breeds (NCBI Bioproject
PRJNA284526), a catalog of over 25 million SNPs and genomic structural variants across
breeds, and a draft genome-wide linkage map (Domyan et al., 2014; Domyan et al., 2016;
Shapiro et al., 2013). These extensive resources, combined with standard experimental
techniques developed for canonical model systems, make the pigeon a viable model to
understand the genetic basis of phenotypic variation, and to test the developmental
consequences of these genetic variants in developing embryos.
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Why study molecular genetics and development in pigeons?

Pigeons offer several advantages as a model to understand the molecular basis of avian and
vertebrate diversity. First, pigeon breeders have selected for dramatic variation over the past
several thousand years in numerous plumage, anatomical, and behavioral traits that are
represented in over 350 breeds (Baptista et al., 2009; Darwin, 1868; Levi, 1965; Price, 2002;
Shapiro and Domyan, 2013). As a result, the extent of variation between breeds can
approach the number and extent of differences typically observed between different species
(Darwin, 1859; Price, 2002).

Second, pigeons are easy to breed, and virtually all varieties can be successfully interbred to
produce fertile offspring. This is a critical strength because it permits traditional genetic
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mapping experiments using birds with highly divergent phenotypes. In contrast, hybrid
incompatibility typically precludes genetic mapping studies between wild species. Levi
(1965, 1986) and many others summarize reproduction and husbandry techniques, with key
aspects mentioned here. Healthy females can potentially lay a clutch of two eggs every 10
days, if the eggs are removed after laying. Pigeon hobbyists commonly remove eggs from
their parents’ nest and place them with foster parents, thereby allowing the first set of
parents to produce additional offspring. Gestation is shorter in pigeon (17–19 days at
37.5°C) than in chicken (21 days at 37.5°C), and pigeon hatchlings are altricial. Both male
and female parents share nesting duties and produce a substance known as “crop milk” to
feed to newly-hatched squabs. Crop milk meals gradually transition to regurgitated seeds
until the young can feed on their own. Typically, juvenile pigeons are weaned after 3–4
weeks, and reach sexual maturity at approximately 6 months of age. The small body size of
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pigeons also allows large crosses to be kept in a manageable space.

Third, classical studies show that the genetic architecture of many traits in pigeons is
probably oligogenic (Hollander, 1937, 1983; Levi, 1986; Morgan, 1911; Sell, 1994, 2012),
thereby increasing the chances of mapping and cloning the genes responsible for differences
among breeds. Furthermore, relatively complex traits (feather color, for instance) can
sometimes be genetically teased apart into discrete components (e.g., by treating the type

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and intensity of melanin as separate traits), thereby facilitating mapping of each component
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(Domyan et al., 2014).

Fourth, many variable traits in pigeons are also variable among birds in general (Baptista et
al., 1997; Darwin, 1868; Price, 2002), providing a critical entry point to finding the genes
that control variation in the wild. For example, Baptista et al. (2009; 1997) noted the striking
similarities between many breeds of domestic pigeon and wild columbids, and proposed that
the same genes might control derived phenotypes in naturally and artificially selected birds.

Fifth, many derived traits in domestic pigeons are constructive rather than regressive; that is,
they represent phenotypes that are absent in the wild ancestor (Stringham et al., 2012).
Although regressive traits have attracted considerable attention in vertebrate evolutionary
genetics, the genetics of constructive traits are less understood (Miller et al., 2014). Pigeons
present a prime opportunity to address this gap.
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Finally, phenotypic convergence is rampant among breeds, with similar traits under selection
in breeds that are not necessarily genetically similar (National_Pigeon_Association, 2010;
Stringham et al., 2012). This situation offers a rich set of animal resources to test whether
the same or different genes – and the same or different mutations in those genes – underlie
this phenotypic similarity. Understanding how these similarities arise is an area of intense
interest in evolutionary developmental biology and genetics (Christin et al., 2010; Hovav et
al., 2008; Martin and Orgogozo, 2013; Paterson et al., 1995; Rosenblum et al., 2014; Stern,
2013; Vickrey et al., 2015).

