02/12/2013 04:33 pm ET Updated Apr 14, 2013

Pigeon Study Contradicts Darwinian Natural Selection

Charles Darwin made the example of extreme variation in the appearance of pigeons a centerpiece of his theory of evolution by natural selection. Pigeons are among the most phenotypically variable of all birds, a description that also pertains to the family's most prominent species, the rock pigeon. Members of this species are distributed across the world in wild and urban settings, and include the domesticated varieties cultivated by pigeon breeders, in whose work Darwin took an intensive interest. Wild rock pigeon subspecies and their domesticated counterparts can differ from one another in size, beak shape, color and pigment patterning, posture, vocalization, feathering and flight capability.

Darwin recognized that that sudden, large-scale, changes in form ("sports") could occur in pigeons and other animals, as well as in plants, within a single generation. However he strongly rejected this mode of change as an evolutionary mechanism, proposing instead his key hypothesis (called "Darwin's dangerous idea" by the philosopher Daniel Dennett) that evolution occurs by natural selection, which "can act only by the preservation and accumulation of infinitesimally small inherited modifications, each profitable to the preserved being."1

In discussing Darwin's use of pigeons in making his case for a correspondence between artificial and natural selection, his biographers Desmond and Moore state:

Darwin wanted to show nature composed of myriad tiny variations invisible to all but experienced fanciers. These enthusiasts could judge to one-sixteenth of an inch. And the differences that only they could spot formed the raw material to be accentuated through generations of selective breeding. From such minute aberrations, enormous sculpted changes had been wrought by fanciers leading to today's pouters, fantails, runts and tumblers ... Darwin believed that similar imperceptible variations held the key to Nature's own Malthusian selection.2

It is clear, then, that Darwin did not simply affirm that organisms evolve by contributing arbitrary heritable differences to future generations (a common misunderstanding of his theory). Instead, he proposed a very specific model for how large differences between organisms, including species and ultimately phylum distinctions, eventually come into being.

In a paper that recently appeared online in the journal Science,3 Michael Shapiro and his coworkers at the University of Utah analyzed the genetics of the pigeon head crest, an array of feathers originating on the head and neck that have reversed polarity, causing them to grow toward the top of the head instead of down the neck. This was one of the traits proposed by Darwin to have arisen in domesticated populations by many cycles of breeding, and therefore in wild populations (by his hypothesis), by many cycles of natural selection. In their close analysis of the newly sequenced pigeon genome and a survey of many wild and domesticated birds the investigators found that pigeons with a head crest all carried the same gene mutation, cr. The chromosomal region in which the cr marker is found suggests that the affected gene is Ephrin receptor B2 (EphB2), a cell surface molecule employed at many different sites during embryonic development.

Apart from their appeal to pigeon fanciers, head crests are important display items in mate selection, and are thus classic "adaptations," functionally relevant structures that are taken as evidence, in the Darwinian paradigm, for natural selection having occurred. Conversely, if a structure has evolved by a more abruptly acting process than natural selection (as indeed was found for the crest by Shapiro et al.), the fact that it is adaptive is simply evidence that the organisms in which it turned up found a way of using it.

While EphB2 is the best candidate for the gene associated with the cr marker, the mechanism by which the receptor it specifies affects feather orientation during embryogenesis so as to produce the morphological "novelty" of the crest is not clear. EphB2 is expressed neither exclusively nor asymmetrically in head and neck feather buds. If it is in fact the determinant of the crest, it must act very early in development, and differently in head and neck feathers than in other ones.

Despite the unknowns in the identity and action of the cr-associated gene in generating the crest, one thing is certain about it: it is a "gene of large effect." Such genes were written out of the mid-20th-century Darwinian synthesis based on statistical arguments of R.A. Fisher,4 which were contrived to make natural selection compatible with a gradualist version of Mendel's genetics. Alternative theories that invoked such "macromutations" and associated phenotypic jumps or "saltations"5 suffered ridicule and neglect.

Not only does the cr mutation induce effects that are "entirely one way or entirely the other" at the phenotypic level, however; the manner in which its presence determines the crest in rock pigeon varieties undermines another tenet of the theory of natural selection: "descent with modification." The cr mutation is present in every pigeon analyzed with a crest, even if they are otherwise distantly related to each other within the rock pigeons. If individual genes can affect shared developmental systems in this precipitous fashion, the role of incremental adaptive selection (i.e., Darwinism) in rationalizing morphological evolution becomes highly questionable.

Significantly, the major features of animal bodies (the "body plans"), are themselves generated by a set of genes of large effect, the so-called "developmental genetic toolkit." Since not every one of the 30-40 different phyla (e.g., chordates, arthropods, mollusks, nematodes) contains each of the genes of this toolkit, the morphological differences among the animal phyla, which emerged more than half a billion years ago, may have been comparably abrupt, and as independent of gradual, adaptive selection as the generation of the novelty of the head crest in pigeons.6

1. Darwin, C., 1859. On the origin of species by means of natural selection, or, the preservation of favoured races in the struggle for life. J. Murray, London.
2. Desmond, A., Moore, J. 1992. Darwin. New York: Warner Books.
3. Shapiro, M. D., Kronenberg, Z., Li, C., Domyan, E. T., Pan, H. et al., 2013. "Genomic diversity and evolution of the head crest in the rock pigeon." Science, in press.
4. Fisher, R. A., 1930. The genetical theory of natural selection. Clarendon Press, Oxford.
5. Goldschmidt, R. B., 1940. The material basis of evolution. Yale University Press, New Haven.
6. Newman, S. A., 2012. Physico-genetic determinants in the evolution of development. Science. 338, 217-9.

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