Genetic Structure of Domestic Pigeon Breeds

2 Darwin C. On the Origin of Species by Means of Natural Selection. 2 Darwin C. On the Origin of Species by Means of Natural Selection. 3 Darwin C.R. Charles Darwin was a pigeon aficionado and relied heavily on the dramatic results of artificial selection in domestic pigeons to communicate his theory of natural selection in wild populations and species []. “Believing that it is always best to study some special group, I have, after deliberation, taken up domestic pigeons,” he wrote in The Origin of Species [] (p. 20). Darwin noted that unique pigeon breeds are so distinct that, based on morphology alone, a taxonomist might be tempted to classify them as completely different genera [], yet he also concluded that all breeds are simply variants within a single species, the rock pigeon Columba livia.

3 Darwin C.R. 6 Sossinka R. Domestication in birds. 7 Driscoll C.A.

Macdonald D.W.

O'Brien S.J. From wild animals to domestic pets, an evolutionary view of domestication. 1 Price T.D. Domesticated birds as a model for the genetics of speciation by sexual selection. 2 Darwin C. On the Origin of Species by Means of Natural Selection. 3 Darwin C.R. 4 Levi W.M. Encyclopedia of Pigeon Breeds. 5 Levi W.M. The Pigeon. Pigeons were probably domesticated in the Mediterranean region at least 3,000–5,000 years ago, and possibly even earlier as a food source []. Their remarkable diversity can be viewed as the outcome of a massive selection experiment. Breeds show dramatic variation in craniofacial structures, color and pattern of plumage pigmentation, feather placement and structure, number and size of axial and appendicular skeletal elements, vocalizations, flight behaviors, and many other traits []. Furthermore, many of these traits are present in multiple breeds. Today, a large and dedicated pigeon hobbyist community counts thousands of breeders among its ranks worldwide. These hobbyists are the caretakers of a valuable—but largely untapped—reservoir of biological diversity.

Here, as an initial step in developing the pigeon as a model for evolutionary genetics and developmental biology, we address two fundamental questions about the evolution of derived traits in this species. First, what are the genetic relationships among modern pigeon breeds? And second, does genetic evidence support the shared ancestry of breeds with similar traits, or did some traits evolve repeatedly in genetically unrelated breeds?

4 Levi W.M. Encyclopedia of Pigeon Breeds. 5 Levi W.M. The Pigeon. 8 National Pigeon Association

National Pigeon Association Book of Standards. 9 Pritchard J.K.

Stephens M.

Donnelly P. Inference of population structure using multilocus genotype data. Figure 1 Genetic Structure of the Rock Pigeon (Columba livia) Show full caption 5 Levi W.M. The Pigeon. Results from STRUCTURE analysis showing coefficients of genetic cluster membership of 361 individuals representing 70 domestic breeds and two free-living populations (European and North American, at the far left and far right of the plots, respectively) of rock pigeon. Each vertical line represents an individual bird, and proportion of membership in a genetic cluster is represented by different colors. Thin black lines separate breeds. At K = 2, the owls, wattles, and tumblers are the predominant members of one cluster (blue), while other breeds comprise another cluster (orange). At K = 3, the pouters and fantails (yellow) separate from the toys and other breeds, and at K = 5, the fantails separate from the pouters. Pouters and fantails also share genetic similarity with the recently derived king, a breed with a complex hybrid background that probably includes contributions from Indian breeds []. At K = 5, fantails are also united with the Modena, an ancient Italian breed, and a free-living European population. The latter two form a discrete cluster at K = 9. At K = 10 and greater ( Figure S1 ), some of the breed groups are assigned to different genetic clusters. This suggests that a number of assumed clusters beyond K = 9 reveals the structure of individual breeds, rather than lending additional insights about genetically similar breed groups. Top row of photos, left to right: Modena, English trumpeter, fantail, scandaroon, king, Cauchois. Bottom row: Jacobin, English pouter, Oriental frill, West of England tumbler, Zitterhals (Stargard shaker). Photos are courtesy of Thomas Hellmann and are not to scale. See Figure S1 for results from K = 2–25 and Tables S1 and S2 for breed and marker information, respectively. To address these questions, we studied the genetic structure and phylogenetic relationships among a large sample of domestic pigeon breeds. Our primary goal was to examine relationships among traditional breed groups, to which breeds are assigned based on phenotypic similarities and/or geographic regions of recent breed development ( Figure 1 ) []. First, we used 32 unlinked microsatellite markers to genotype 361 individual birds from 70 domestic breeds and two free-living populations. We next used the Bayesian clustering method in STRUCTURE software [] to detect genetically similar individuals within the sample ( Figure 1 ; see also Figure S1 available online). When two genetic clusters were assumed (K = 2, where K is the number of putative clusters of genetically similar individuals; Figure 1 ), the first cluster combined several breed groups with dramatically different morphologies. Principal members of this grouping included the pouters and croppers, which have a greatly enlarged, inflatable crop (an outpocketing of the esophagus); the fantails, which have supernumerary and elevated tail feathers; and mane pigeons, breeds with unusual feather manes or hoods about the head ( Figure 1 ).