In short, pigeons are amenable to a combination of classical breeding strategies and

genomics to dissect different components of complex phenotypes and define functional
interactions among genes. Notably, equivalent insights about the genetic architecture of
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phenotypic divergence between wild vertebrate species are often very difficult to acquire.

Practical pigeon breeding – advantages for genetic association studies

As with show dogs, fancy mice, orchids, and a multitude of other domestic species, fancy
pigeons are typically bred to compete at shows. Pigeon breeds have strict breed standards,
but no pedigree requirements (e.g., parents and grandparents need not be registered members
of a breed) (National_Pigeon_Association, 2010). Due to these strict standards, different
individuals within a breed are – not surprisingly – genetically very similar (Shapiro et al.,
2013; Stringham et al., 2012). However, breeds that are phenotypically highly divergent also
show genetic signatures of shared ancestry, which is also expected given the recent
divergence time among breeds (Shapiro et al., 2013; Stringham et al., 2012). Some of this
genetic similarity also likely results from introgression of traits from one breed to another.
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Introgression and hybridization among breeds have two fortunate consequences for the
molecular geneticist. First, introgression raises the possibility that the same mutations were
repeatedly passed from breed to breed. If this is the case, then we should expect to detect the
same haplotype blocks in multiple breeds with the same trait. Second, hybridization of two
(or more) breeds followed by backcrossing to remove undesirable donor traits from recipient
breeds should break long haplotype blocks in the genome. Therefore, instead of having near-

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isogenic inbred lines, pigeons with similar traits might share identical – but small –
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haplotypes in different genetic backgrounds. Both of these factors contribute to the power of
genome-wide association mapping across breeds. Below, we highlight recent progress using
these strategies to identify the genes and molecular mechanisms that underlie morphological
diversity among breeds.

The molecular basis of phenotypic variation in pigeons

Head crests
Price (2002) likened the process of artificial selection on birds under domestication (breeder
choice) to sexual selection in the wild (typically female choice). The types of traits selected
in both cases – color, head crests, and other ornamental, structural, and behavioral variants –
also show remarkable parallels. Head crests of various kinds are found in numerous wild and
domesticated avian species and can serve important functions in mate choice (Amundsen,
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2000; Price, 2008; Price, 2002). By analyzing the genomes of a variety of pigeon breeds, we
identified a single-nucleotide coding mutation in the highly conserved intracellular kinase
domain of EphB2 that is perfectly associated with crests of reversed feathers on the head
(Shapiro et al., 2013; Fig. 2). All crested pigeons appear to share the same mutant haplotype
as a result of introgression among breeds. EphB2 is involved in numerous aspects of
vertebrate development, including feather development, palate morphogenesis, melanocyte
migration, tissue polarity, and axon pathfinding (Henkemeyer et al., 1996; Kelsh et al., 2009;
Risley et al., 2009; Suksaweang et al., 2012; Xu et al., 2000). However, because only the
kinase domain is affected in crested pigeons (Shapiro et al., 2013), forward signaling should
be disrupted, but reverse signaling (through ephrin ligands) should be intact (Mendes et al.,
2006). The EphB2 mutation is found in pigeons with different crest phenotypes – both the
area comprising the crest and the length of its feathers can vary – so other modifier loci
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likely contribute to the extent of crest formation. Developmentally, head crests in domestic
pigeons originate as a reversal of feather placodes on the head and neck (Shapiro et al.,
2013). Head crest development in domestic chickens, in contrast, comprises elongation of
head feathers but not a change in the direction of growth, and is not associated with EPHB2,
but instead with ectopic expression of HOXC8 (Wang et al., 2012).

