Did sexual selection drive the evolution of Gallopheasants?

The variety of extravagant plumage patterns certainly suggests a pivotal role for sexual selection.

“The sight of a feather in a peacock’s tail, whenever I gaze at it, makes me sick,” Charles Darwin wrote. He was trying to figure out why natural selection would produce such an elaborate and seemingly useless extravagance. Surely, the colorful tail of a peacock would lower its chances of survival. Pondering this conundrum led Darwin to develop his theory of sexual selection, in which males compete for access to females. Male peacocks use their beautiful plumage patterns to attract potential mates and show off their “good genes”. A bird that can produce such extravagant feathers while fending off parasites and predators should definitely become the father of your offspring.

Peacock is actually a common name that refers to several species in the genera Pavo and Afropavo, which have been classified in the family Phasianidae (the gallopheasants). A quick glance at other members of this bird family reveals an additional wealth of colorful feathers in species such as Bulwer’s Pheasant (Lophura bulweri) or Golden Pheasant (Chrysolophus pictus). It is not surprising that several ornithologists have argued that sexual selection has been the driving force behind the diversification of this bird group. A recent study in the journal Zoologica Scripta put this idea to the test.

Problematic Phylogeny

Before we can infer the evolutionary importance of sexual selection, we need a proper phylogeny. However, previous molecular studies of the gallopheasants could not confidently resolve the evolutionary relationships between and within genera. This rampant phylogenetic conflict was attributed to the rapid succession of several speciation events. In this study, Peter Hosner and his colleagues used ultraconserved elements, nuclear introns and mitochondrial DNA sequences to unravel this phylogenetic knot. Their analyses resulted in a well-resolved evolutionary tree with few conflicting branches (see figure below). The issues in previous analyses were probably due to a limited number of genetic loci. Sometimes just adding more data can work.

Next, the researchers determined the strength of sexual selection by quantifying the degree of sexual dimorphism in different species. Sexual dimorphism refers the differences in appearance between males and females of the same species. Larger differences, such as more colorful males, suggest stronger sexual selection. If the evolution of gallopheasants was driven by sexual selection, then the gain of sexual dimorphism on certain branches should have resulted in accelerated diversification.

Evolutionary tree of gallopheasants based on ultraconserved elements, nuclear introns and mitochondrial DNA sequences. From Hosner et al. (2020) Zoologica Scripta.

Other Factors

In contrast to the expectations, there was no clear phylogenetic signal that the strength of sexual selection accelerated the speed of evolution. Moreover, other factors, such as female morphology and ecological differences, also contributed to the diversification patterns across the phylogeny. For example, divergence in environmental niche can explain the evolution of Golden Pheasant (Chrysolophus pictus) and Lady Amherst’s Pheasant (C. amherstiae). The authors concluded that their findings add “to the growing body of literature suggesting that multiple factors work in concert and that focusing on sexual selection alone as a driver of diversification may lead to erroneously narrow conclusions.”

Indeed, although sexual selection has played an important role in certain gallopheasant species (as exemplified by their extravagant plumage), we should not automatically discard other processes. Evolution involves the complex interplay of numerous selective pressures, spiced up with some chance events.

References

Hosner, P. A., Owens, H. L., Braun, E. L., & Kimball, R. T. (2020). Phylogeny and diversification of the gallopheasants (Aves: Galliformes): Testing roles of sexual selection and environmental niche divergence. Zoologica Scripta, 49(5), 549-562.

Featured image: Golden Pheasant (Chrysolophus pictus) © Eric Kilby | Wikimedia Commons

A genomic continuum from feral to wild Red Junglefowl in Singapore

The admixed nature of the population raises several conservation issues.

Hybridization and the consequent exchange of genetic material (i.e. introgression) is not limited to wild populations. Domesticated animals or plants regularly interbreed with their wild relatives and genes flow both ways. These hybridization events can be accidental. After the disaster at the Fukushima Nuclear Power Plant in 2011, for example, several domestic pigs (Sus scrofa) escaped into the Japanese nature and hybridized with local wild boars. In other cases, captive animals are intentionally released into the wild, such as the restocking of European partridge populations with the non-native Chukar Partridge (Alectoris chukar) for hunting purposes. Unsurprisingly, the introduced partridges interbred with the local birds. Another example of hybridization between domestic and wild birds concerns chickens (Gallus gallus) in Singapore and was recently described in the journal Evolutionary Applications. Time for a trip to Asia!

 

Museum Samples

Wild chickens – the Red Junglefowl – were thought to be extinct in Singapore until they were rediscovered on the island Ubin in 1970. These birds probably crossed the 800 meter wide sea channel from the neighboring island Johor (part of Malaysia). Years later, Red Junglefowl also roamed the main island of Singapore. This recolonization was accompanied by an increase in domestic chickens (whether intentionally released or escaped remains uncertain) that occasionally hybridized with their wild relatives. This situation leads to an interesting discussion: are the Red Junglefowl populations on Singapore really wild? Or are they a mixture of wild and domesticated birds? Meng Yue Wu and her colleagues turned to genomic data to solve this mystery.

