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recurved beak of the Scandaroon Quick guide (Figure 1A,B); many breeds have elaborate feather ornaments, such as the Jacobin breed favored by Queen Domestic pigeons Victoria (Figure 1D); and extremes in body mass among breeds differ by an Michael D. Shapiro order of magnitude. and Eric T. Domyan When and where were they domesticated? By genetic measures, “That man is fortunate who finds domestic breeds are only weakly in his breast an inexplicable love differentiated. This could be partly due for them [pigeons]…When fortune to crosses among breeds to ‘improve’ frowns and when the cares of a harsh traits such as plumage pigmentation or disordered world seem almost and pattern, or to transfer traits among too heavy to bear…then the pigeon breeds. The precise number and timing lover finds in his birds a solace and of domestication events could be consolation impossible to describe.” forever obscured by this widespread — Levi, The Pigeon, p 34 hybridization and introgression. Rock pigeons are native to Europe, What are domestic pigeons? North Africa, the Middle East, and While several of the approximately South Asia, and they were probably 300 species of pigeons and doves domesticated at several times and (family Columbidae) are kept as pets, places. Archeological evidence points the term domestic pigeon usually to human use of pigeons as a food refers to breeds of Columba livia, source as early as the Pleistocene the rock pigeon. Pigeon breeding (~10,000 years ago) in the Fertile is a popular hobby worldwide, Crescent, though whether this entailed and over 350 different breeds are domestication is not known. Ancient currently recognized. Their ubiquitous Egyptians began using pigeons for association with humans over the ceremonial and culinary purposes millennia pervades literature, visual at least 4000 years ago, and later arts, and religious symbolism, and as harbingers of the progress of the they have also served as steadfast Nile’s annual flood. Ancestors of messengers during war and peacetime. some modern breeds such as the As with dogs, chickens, and other resplendent fantails (Figure 1E) and domesticated animals, the huge enormous, amusingly-named runts variety of domestic pigeons represents were probably developed at least 860 a large-scale selection experiment and 2000 years ago, respectively. that started thousands of years ago. The temporal origins of many other Domestication involves intensive fancy breeds are lost to antiquity, but directional selection for particular the ancient geographic centers of phenotypes, followed by stabilizing or domestic pigeon diversity appear to Figure 1. Diversity among breeds of domestic purifying selection; similar evolutionary be the Middle East and South Asia pigeons (Columba livia). Variation among pigeon breeds is often of the processes operate during selective (modern India and Pakistan). Moreover, magnitude observed among different spe- sweeps and sexual selection in birds were exchanged between cies of birds, including beak size extremes natural populations. In pigeons, these these two regions in the 16th Century of the (A) African owl and (B) Scandaroon; processes have produced arguably the (and probably earlier), providing (C) the head crest of the Old German owl and greatest phenotypic diversity within ample opportunity for hybridization (D) hood of the Jacobin; (E) supernumerary any single avian species. among breeds. Writings from the 16th and elevated tail feathers of the fantail; and (F) scales versus (G) feathers on the lower leg Some pigeon breeds are under century and earlier discuss derived and foot of the Brunner pouter and English intensive selection for flight morphological and behavioral traits pouter, respectively. (Photos in (A–D) modified characteristics: racing homers can and breeds that persist today. In from Stringham et al. (2012); original images navigate to their home lofts after being Europe, the popularity of the pigeon in (A) and (D) courtesy of Thomas Hellmann.) released from hundreds of miles away; hobby rose markedly in the 17th the tippler can remain continuously Century, and artistic depictions of aloft for more than 20 hours; and some domestic breeds from this era fascinated humans, and pigeons tumblers and rollers perform backward already closely resemble modern have served as message bearers somersaults in flight. Others are forms. for millennia. For example, Julius bred for vocal traits and striking Caesar used pigeons to communicate morphological differences (Figure 1). What are homing pigeons and how to Rome his victory over Gaul, For example, facial morphology in do they navigate? The rock pigeon’s and the pigeon’s role in military pigeons ranges from the tiny beak innate ability to navigate to its home communication persisted well into the of the African owl to the massive, loft over unfamiliar terrain has long 20th Century. Magazine R303

The modern racing homer breed is a selection has resulted in their close variation in several traits shows similar surprisingly recent creation, however, morphological resemblance to the trends in distantly related breeds, and was generated independently wild rock pigeons of the Old World. making it possible to test whether the and contemporaneously in Belgium Molecular evidence suggests that the same or different genes underlie similar and England in the early 1800s by racing homer, a breed that has regular phenotypes in different breeds, a topic the hybridization of several different opportunities to fly outside the loft of longstanding interest in studies breeds, followed by interbreeding of and potentially escape, is a major of biodiversity in domesticated and these two racing strains. genetic contributor to some North natural populations. Today, pigeon racing is a popular American feral populations. A reference genome sequence of the sport worldwide, and prize purses