Baptista (2009) predicted that derived traits in pigeons and other columbids might have a
similar genetic basis. In another domesticated columbid species, the crested ringneck dove
(Streptopelia risoria), this appears to be the case (Fig. 2). As in domestic pigeons, crested
ringneck doves have an amino acid substitution at a highly conserved residue in the catalytic
site of the EPHB2 kinase domain (Vickrey et al., 2015). Both mutations produce kinase-dead
versions of EPHB2, yet the amino acid substitutions found in pigeon and ringneck dove are
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separated by more than 100 residues and are predicted to have different effects on protein
function. The pigeon mutation is predicted to destabilize the active site by breaking a critical
salt bridge, while the dove mutation likely hinders entrance of ATP into the catalytic domain
(Carrera et al., 1993; Hemmer et al., 1997; Vickrey et al., 2015). Thus, different mutations in
the same gene result in similar phenotypes in two columbid species that diverged over 20
million years ago (Goodwin, 1983; Pereira et al., 2007).

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Plumage color
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Whether for aesthetic or practical reasons, or a combination of the two, the genetic basis of
pigmentation has been one of the most-intensively investigated fields in pigeons and other
vertebrates (Domyan et al., 2014; Hubbard et al., 2010; Manceau et al., 2010; Rosenblum et
al., 2014; Sulem et al., 2007). Pigeons display a tremendous amount of color variation, and
rely on essentially the same pigmentation system as mammals; by varying the absolute and
relative amounts of black eumelanin and red pheomelanin, a wide variety of colors can be
generated (Haase et al., 1992). In addition to being a visually pleasing phenotype to
breeders, color variation also has relevance in free-living populations of pigeons, as color
variants are correlated with differences in parasite load, juvenile survivorship, and predator
avoidance (Jacquin et al., 2011; Jacquin et al., 2012; Jacquin et al., 2013; Palleroni et al.,
2005; Recapet et al., 2013).
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For more than a century, transmission genetic experiments have provided clues about the
number of color genes and alleles, their dominance and epistatic relationships, and their
cumulative effects on melanin phenotype (Hollander, 1937, 1983; Levi, 1986; Sell, 1994,
2012). For example, classical studies show that the basic or “ground” color locus B is sex-
linked and has three alleles: a wild-type allele (B+) that causes primarily black eumelanin to
be deposited on feathers, a dominant ash-red allele (BA) that results in red pheomelanin, and
a recessive brown allele (b) that primarily produces eumelanin (Fig. 3; Cole, 1912; Cole and
Kelley, 1919; Haase et al., 1992; Hawkins, 1931; Steele, 1931). Using a combination of
genomics and breeding experiments, tyrosinase-related protein 1 (Tyrp1), which encodes a
melanin biosynthesis enzyme, was identified as the B locus (Domyan et al., 2014). All ash-
red birds tested to date harbor the same Tyrp1 haplotype, suggesting that this trait was
transferred to different breeds via hybridization and introgression. The BA allele has a single
missense mutation in Tyrp1 that is predicted to cause an alanine-to-proline substitution in
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the TYRP1 signal peptide, which greatly diminishes cleavage of the mature protein
(Domyan et al., 2014). While the cellular consequences of this processing defect are
unknown, a similar cleavage site mutation in the corn gene fl2 causes the encoded protein to
be retained in the ER (Coleman et al., 1995; Gillikin et al., 1997), suggesting a similar fate
for the ash-red version of TYRP1. How misprocessing of TYRP1 causes such a dramatic
shift in pigment type, even in the presence of the wild-type allele, is an area of active
investigation. Given the dominant inheritance pattern of the ash-red phenotype, either
dominant-negative or neomorphic functions are likely.

Sequencing of Tyrp1 in brown birds, the other derived phenotype at the classic B locus,
revealed a surprising amount of allelic heterogeneity: three distinct mutant alleles were
identified among breeds (Domyan et al., 2014). All three mutations (two frameshift and one
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nonsense) are predicted to result in null alleles, consistent with Tyrp1 inactivation
phenotypes in other vertebrates (Hubbard et al., 2010; Jackson, 1988). Collectively, variation
at the B color locus in pigeons shows a wide range of effects on color. This includes the
dominant BA allele that causes a shift from eumelanism to pheomelanism, and recessive b
alleles that arose at least 3 times within the rock pigeon.

