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Was Darwin wrong? The sole descent of the domestic pigeon from the rock pigeon

Molecular genetic studies also put many beliefs in pigeon breeding to the test. An important finding of recent studies on the check pattern in domestic pigeons and on the Stipper gene and its alleles was that colorations were associated with a structural change in the genetic make-up by changing the number of copies of segments of DNA (Copy Number Variation CNV) in a genome (Vickrey et al. 2018, Bruders et al. 2020). Not every deviation from the wild type is due to mutative changes in the base sequences in a DNA segment. Based on research in human genetics after 2000, this has already been investigated for other animal species. The findings also show much in pigeon breeding that was previously believed in a new light. Another thesis derived in connection with the study of the pattern is more provocative. Namely, that the genes for the check pattern were very likely transferred from the Guinea pigeon to the domestic pigeon. In a period of time only centuries ago, and far after the species separated millions of years ago.

Darwin and the pigeons

For Darwin, the various breeds of domestic pigeons all come from the rock pigeon (C. livia), of which he had a drawing of a shot individual in his work 'The variation of animals and plant under domestication' (1868, 2nd ed. 1875). The wild and semi-wild pigeons in the English 'Dovecots' were a typical link in domestication. The occasional and non-unique appearance of checks in otherwise blue-bar wild and semi-wild populations was a domestication phenomenon for him (1868, 1875). The deviation of the pattern was no justification to consider checks as a subspecies in the rank of the somewhat darker rock pigeon variant in the Indian region or the somewhat lighter variant in the Nile region. In some regions of England, half-wild check pattern pigeons were so common that Dixon described them as a typical 'Dovecote-Pigeon' in his book in 1851 and depicted an individual. For a discussion of the check variant, which has meanwhile been named by Blyth C. affinis, see Darwin 1875 Vol. 1 Chapter VI.

    

Fig. 1: The Rock Pigeon at Darwin 1868/1875 and the blue check ‚Dovecot-Pigeon‘ (Columba affinis at Blyth). Source: Dixon 1851

Checkered pigeons before Darwin

Going back further in time, Albin has a drawing of a check 'Dovecot pigeon', dated 1735, with reference to the wide range of variation of these half-wild pigeons at the time. This can already be seen in the coloration of the individual shown and in the text, when referring to the check, 'black with ash-gray admixture' (mixture with cinereous) is written. From today's point of view artistic freedom or even a diluted check and an early hint on a gene later named dilution.

Fig. 2: The Common Dove House, or Wild Pigeon, dated 1735. Source: Albin, Natural History of Birds 1738 Vol III (sheet 39)

In Thuringia, Bechstein, who was not only a scientist but also a pigeon keeper, described on domestic semi-wild stocks how new colors were created in the process of domestication (1795, 1807). Among other colors, the 'gedüpfelte' = checkered field pigeon.

Since I am a great friend of these birds, not only as a naturalist, but also as a fancier, I have taken great care to observe how the various tame varieties of this wild breed gradually form the various tame varieties of this wild race (because they still belong among them).

From this common wild pigeon, the checkered field pigeon described below first emerges, even if it is not fed in the house. This gradually becomes reddish-gray and pearl-gray with red-brown strings, fox-red and very dark blue; then the wings and tails vary, initially becoming light gray ...

 

Fig. 3: Domestication and the variation in coloration, Bechstein (1795), p. 18.

About 200 years earlier, Marcus zum Lamm had field pigeons (ferrals or in an old German terminology 'Feldratzen') painted around 1600, one of the pigeons undoubtedly in the check pattern. In his notes he writes about checkered pigeons (a Visch Schüppichte or hammerschlegichte Daub), quoted in Kintzenbach / Hölzinger 2000, p. 189.

Fig. 4: Field pigeons or Feldt Ratzen at Marcus zum Lamm around 1600 (Kintzenbach/Hölzinger 2000)

In the falcon book 'De arte venandi cum avibus', written by Friedrich II between 1259 and 1266 and illustrated also with drawings of pigeons. Not only falcons are discussed but the work is considered an early ornithology using earlier sources besides own observations. If the pigeon depicted individually is supposed to represent the bluebar archetype (fol. 18), then the domestic pigeons shown together with wild pigeons (fol. 11) should also be checkered deviations from the bar pattern. Interesting is an even earlier illustration from the time before Christie's birth, printed in the book by Daniel Haag-Wackernagel, which is interpreted as check.

    

Fig. 5: A blue house pigeon and house pigeons together with wild pigeons in the falcon book Friedrich II 1241-1248, fol. 18 and fol. 11, wall painting from the green room of the north palace of Tell el Armana, Egypt 1350 BC Chr. (Printed in Haag-Wackernagel 1989, Sell 2009)

Evolution of the pigeon species

For some groups of pigeon species, Goodwin has tried to trace when individual groups and species, starting from a common origin, split up and split off.

