All crows are black, aren’t they?

Pig begets pig and fly begets fly. In a continuous stream of ‘like begets like’, how do new species come into existence?

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Mar 25, 2019
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While camping on the volcanic shores of an isolated island in the Galapagos archipelago, this question seemed omnipresent. In this harsh, depauperate environment, variation and selection are palpable: marine iguanas glitter in different hues from island to island, tortoises display variation in their armour, and variation in the beak of Darwin's finches seems endless. Quite simply, I became infected with the question of adaptation and speciation. But how do you study this process? I needed an evolutionary experiment in an amenable system, ideally closer to home! I flipped through the pages of my favourite bird book and got stuck on the page displaying carrion and hooded crows.  

As already described in great detail by Wilhelm Meise in 1928, all-black carrion crows and grey-coated hooded crows are distributed in a leap frog pattern across Eurasia. Black / grey / black - with replicated hybrid zones in between running through Germany in the west and Siberia in the east. An evolutionary experiment had naturally unfolded: the morphologically distinct lineages hybridize, but still maintain a narrow hybrid zone. Their genomes are compatible in principle, but apparently contain factors acting as barriers that impede free mixing. But what keeps them apart? My early hunch was mate choice based on their different plumages, and thus focussing on plumage genes seemed obvious.   

Siblings from a mixed parent nest. Photo credit: Christen Bossu


I soon embarked upon the quest for the genes driving a wedge between these populations –  scrambling up funds to get going. The first grant application revolved around candidate genes and markers designed on chicken and zebra finch which were the only bird genomes available at the time. Luckily, technology soon overran these ambitions and we assembled various genome drafts (1, 2), sequenced over a hundred full genomes of specimens across the distributional range (3) and characterized gene expression profiles in feather follicles (4), now even at single cell resolution (5). This work highlighted a handful of candidate genomic regions that may indeed point towards melanogenesis – the metabolic pathway painting the feathers.  Yet, while the data supported the initial hypothesis, we weren't convinced yet. More direct evidence was needed.    

The answer turned out to be written in the admixed genomes of the hybrids. For an evolutionary geneticist, backcrossed hybrid genomes are like a microscope for the cell biologist. The mixture of carrion and hooded crow components allows dissecting the genomic regions that result in black, grey or mottled plumage. To get to the genes, we formed an international team of researchers and local ornithologists and ran transects across the German and Italian part of the European hybrid zone. Yet, sampling crows in anything but easy. Nests have to be scouted and daring climbs to the thin twigs of the canopy need to be undertaken to sample the precious DNA - often to find out that other predators have been there first. Discussing the matter with my then nine years old son soon provided the obvious solution: a drone. This electronic bird sped up field work significantly and saved hours of climbing in vain (6).  

Field work. Photo credit: Christen Bossu

That way we obtained several hundred samples which helped us unravel the crows’ secret: as few as two genes intertwined in epistatic interactions code for most of the striking contrast in plumage pigmentation and act as the source of selection against migration across the hybrid zone. A mate choice barrier in its purest form. To learn more about how crow genomes flow across Europe consult the manuscript here:

https://www.nature.com/articles/s41559-019-0847-9

Bibliography 
1.          J. W. Poelstra et al., Science. 344, 1410–1414 (2014).
2.          M. H. Weissensteiner et al., Genome Res. 27, 697–708 (2017). 
3.          N. Vijay et al., Nat. Commun. 7, 13195 (2016).
4.          J. W. Poelstra, N. Vijay, M. P. Hoeppner, J. B. W. Wolf, Mol. Ecol. 24, 4617–4628 (2015).
5.          C.-C. Wu et al., J. Exp. Biol. 222, jeb194431 (2019).
6.          M. H. Weissensteiner, J. W. Poelstra, J. B. W. Wolf, J. Avian Biol. 46, 425–430 (2015).

 

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Jochen Wolf

Professor, University of Munich

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