Like the dominant ash-red (BA) allele of Tyrp1, an autosomal mutation known as recessive
red (e) also causes red feathers, and is epistatic to the B locus (Cole and Kelley, 1919; Haase

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et al., 1992). Consistent with these classical genetic results, recessive red birds have reduced
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expression of the gene Sox10 (Domyan et al., 2014), which encodes a transcriptional
activator of Tyrp1 (Murisier et al., 2006). This downregulation is associated with two
distinct, partially overlapping deletions of a known melanocyte enhancer of Sox10 in
recessive red birds species-wide. It remains unclear why recessive red pigeons are red,
however, given that the Tyrp1 loss-of-function phenotype is brown rather than red. This
disparity strongly suggests that additional targets of SOX10 are also misregulated in the
melanocytes of recessive red birds.

A third mutation, at the sex-linked dilute (d) locus (Cole, 1912; Cole and Kelley, 1919;
Haase et al., 1992), is in a gene encoding a melanosomal solute carrier, Slc45a2, and is
associated with lightened feather color (Domyan et al., 2014). This mutation is predicted to
cause a histidine-to-arginine substitution in one of the protein’s transmembrane domains,
presumably altering its ability to transport substrate across the melanosomal membrane.
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One of the most-intensively studied pigmentation genes in vertebrates is melanocortin-1-

receptor (Mc1r), which has been implicated in color variation in many organisms, including
humans (Andersson, 2009; Gross et al., 2009; Hoekstra, 2006; Manceau et al., 2010; Mundy,
2005; Rosenblum et al., 2014; Sulem et al., 2007). Analysis of Mc1r sequences in feral
pigeons with different color phenotypes did not identify an association between Mc1r
genotype and pigment variation (Derelle et al., 2013). However, a second study found that a
Val85Met substitution in MC1R was weakly associated with pheomelanism in domestic
populations (Guernsey et al., 2013). Functional assays in cell culture demonstrate that the
Val85Met allele is a hypomorph, and is correlated with reduced MC1R protein localization
at the plasma membrane. Paradoxically, the same amino acid substitution is strongly
associated with eumelanism in two other avian species (Baiao et al., 2007; Mundy et al.,
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2004). However, the contradicting associations are difficult to reconcile without functional
tests of Val85Met alleles from these other species.

Together, variation in Tyrp1, Sox10, and Slc45a2 accounts for some of the most common
melanin phenotypes in pigeons. The various combinations of genotypes at these three loci
generate a broad spectrum of color diversity through both coding and regulatory mutations.
A large number of modifier pigment loci also contribute to color variation (Levi, 1986; Sell,
1994, 2012), and an important line of future research is to determine their molecular
identities and interplay with the already-identified loci.

Feathered feet
In domestic pigeons, the epidermis of the ankle and foot can be completely scaled or
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covered with feathers (Fig. 4). Classical breeding experiments demonstrate that diversity in
epidermal appendage type is governed by a small number of loci (Doncaster, 1912;
Hollander, 1937, 1983; Wexelsen, 1934). This epidermal variability is reminiscent of
interspecific variation among wild birds, as some raptor and boreal species have feathered
feet (e.g., some ptarmigans and owls). Previous studies of chicken development and genetics
suggest changes in dermal-epidermal interactions as a mechanism governing the decision
between scaled and feathered epidermis (Chang et al., 2004; Crowe et al., 1998; Dorshorst et
al., 2010; Harris et al., 2002; Harris et al., 2004; Somes, 1992; Zou and Niswander, 1996).

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Recent findings about the molecular basis of epidermal variation in pigeons, however,
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suggest a more fundamental developmental basis (Domyan et al., 2016).

Darwin’s observations of heavily feathered pigeon feet (“muffs” in the parlance of

hobbyists) provide some of the earliest anatomical clues about the potential molecular
mechanisms that govern the transition from scaled to feathered epidermis. For example, he
noted the feet of the English trumpeter breed were “so heavily feathered, they almost appear
like little wings,” and, “pigeons with feathered feet very generally have the bases of their
outer toes connected by skin” (Darwin, 1868). Furthermore, in the heavily muffed English
trumpeters, the first digit of the foot (homologous to the big toe of humans) is sometimes
rotated forward, rather than pointing backward as in other pigeons (Domyan et al., 2016).
Together, these lines of anatomical evidence suggest forelimb-like traits in the hindlimbs of
muffed birds, and support a model that the underlying mutations causing feathered feet are
not simply altering the fate of individual epidermal placodes, but instead are altering
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hindlimb identity itself.