Fig. 6.: Assumed relationships in the Columba genus in Goodwin, Pigeons and Doves of the World, second ed. London 1970, p. 53.

The rock pigeon, and the domestic pigeon derived from it, is regarded as C. livia as being closely related to the amphara pigeon, the snow pigeon, the guinea pigeon and the cliff pigeon or Eastern rock pigeon. This branch is shown separately here.

 

Fig. 7: Excerpt from the diagram on the relationships in the Columba genus in Goodwin, Pigeons and Doves of the World, second ed. London 1970, p. 53 with text addition

The wild forms of pigeon species whose paths separated earlier in their developmental path are more different in appearance and behavior from one another than species in which this happened later. According to the diagram, the white-collared (amphara) pigeon, guinea pigeon, snow pigeon and cliff pigeon have followed a common development path longer than with the stock pigeon and the wood pigeon that had split off before. The longer in the past the split, the greater the likelihood that behavior and appearance of the wild form will also develop differently due to different mutations in the separate groups and due to the loss of previously common genes in a population. The genetic similarity of species and the assumed periods of time are shown in a molecular genetic study with the attempt to classify closely related species by Soares et al. 2016.

Fig. 8: Clustering of wild pigeons according to genetic similarity by Soares et al. 2016 (excerpt)

Species that are already extinct are also included in the study. The guinea pigeon was not there, nor the stock dove and the wood pigeon. The two examples of the Columba livia are, according to the sources, to presume Gimpel pigeons as a domestic pigeon breed and rock pigeons with little genetic distance to it. The closest related species is the cliff pigeon C. rupestria, which outwardly hardly differs from the C. livia except for the typical white lightening in front of the tail band. In amateur breeding, the trait is anchored in Bern mirror tails. The bleaching of the tail feathers in both cases differs from the darker-framed mirrors of oriental owls. Similar bleaching occurs in combination with other hereditary factors in a weakened form in other domestic pigeon breeds (see also pictures in Pigeon Genetics 2012 and Genetics of Pigeon Colorings 2015), possibly a shared inheritance of a common preform or an early introgression.

Introgression and 'retrogression' from a historical perspective

Introgression, in the title of the 2018 study cited, means the transfer of genes from one species to another after the formation and consolidation of different species. According to the model calculations, the period of the transfer of the check pattern from C. guinea to C. livia is estimated to be 429 to 857 years ago with a generation succession of one to two generations per year (Vickrey et al. 2018, p. 12). In retrospect, that would be around AD 1200 - 1600. It is the time when Friedrich II, Emperor of the Roman-German Empire, wrote the falcon book 'De arte venandi cum avibus' (1258-1266) and when Marcus zum Lamm wrote his notes on the 'Picturarum' and had pictures of domestic pigeons and field pigeons painted (around 1600). The centuries in between were marked in Europe by the plague in the 14th century and by armed conflicts. At the end of the 15th century, America was discovered by Europeans and after 1600 the Thirty Years War devastated many parts of Europe. The distribution of the guinea pigeon should not have deviated from the distribution given by Goodwin at the time. There has been an overlap in the distribution of the rock pigeon and the guinea pigeon in some parts of Africa. It is unlikely that crossbreeds with domestic pigeons would have taken place in Europe at that time.

    

Fig. 9: Distribution maps for the rock pigeon and the guinea pigeon at Goodwin (1970)

From historical circumstances, it was assumed that the sporadic appearance of check variants in widely separated parts of Central Europe was due to repetitive mutations and not to deliberate or accidental crosses with the guinea pigeon. The check pattern is dominant and, unlike a re­cessive gene, cannot be obscured in a population for long until it appears sporadically. Bechstein's observation (1795) of the emergence in wild-colored field pigeon populations in Thuringia and the occurrence in populations on the coasts of England and on the Faroe and Orkney Islands, in the far north of the distribution area of ​​the rock pigeon (Darwin), can hardly be explained with crossbreeds between the arts.

A summary of the results of crossings of wild pigeon subspecies with one another can be found in Gray 1958. The list, here an excerpt, shows the problems of maintaining a first generation even under controlled conditions.

Fig. 10: Bird Hybrids, excerpt from Annie P. Gray 1958, p. 128.

Successful rearing of hybrids in crossings with guinea pigeons has nevertheless been reported several times. Dietmar Fennelt, who brought cliff pigeons to Germany, reported on quadruple crossings with proportions of stock pigeons, rock pigeons, guinea pigeons and cliff pigeons, which would have resulted in a consistently fertile line (messages in an internet blog and personal). That it was possible to obtain offspring from the male hybrids even in infertile female hybrids from rock pigeon x guinea pigeon and, after two mating back of cocks to blue-bar C. livia, also fertile offspring (Vickrey et al. 2020, p. 10 with reference to Taibel, 1949) does not have to mean that it also takes place in the wild and that the genetic material has been permanently incorporated into the population. In 2004 Stauber reported about an introgression from crossing Bern mirror tails, a Swiss color pigeon, with cliff pigeons.

