By crossing individuals with different characteristics, he could generate different offspring.
Some had brown feathers, others white. Some had long legs - others very short beaks. It provided valuable evidence for his theory of evolution.
Now, scientists have finally identified the gene behind beak length in pigeons - 162 years later.
Mutations, or phenotypes, in ROR2 also underlie a rare human disorder called Robinow syndrome that causes short bones and dwarfism.
It offers the hope of developing a gene therapy instead of bracing, surgery, or injections of growth hormones.
Lead author Dr. Elena Boer said: "Some of the most striking characteristics are the facial features which include a broad, prominent forehead and a short, wide nose and mouth, and are reminiscent of the short-beak phenotype in pigeons.
"It makes sense from a developmental standpoint because we know the ROR2 signaling pathway plays an important role in vertebrate craniofacial development."
Darwin was obsessed with domestic pigeons - insisting they held the secrets of natural selection in their beaks.
They come in all shapes and sizes in the 350-plus breeds within a single species - Columba livia.
The most striking are so short they prevent parents from feeding their young.
Centuries of interbreeding taught early pigeon fanciers length was likely regulated by just a few heritable factors.
Now for the first time geneticists have pinpointed the variant controlling short beaks.
The latter was a male Racing Homer - bred for speed with a beak length similar to the ancestral rock pigeon.
The former was a small-beaked female Old German Owl, a fancy pigeon breed that has a little, squat beak.
Senior author and professor Michael Shapiro said: "Breeders selected this beak purely for aesthetics to the point that it’s detrimental - it would never appear in nature.
"So, domestic pigeons are a huge advantage for finding genes responsible for size differences.
"One of Darwin's big arguments was that natural selection and artificial selection are variations of the same process. Pigeon beak sizes were instrumental in figuring out how that works."
The short and medium-beaked parents produced an initial brood of children, dubbed F1, with intermediate-length beaks.
When the F1 birds mated resulting grandchildren, dubbed F2, had beaks ranging from big to little - and all sizes in between.
Beak size and shape in the 145 F2 individuals was measured using micro-CT (computed tomography) scans.
Boer said: "The cool thing about this method is it allows us to look at size and shape of the entire skull.
"It turns out it is not just beak length that differs - the braincase changes shape at the same time.
"These analyses demonstrated beak variation within the F2 population was due to actual differences in beak length and not variation in overall skull or body size."
Mapping the pigeons' genomes also showed mutations were handed down the generations.
Shapiro said: "The grandkids with small beaks had the same piece of chromosome as their grandparent with the small beak, which told us that piece of chromosome has something to do with small beaks.
"And it was on the sex chromosome, which classical genetic experiments had suggested, so we got excited."
Comparing 56 pigeons from 31 short-beaked breeds and 121 from 58 medium or long-beaked peers found the former group[ had the same DNA sequence in an area of DNA containing the ROR2 gene.
Boer said: "The fact we got the same strong signal from two independent approaches was really exciting and provided an additional level of evidence the ROR2 locus is involved."
The short-beak mutation described in Current Biology is believed to cause the ROR2 protein to fold in a new way.
Functional experiments are now being planned to figure out how the mutation impacts craniofacial development.
The lure of the domestic pigeon that mesmerized Darwin is still captivating the curious to this day.
Enthusiasts continue to breed pigeons and participate in competitions to show off the striking variation among breeds.
Shapiro added: "Every paper our lab has published in the last ten years has relied on their samples in some way.
"We could not have done this without the pigeon-breeding community."
Darwin wondered about changes in bird beaks on the Galapagos Islands during his famous voyage around the world in 1831-1836.
It formed the basis of his 1859 book 'On the Origin of Species' - which would become one of the most important ever written.
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