Consistent with a model of limb identity change, and with the small number of large-effect
loci predicted by classical experiments, whole-genome scans of allele frequency
differentiation showed that two loci are associated with the conversion of scaled to feathered
epidermis across multiple pigeon breeds (Domyan et al., 2016). The first region contains the
transcription factor Pitx1, a critical determinant of hindlimb identity and morphology
(Duboc and Logan, 2011; Logan and Tabin, 1999; Szeto et al., 1999). Variation at the Pitx1
locus also underlies the repeated evolution of pelvic reduction in two species of stickleback
fish (Chan et al., 2010; Coyle et al., 2007; Cresko et al., 2004; Shapiro et al., 2006; Shapiro
et al., 2004; Shikano et al., 2013). The second genomic region contains the transcription
factor Tbx5, which plays key roles in forelimb bud outgrowth and identity (Duboc and
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Logan, 2011; Hasson et al., 2007; Hasson et al., 2010; Minguillon et al., 2005; Rallis et al.,
2003; Rodriguez-Esteban et al., 1999; Takeuchi et al., 1999; but see Minguillon et al., 2005).
In an F2 laboratory cross, genetic markers for Pitx1 and Tbx5 co-segregate with the extent of
feather coverage on the foot and the length of foot feathers, respectively, providing
independent confirmation of the association between phenotype and genotype.

Studies of pigeon diversity can move beyond genetic associations to measure the effects of
allelic variants during embryonic development. In embryos of feather-footed birds, Pitx1
hindlimb expression levels are reduced relative to embryos of scaled birds. In contrast, Tbx5,
which is normally not expressed in the vertebrate hindlimb, is expressed ectopically in the
hindlimbs of feathered-foot embryos. Allele-specific expression tests in hybrid embryos of
scale- and feather-footed parents show that these differences in Pitx1 and Tbx5 expression
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result from cis-regulatory changes. Surprisingly, ectopic expression of Tbx5 is not diffuse
throughout the hindlimb, as is the endogenous pattern in the forelimb. Instead, it is expressed
robustly at the posterior aspect of the limb bud, which is the site of outgrowth of the largest
foot feathers (Fig. 4). Remarkably, feather-footed chicken embryos also manifest ectopic
expression of TBX5 in the posterior hindlimb, due (at least in part) to a cis-regulatory
change (Domyan et al., 2016). Thus, feathered feet in two domestic bird species are
associated with tissue-specific regulatory changes in key limb development genes.

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Taken together, these anatomical, genetic, and developmental data suggest that the feathered
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legs and feet of muffed pigeons result from the partial transformation of hindlimbs into
forelimbs, and that this is due to cis-regulatory changes in two crucial determinants of limb
identity and outgrowth (Fig. 4). Notably, some dinosaurs and basal birds had nearly
completely feathered hindlimbs, including large, muff-like feathers on the posterior aspect of
the leg and foot (Foth et al., 2014; Godefroit et al., 2014; Hu et al., 2009; Turner et al., 2012;
Xu et al., 2003; Zheng et al., 2013). Although scales replaced these distal feathers in modern
birds, feather-footed pigeons, chickens, and other species demonstrate that bird feet are still
competent to form feathers when given the appropriate molecular signals. Thus, by
understanding the molecular changes that can lead to the gain of feathers in modern pigeons,
we might also begin to understand the genetic and developmental changes that led to the loss
of foot feathers in proto-avian dinosaurs and basal birds.
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Discussion
A novel entry point to general mechanisms of variation
Studies of pigeons illustrate how comparative genomics can inform developmental analyses
to discover the molecular basis of variation. Notably, many of the traits that vary among
pigeons also vary among other avian species (Baptista et al., 2009; Price, 2002).
Complementary genetic, genomic, and developmental approaches are enabling the rapid
discovery of the molecular basis of astonishing variation among pigeons, thereby opening
new avenues to understand the potential roles of specific genes in variation among
vertebrates in general (Baptista et al., 2009; Domyan et al., 2016; Vickrey et al., 2015). The
limited fecundity of females and dearth of commercial hatcheries makes obtaining material
for embryonic manipluation more difficult in pigeon than in chicken, but embryos of both
species develop in ovo, and we expect that gene perturbation technologies developed for
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chicken will be readily-transferrable to the pigeon model, as well.