Fig. 11: Bern mirror tail and cliff pigeon (Source: Sell, Genetik der Taubenfärbungen 2015 (Genetics of pigeon colors))

Fig. 12: F1 from ‚Bern mirror tail‘ and cliff pigeon (Photo Karl Stauber, reprinted in Sell, Taubenzucht, Achim 2019)

Unexpectedly, because of the great similarity, it was initially not possible to raise young in the first cross. The chicks seemed to need a longer supply of pigeon ‘milk’. However, by mating the few hybrids finally raised back to Bern mirror tails, fertile offspring were obtained, which inherited the mirror tails of the parent animals on both sides. To speak of introgression into the domestic pigeon population is nevertheless an exaggeration. For one thing, the mirror tail was already there before the intersections. The intermediate first generation in crossbreeds rather indicates parallel developments in this trait. Second, the Bern mirror tails are a rare breed themselves, and breeds and lines are disappearing with breeders. Genes that have potentially flowed in through crossbreeding can also be lost again, resulting in 'retrogression'.

Molecular genetic evidence

For investigations into the extent and when an introgression between two species took place, the D-statistics are used in more recent studies. Methodologically, the procedure is similar to a cleverly designed chi-square test. Check and bar C. livia are compared with Guinea pigeons and, as a reference (in the terminology of the methodology, the 'outgroup population'), the wood pigeon. Their genome serves as a representative of the genome of the original art before the split. All of the individual species that have emerged from the original specie have parts of their origins in their genome. In the further evolution, different new mutations in the genome have prevailed in the new species split off from it over the course of millennia and sometimes for longer periods of time. Other, originally existing hereditary factors have been replaced. The genetic makeup has changed. If check and bar C. livia do not represent different arts or one of them contain external parts by former introgression, then it is to be expected that they have the same proportion of the genetic make-up of the 'outgroup population' with regard to the genetic makeup.

There are sequences of chromosomes of the bar C. livia (designated as P1), the check C. livia (P2), the C. guinea, which also has the check pattern (P3) and, as 'outgroup population', sequences of the wood pigeon.The null hypothesis is that P1 and P2 are descended from a common parent species and after the separation did not receive any gene inflow from one of the also split off P3s. The alternative hypothesis is that of introgression following the separation of the species, whereby the check trait could have been transmitted. Methodologically, we speak of the ABBA and BABA configuration. Areas of the genome in which there is overlap in the four populations are considered. The ABBA configuration refers to areas in which P1 has the outgroup allele and P2 and P2 the acquired allele (derived copy). The configuration BABA corresponds to areas in which P1 and P3 have the acquired alleles and P2 the outgroup allele (Durand et al. P. 2240, and related thereto, Vickrey et al., 2018, p. 10). In the formulation by Durand et al .: “For the ordered set {P1, P2, P3, O}. we call the two allelic configurations of interest "ABBA" or "BABA." The pattern ABBA refers to biallelic sites where P1 has the outgroup allele and P2 and P3 share the derived copy. The pattern BABA corresponds to sites where P1 and P3 share the derived allele and P2 has the outgroup allele ”.

The D statistic measures empirically which configuration is more plausible by determining the difference in the measured genetic similarity in the ABBA and BABA configuration. This is normalized by the sum of the two values ​​(cf. Durand et al. P. 2240).

Maybe another kind of departure is more obvious. The similarities are measured

P1 O + P2 P3 for a potential ABBA figuration, and P1 P3 + P2 O for an alternative BABA figuration. For the D statistic follows

If P1 and P2 have not experienced introgression, then the measured similarities with the other populations will be within the scope of statistically insignificant deviations. The similarity P1 O will correspond to the similarity P2 O (P1 O ≈ P2 O). P2 P3 and P1 P3 will also correspond (P2 P3 ≈ P1 P3). Readable on the numerator, the summands in the numerator will largely neutralize each other and the D statistics will approach zero. Larger deviations from this can be interpreted as an indicator of introgression.

The hypothesis was also confirmed in the samples with D Statistics ​​close to zero for a consideration of the entire genome (Vickrey et al., Pp. 12, 17). Tests for the candidate region, in which the traits for the pattern and also the genes for checks are located, however, showed a different picture (p. 12). The expectation was that bar and check C. livia are more similar here than C. guinea. It was found in the 'candidate region' for the pattern that the check C. livia there were more similar to the C. guinea pigeon than the bar C. livia. According to the high D Statistic values, the candidate region appears to essentially comprise the genome regions responsible for the checks. The areas also do not seem large enough to be mixed up to a greater extent by linkage breaks and the exchange of factors not directly responsible for the checks. In contrast to the domestic pigeon, the area relevant for checks in the guinea pigeon showed no multiple copy variation (MCV) (p. 12). This could also indicate the need for other explanations which are indicated below.