4 Levi W.M. Encyclopedia of Pigeon Breeds. 8 National Pigeon Association

National Pigeon Association Book of Standards. 4 Levi W.M. Encyclopedia of Pigeon Breeds. 5 Levi W.M. The Pigeon. 5 Levi W.M. The Pigeon. The second ancestral cluster consisted mainly of the tumblers (including rollers and highflyers), the most breed-rich of the major groups (at least 80 breeds recognized in the USA) []. Tumblers are generally small bodied and were originally bred as performance flyers, with many breeds still capable of performing backward somersaults in flight. In most modern tumbler breeds, however, selection is most intense on morphological traits such as beak size and plumage. Also included in this cluster are the owl and the wattle breeds (wattles are skin thickenings emanating from the beak). These two breed groups contrast dramatically in several key traits: owls are typically diminutive in body size, have a pronounced breast or neck frill, and have among the smallest beaks of all breeds, whereas the wattle breeds (English carrier, scandaroon, and dragoon in our analysis) are larger bodied, lack a frill, and have among the most elaborated beak skeletons of all domestic pigeons []. The homers (homing pigeons and their relatives) are included in the second cluster as well. The carrier, cumulet, and owl breeds—all members of this cluster—contributed to the modern homing pigeon during its development in England and Belgium approximately 200 years ago []. Consistent with this recent admixture, the owls and several homer breeds continue to share partial membership in the same cluster at K = 4 and beyond, and the cumulet shares similarity with the homers and wattles at K = 7. Numbers of clusters beyond K = 9 reveal the structure of individual breeds, rather than lending additional insights about breed groups ( Figure S1 ). Notably, although allelic similarity is potentially indicative of shared ancestry, this analysis does not explicitly generate a phylogenetic hypothesis. Moreover, an alternative explanation for clustering is that large effective population sizes might result in an abundance of shared alleles.

ST = 0.204 for all breeds, maximum F ST = 0.446; potentially more reliable differentiation estimates considering the modest sample sizes for some breeds [ 10 Jost L. G ST and its relatives do not measure differentiation. est = 0.156, maximum D est = 0.421; ST = 0.106, maximum F ST = 0.240 for the comparison between Pygmy and Chinese populations using a dense genome-wide SNP set [ 11 Xing J.

Watkins W.S.

Witherspoon D.J.

Zhang Y.

Guthery S.L.

Thara R.

Mowry B.J.

Bulayeva K.

Weiss R.B.

Jorde L.B. Fine-scaled human genetic structure revealed by SNP microarrays. Figure 2 Consensus Neighbor-Joining Tree of Forty Domestic Breeds and One Free-Living Population of Rock Pigeon Show full caption The tree here was constructed using pairwise Cavalli-Sforza chord genetic distances and includes the subset of breeds with >50% membership in one genetic cluster at K = 9. Branch colors match cluster colors in Figure 1 , except all tumbler breeds are represented with light blue for clarity. A notable incongruence between the STRUCTURE analysis and the tree is the grouping of the English pouter with a tumbler rather than with the other pouters; however, this grouping is not well supported. Percent bootstrap support on branches (≥50%) is based on 1,000 iterations, and branch lengths are proportional to bootstrap values. We next used multilocus genotype data from a subset of breeds (those with >50% membership in a cluster at K = 9) to calculate genetic distances among breeds and to generate a neighbor-joining tree ( Figure 2 ). Among the major groups, only subsets of the pouter, fantail, mane, tumbler, Modena and free-living European, and owl branches of the tree have strong statistical support ( Figure 2 ). Nevertheless, at the breed level we observed substantial genetic differentiation, suggesting that in many cases, hybridization among breeds has been limited (mean pairwise F= 0.204 for all breeds, maximum F= 0.446; potentially more reliable differentiation estimates considering the modest sample sizes for some breeds []: mean D= 0.156, maximum D= 0.421; Tables S4 and S5 ). As a comparison, mean pairwise differentiation among African and Eurasian human populations with historically limited gene flow is lower (mean F= 0.106, maximum F= 0.240 for the comparison between Pygmy and Chinese populations using a dense genome-wide SNP set []).