Future work holds promise to exploit the remarkable diversity of pigeons to define the
genetic and developmental basis of additional phenotypic variation. For example, pigeon
breeds differ in body mass by more than an order of magnitude (Levi, 1965). In addition,
craniofacial variation is extreme within this species, ranging from the inconspicuous beak of
the pigeon breed dubbed the African owl to the curved, buzzard-like face of the Scandaroon
(Fig. 1C,D) (Levi, 1965). While we now have a better understanding of how different
pigment types are specified, we know considerably less about how these pigments are
deposited to generate color patterns within and among feathers (Lin et al., 2013; Willier and
Rawles, 1940). Together, color pattern and pigment traits in myriad vertebrate species have a
profound influence on mate choice, species recognition, and crypsis – traits that are probably
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under selection in free-living pigeon populations as well (Jacquin et al., 2012). Pigeons also
offer numerous opportunities to understand the genetic basis of intriguing behaviors
(Darwin, 1868; Hollander and Mangile, 1994; Sell, 1994). Of particular interest, rolling is a
heritable behavior in which pigeons uncontrollably perform backward somersaults while in
flight or when trying to initiate flight; it was described by Darwin (1868) as “one of the most
remarkable inherited habits or instincts ever recorded” (p. 150). This behavior might be
rooted in changes to serotonin signaling (Smith et al., 1987), providing a potential model for

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serotonergic control of skeletal muscle. In summary, selection in pigeons has produced an

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unusually broad exploration of morphospace for a single species, thereby providing ample
opportunities to understand the genetic and developmental basis of variation.

Importance of domesticated animals in understanding evolutionary diversity

Domesticated species are important models for rapid evolutionary change over short time
scales (Akey et al., 2010; Andersson, 2009; Boyko et al., 2010; Driscoll et al., 2009; Gaut,
2015; Price, 2002; Ross-Ibarra et al., 2007). Some of the same evolutionary processes that
operate during selective sweeps and sexual selection in natural populations also shape
domestic populations (Andersson, 2009; Careau et al., 2010; Gregory, 2009; Price, 2008;
Price, 2002). Like their wild ancestors, domesticated species have undergone genetic
adaptation to various climates and living conditions, including human preferences, making
them excellent models for variation under natural selection and divergence by prezygotic
Author Manuscript

isolation (Andersson, 2009; Driscoll et al., 2009; Hartl and Clark, 2007).

Furthermore, studies of domesticated species have led to the surprising realization that the
same genes are sometimes involved in cases of natural and artificial selection. For example,
derived alleles of Mc1r are associated with color variants not only in domestic cows, pigs,
pigeons, and sheep, but also in wild populations of mammals, reptiles, birds, and fish
(Andersson, 2009; Gross et al., 2009; Guernsey et al., 2013; Hoekstra, 2006; Manceau et al.,
2010; Mundy, 2005; Rosenblum et al., 2014). In domestic dogs, variation at the IGF1 locus
is associated with variation in body mass and age of death (Jones et al., 2008; Sutter et al.,
2007), and this same gene plays critical and conserved roles in variation in body size and
longevity in other vertebrates as well (Suh et al., 2008). Further illuminating the genetic
basis of derived traits in domesticated and natural populations will help resolve whether
selection is biased toward repeated changes in the same genes, or whether multiple
Author Manuscript

developmental pathways are utilized in the repeated evolution of derived phenotypes.