Consideration beyond the test

Identical features as in C. livia can also be found in subspecies of the turtle dove (genus Streptopelia) such as the domesticated Ring-Neck Dove or Barbary dove (Streptopelia, risoria). There are whites with dark eyes, albinos with pink eyes, silky feathered ones and those with feather structures that differ from normal (Goodwin 1970, p. 129). Gray also reported on offspring from matings with C. livia in 1958. James Demro raised a peak-crested young from a peak-crested satinette pigeon with a peak crested dove (Miller/Demro 2011). Since the peak-crest is a recessive feature in the domestic pigeon and the doves as well, first of alleles were initially spoken of.

Fig. 13: Cross of Satinette (domestic pigeon) x Ring-Neck Dove with a peak crested young. Source: Miller/Demro 2011.

Subsequent molecular genetic analysis by a research group at the University of Utah (Vickrey et al. 2015) showed, also based on this animal, that the mutation in the wild pigeon indeed was a recessive also in that species, but was not located directly in the genome at which it was suspected based on the location at the rock pigeon. Both mutations nevertheless trigger similar biochemical processes in the respective species and thus fulfil similar functions (Vickrey et al., 2015, p. 2659ff.). Both traits are recessive in their respective environment, but interact like alleles at the illustrated intersection, so that the trait shows up in the hybrid. For the different kinds of feather crests in different domestic pigeon breeds, the research group had come to the conclusion in previous studies that a mutation probably occurred a very long time ago. This would have spread through crossbreeding to the different breeds (Shapiro et al. 2013), for which there have been many references in the domestic pigeon literature, at least for the last millennium. The question remains, however, whether there is a bias for mutations in the relevant genome area among the pigeon-like due to their common origin and whether something like a common development program exists for them, here for the hood. This is the subject of a side note of the 2015 study (p. 2661f.) and could also apply analogously to other phenomena, such as checks. That would call into question the criterion of the D-statistic for the determination of introgressions, applied to very narrow genome areas. This could also explain the strikingly high values of the D-statistics here. The mentioned possibility does not seem unique in the animal world.as was shown by extensive studies on cichlids. The genetic environment of diverging species could remain similar in certain areas without showing a certain characteristic. However, it could be activated in successor species in parallel by selective triggering mutations and express a characteristic without introgression. For example, for cichlids it is assumed that parallel evolutions take place quickly and that certain features are fixed independently of one another in different populations (Urban et al. 2020, p. 466).

Interesting from the point of view of gaining more experience about similar phenomena and possible similar chains of effects, also the relationship of C. livia to the cliff pigeon mentioned above. The characteristic of the mirror tail, an analogy to checks, is found in both domestic and wild pigeons. The lightening is not only evident in Bern mirror tails, but also in other domestic pigeon breeds. Thus, in the picture with a Frosty variant and a Turkish Takla Tumbler. Molecular genetic studies specifically on the mirror tail and possible parallels between domestic pigeons and rock pigeons do not seem to be available. Also, whether it is genetically identical in appearance in Bern mirror tails and other breeds has not yet been investigated.

 

Fig. 14: Lightening in front of the tail band of domestic pigeons and the cliff pigeon (Genetik der Taubenfärbungen 2015, Pigeon Genetics  2012, p. 158

Further investigations into phenomena that occur in very similar ways in the domesticated rock pigeon and Barbary pigeon could also expand our knowledge of the underlying mechanism

Summary

One of the certainties that one believes to have taken away from reading Darwin's book is that the domestic pigeon descends solely from the rock pigeon. Molecular genetic studies that come to the conclusion that the pigeons in the check patter that is widespread today are supposed to carry the genetic makeup of another species, the checkered C. guina, are surprising. Some indications are given here that make this seem unlikely. It is the different distribution areas of the two species and the problems of getting fertile hybrids from crossing the species. In addition, there is the estimated time in which an introgression should have taken place after the calculations, and reports of observations that suggest a mutative appearance of the check pattern, among other changes, in domesticated or semi-wild pigeons instead of an introduction by hybridization. The D statistical values of the molecular genetic analysis, which indicate introgression, are not shown genome wide but selectively in the 'candidate region' of the genome in which the pattern traits are located. There may be other explanations for this, such as mutations that repeat independently of each other. These could be favored by a similar genetic environment inherited from a common ancestor as still was supposed in other species. Thus, it could be instructive to study with the same methodology, and also a similar narrow sequence, relations between the domesticated Barbary pigeon (Streptopelia 'risoria') in their recessive white, albino and silky varieties and C. livia.

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A.S.