of rock pigeon was recently assembled, thousands of dollars are common. Why did Darwin value domestic thereby facilitating exploration of the Racing is serious business: the top pigeons? The rock pigeon is molecular origins of diversity within price paid for an individual racing generally held in low regard by most and among breeds. For example, by pigeon was £207,000 ($328,000) in ornithologists, but this species has sequencing the genomes of breeds 2012! Generations of intense selection a special place in the history of with (Figure 1C,D) and without (Figure have enhanced the homing ability evolutionary biology. Charles Darwin 1A,B) crests of reversed feathers on of racing strains: domestics get lost was a pigeon aficionado and used their heads, we found that breeds less often and show a greater drive this dramatic example of diversity with crests shared the same coding to return home than their free-living within a species to convey his ideas mutation in the Ephrin receptor B2 counterparts, particularly over long about natural selection in The Origin (EphB2) gene. The genomic data distances. The hippocampus, an of Species. He recognized the also suggested that the head crest important part of the vertebrate brain fundamental similarities between mutation evolved just once and spread for spatial learning and memory, artificial and natural selection, and to a variety of breeds through either is larger in racing homers than took a special interest in the extreme hybridization, repeated selection on in wild rock pigeons, though the variation among pigeons that evolved a mutation that was already present respective contributions of fixed from a common ‘blue’-colored wild in a wild rock pigeon population, or genetic differences and phenotypic type. “Believing that it is always best perhaps both. plasticity to this phenomenon are not to study some special group, I have, Will the finding that the same, simple completely understood. after deliberation, taken up domestic genetic basis underlies similar derived Experiments suggest that pigeons,” he wrote in The Origin. He traits in different pigeon breeds hold pigeons rely on the position of the chose pigeons as an exemplar of true for additional traits? Classical sun, direction and intensity of the diversity under domestication in a later genetic experiments suggest this might geomagnetic field, and olfactory cues volume, The Variation of Animals and sometimes — but not always — be when far away from home, switching Plants Under Domestication, noting, “I the case, and genomic resources now to visual landmark navigation as they have selected this case, because…the permit rigorous testing of this question near the home loft. Magnetoreceptive materials are better than in any other; from a molecular perspective. The cells, long thought to reside in the and one case fully described will in fact tremendous amount of phenotypic beak, were recently demonstrated illustrate all others.” Darwin asserted diversity in this species, coupled with to reside in the inner ear lagena, and that based on external morphology tractability in genetics, genomics, and signal to neurons in the vestibular alone, some domestic pigeon breeds developmental biology, makes the brainstem. Interestingly, these neurons were as distinct as different genera of domestic pigeon a powerful model are capable of responding to the wild pigeons and doves. Yet he also for understanding trait evolution and direction, polarity, and intensity of observed that even highly divergent development in vertebrates. a magnetic field, and these factors domestic breeds could be crossed to vary predictably based on geographic produce viable offspring, and thus they Where can I find out more? location. While the relative importance belonged to the same species. Darwin, C.R. (1868). The Variation of Animals and Plants Under Domestication, Volume 1, of each homing cue to navigation is (London: John Murray). not entirely clear, pigeons probably What do we know about the genetic Hansell, J. (1998). The Pigeon in History. (Bath, U.K.: Millstream Books). use information opportunistically basis of variation among pigeons? Levi, W.M. (1986). The Pigeon, Second Revised depending on environmental Several key features make pigeons Edition, (Sumter, S.C.: Levi Publishing Co.). conditions. a promising model for avian and Secord, J.A. (1981). Nature’s fancy: Charles Darwin and the breeding of pigeons. ISIS 72, 163–186. vertebrate evolutionary genetics. First, Shapiro, M.D., Kronenberg, Z., Li, C., Domyan, E.T., What are feral pigeons? The current some traits that vary among pigeon Pan, H., Campbell, M., Tan, H., Huff, C.D., Hu, H., Vickrey, A.I., et al. (2013). Genomic diversity geographic range of the rock pigeon breeds also vary among numerous and evolution of the head crest in the rock extends to all continents except natural species of birds, providing pigeon. Science, Epub ahead of print, Jan 31. Antarctica. Outside the native range — a model for understanding genetic Stringham, S.A., Mulroy, E.A., Xing, J., Record, D., Guernsey, M.W., Aldenhoven, J.T., Osborne, and even many places within it — rock mechanisms that control variation in E.J., and Shapiro, M.D. (2012). Divergence, pigeons are feral. That is, they are the wild. Second, classical experiments convergence, and the ancestry of feral populations in the domestic rock pigeon. free-living descendants of escaped by academic geneticists and hobbyists Curr. Biol. 22, 302–308. domestics, and some Old World feral alike suggest the genetic architecture populations are probably thousands for many traits is relatively simple, of years old. Rock pigeons first thereby increasing the likelihood of Department of Biology, University of Utah, became feral in North America over identifying genes responsible for Salt Lake City, UT 84112, USA. 400 years ago, and ongoing natural differences among breeds. Finally, E-mail: [email protected]