Acknowledgments
We thank Elena Boer, Rebecca Bruders, Emily Maclary, and Anna Vickrey for discussions and comments on drafts
of the manuscript; and Sydney Stringham for images in Figs. 1 and 2. This work was supported by National
institutes of Health grant R01GM115996 and NSF CAREER award DEB1149160 to M.D.S.

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• Domestic rock pigeons display dramatic variation within a single species.

• Pigeons are amenable to genetic, genomic, and developmental studies of

diversity.

• The molecular basis for several classic traits is now known.

• Variation in pigeons is relevant to other evolutionary and biomedical

phenotypes.

• Pigeons can reveal general mechanisms of avian and vertebrate diversity.

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Fig. 1.
Variation among domestic pigeon breeds. A, frillback; B, Old German owl; C, African owl;
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D, Scandaroon; E, English trumpeter; F, Indian fantail; G, archangel; H, fairy swallow; I,

Old Dutch Capuchin; J, figurita; K, English pouter. Images are not to scale. Photo credit:
Sydney Stringham.
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Fig. 2.
Head crests in domestic pigeons and ringneck doves. A. The simple “peak” crests of both
species are associated with different amino acid substitutions in the kinase domain of
EphB2. B. Pigeons also have elaborate crests, such as the mane of the Old Dutch Capuchin,
that require contributions from modifier loci. The molecular identities of these additional
loci are unknown. C. Occipital region of an English trumpeter embryo shows reversed
growth trajectory of crest feathers (arrowheads). Feathers have a rostral instead of caudal
orientation. The top of the head is at the upper right of the frame, beak is to the lower right
(out of frame). e, eye. Photo credits for A, B: Sydney Stringham.
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Fig. 3.
Interactions among 3 loci produce 8 different melanin phenotypes. Allelic variation at Tyrp1
determines blue (wild-type), ash-red, or brown base color. The d allele of Slc45a2 reduces
the intensity of the base color. Recessive red pheomelanism results from regulatory
mutations at the Sox10 locus. Consequently, its downstream target Tyrp1 – and probably
other pigmentation genes (PGs) – is also downregulated. Modified from Domyan et al.,
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2014.
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Fig. 4.
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Developmental and genetic basis of feathered feet in pigeons. A–D. Ontogeny of the
feathered-foot phenotype. A. Hamburger-Hamilton (Hamburger and Hamilton, 1951) stage
25 English trumpeter pigeon embryo showing ectopic expression of Tbx5 (arrows), a gene
that normally is expressed in the forelimb (f) but not in the hindlimb (h). B. Lateral view of
right hindlimb of late-stage English trumpeter embryo, showing elongated feather buds on
the toes (arrows). C. Juvenile English trumpeter with large foot feathers (arrows). D.
Comparison between scaled foot of a racing homer (left) and feathered foot of an English
trumpeter (right). Feathers have been removed, but the large insertion points of lateral
feathers on digit 3 are visible (arrowheads) and hide digit 4. Digit 1 is rotated anteriorly,
unlike the posterior-facing digit 1 of the scaled breed (arrows). E. Two genomic regions are
associated with foot feathering among pigeon breeds. Scaffold 79 contains Pitx1 and
scaffold 70 contains Tbx5. F. Gene-expression model of epidermal appendage variation
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among pigeons. Grouse is associated with slight downregulation of Pitx1, which is

transformed into small muff by synergy with ectopic Tbx5 expression. Large muff results
from more-severe misregulation of both genes. f, forelimb. Modified from Domyan et al.,
2016.

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Table 1

Summary of known molecular bases of trait variation in pigeons

Trait Symbol Gene Coding or regulatory Molecular & developmental correlates Notes (Reference)
Head crest cr EphB2 coding Salt bridge disrupted in kinase domain, reversed polarity Coding change in EphB2 associated with crest in ringneck dove (Shapiro
of feather placodes et al., 2013)

Ash-red Tyrp1 coding Signal peptide cleavage site disrupted, mislocalization

Domyan and Shapiro

BA Dominant to B+ WT allele (Domyan et al., 2014)

of pigment sythesis

Brown b Tyrp1 coding Nonsense/missense mutations, decay of mRNA b alleles evolved at least 3 times (Domyan et al., 2014)
Recessive red e Sox10 regulatory Deletions of melanocyte enhancer, downregulation of e alleles evolved at least 2 times; epistatic to B (Domyan et al., 2014)
Tyrp1
Dilute d Slc45a2 coding Substitution in transmembrane domain, functional effect Same gene associated with pigment dilution in several vertebrates
unknown (Domyan et al., 2014)

Pheomelanism NA Mc1r coding Substitution in intracellular loop, reduced plasma Same Val85Met substitution associated with eumalanism in other birds
membrane-integrated protein (Guernsey et al., 2013)

Grouse gr Pitx1 regulatory Usually associated with 44-kb upstream deletion, Synergizes with Sl to form muffs, second allele likely (Domyan et al.,
controls extent of foot feathering 2016)

Slipper Sl Tbx5 regulatory Ectopic enhancer activity and hindlimb expression, Synergizes with gr to form muffs (Domyan et al., 2016)
controls extent and size of foot feathers

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 Domyan and Shapiro
Selected derived and variable traits in domestic pigeons and their evolutionary and/or biomedical relevance;
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see Baptista et al. (2009) and Price (2002) for further discussion of avian traits
Trait in pigeon
Head crest
Foot feathers
Feather color (melanin type)
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Color pattern (melanin
distribution)
Beak morphology
Rolling behavior
Body size
Eye and nasal ceres
Supernumerary tail feathers
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Homing behavior
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Table 2
Identified Evolutionary and/or biomedical relevance
loci (where
applicable)
Ephb2 Avian head crests, sexual selection,
directionality of epidermal appendage
outgrowth, cell migration, palate development,
axon guidance, prostate and colorectal cancer
Pitx1, Tbx5 Epidermal appendage and limb identity,
feathered feet of dinosaurs and birds, pelvic
reduction in sticklebacks, clubfoot,
Liebenberg and Holt- Oram syndromes
Tyrp1, Plumage, hair, and skin color diversity;
Sox10, crypsis and mate choice; melanoma risk
Slc45a2,
Mc1r
Plumage, hair, and skin color diversity;
crypsis and mate choice; melanocyte
migration and survival, piebaldism; vision
defects associated with at least 2 pattern
phenotypes in pigeons
Adaptive diversity in craniofacial structures
(including beaks), craniofacial developmental
disorders
Neurotransmitter and stereotypic behavior
patterns
Body size
Ornamentation and mate choice, epidermal
growth
Epidermal placode specification
Navigation and migration
Page 25
Selected References
(Baptista et al., 1997; Fu et al., 2009;
Henkemeyer et al., 1996; Huusko et al.,
2004; Kelsh et al., 2009; Risley et al.,
2009; Vickrey et al., 2015)
(Adachi et al., 2016; Al-Qattan et al.,
2013; Chan et al., 2010; Gurnett et al.,
2008; Postma et al., 2008; Shapiro et al.,
2004)
(Lao et al., 2007; Pho and Leachman,
2010; Rosenblum et al., 2014; Sturm,
2009; Tully, 2007)
(Fleischman, 1992; Fleischman et al.,
1991; Hollander, 1983; Levi, 1986; Lin et
al., 2013; Linnen et al., 2013; Singh and
Nusslein-Volhard, 2015)
(Abzhanov and Tabin, 2004; Helms and
Brugmann, 2007; Hu et al., 2015;
Schneider, 2007; Smith et al., 2015)
(D’Souza and Craig, 2008; Darwin, 1868;
Mowrer, 1940; Smith et al., 1987)
(Durand and Rappold, 2013; Lettre, 2013;
Wood et al., 2014)
(Lahaye et al., 2014)
(Houghton et al., 2005; Houghton et al.,
2007; Morgan, 1911)
(Beason and Wiltschko, 2015; Edelman et
al., 2015; Guilford and Biro, 2014; Treiber
et al., 2012)