Studying introgression in chickens is challenging because there has been gene flow between several species and breeds (as explained in this blog post). To obtain a genomic reference for the wild Red Junglefowl, the researchers used two museum samples that were collected about 150 years ago on Malaysia. Next, they sequenced the DNA of 70 free-roaming birds from Singapore. The genomic analyses revealed a continuum from domestic to wild chickens with varying levels of introgression. There were no clear spatial patterns, suggesting that the wild and domestic chickens are freely mixing in Singapore (although most wild-type birds seem to cluster around Singapore’s largest national park).

Genomic analyses revealed a continuum from domestic (orange) to wild (blue) birds in Singapore. Each column represents an individual and the colors indicate the percentage of wild and domestic ancestry in the genome. The museum samples are indicated with stars in figure a. The three graphs represent different analyses: (a) all genomic samples, (b) all genomic samples without museum specimens, and (c) all genomic samples + additional RADseq samples. From: Wu et al. (2020) Evolutionary Applications.

 

Conservation

These findings result in a conservation conundrum. On the one hand, managers might warn that the wild Red Junglefowl on Singapore have been “genetically contaminated” by domestic genes. On the other hand, the exchange of genetic material might lead to higher genetic diversity and could potentially speed up adaptation.

Morphological analyses of the Singaporean chickens indicated that a handful of traits (tarsus and primary feather coloration for females and tail feather, primary feather, and lappet coloration for males) can be used to confidently discriminate between wild and domestic chickens. It is thus feasible to detect and remove “introgressed” individuals from the population. Should we intervene or not? I will not try to answer this question here, but feel free to share your thoughts in the comments below.

The researchers studied several traits to see whether it is possible to tell the difference between wild, domestic and mixed individuals. From: Wu et al. (2020) Evolutionary Applications.

 

References

Wu, M. Y., Low, G. W., Forcina, G., van Grouw, H., Lee, B. P. Y. H., Oh, R. R. Y., & Rheindt, F. E. (2020). Historic and modern genomes unveil a domestic introgression gradient in a wild red junglefowl population. Evolutionary Applications, 13(9), 2300-2315.

Featured Image: © Seng Alvin | Singapore Bird Group

 

This paper has been added to the Galliformes page.

How many ancestral species gave rise to the domestic chicken breeds?

Genomic data provide an answer to this long-standing debate?

In 1868, Charles Darwin wrote that “we have not such good evidence with fowls as with pigeons, of all breeds having descended from a single primitive stock.” This statement is rather surprising if you read The Origin of Species – published in 1859 – where he argued that all domestic chicken breeds descend from a single ancestor: the Red Junglefowl (Gallus gallus, then named Gallus bankvia). Where did the uncertainty in 1868 about the origin of domestic chickens come from? A recent paper by Hein van Grouw and Wim Dekkers in the Bulletin of the British Ornithologists’ Club reconstructed the historical events leading up to Darwin’s uncertainty.

 

Giant Chickens

Our story begins with French naturalist Georges–Louis Leclerc, Comte de Buffon who believed that different chicken breeds can be traced back to several ancestral wild species (i.e. a polyphyletic origin). For example, he stated that most European breeds descended from the wild Red Junglefowl, while seven giant chicken breeds could be traced back an unknown wild ancestor. Several decades later, Coenraad Jacob Temminck (director of the State Museum of Natural History in Leiden) received a single foot of very large fowl from Indonesia. He assumed it belonged to a large species of wild junglefowl and described it as the Jago Cock (Gallus giganteus). Could this be the ancestor that Buffon predicted?

Edward Blyth, the curator of the Asian Society of Bengal in Calcutta, rejected the polyphyletic origin of chicken breeds. He argued that the varieties of domesticated chickens had evolved by artificial selection from a single wild ancestor: the Red Junglefowl. This monophyletic theory, published in 1851, caught the attention of Charles Darwin because it supported his analogy between artificial selection by humans and natural selection. If humans can create such diverse creatures in a few generations, imagine what nature can do over millions of years! The two naturalists corresponded about the domestication of chickens and in one letter Blyth firmly buried the polyphyletic ideas of Buffon and Temminck, writing: “My very decided opinion, that we may seek in vain for wild types of G. giganteus.”

The foot of Gallus giganteus (© Jonathan Jackson, Natural History Museum, London) and an artistic impression of a giant domestic breed by Benjamin Waterhouse Hawkins in Gray & Hardwicke’s Illustrations of Indian zoology (© Ben Nathan, Natural History Museum, London)

 

Darwin’s Doubt

In The Origin of Species, Darwin credits Blyth for the monophyletic idea: “Mr. Blyth, whose opinion, from his large and varied stores of knowledge, I should value more than that of almost any one, thinks that all the breeds of poultry have proceeded from the common wild Indian fowl.” So, why did Darwin change his mind a few years later? Following the First Opium War between the Qing dynasty and the United Kingdom (1839-1842), several large chicken breeds reached the English naturalists from Asia. After studying these peculiar specimens, Darwin was unsure whether some morphological characters could have been the result of artificial selection from a single ancestor. Perhaps different domestic chicken breeds did originate from different ancestors, such as the Jago Cock?

Darwin continued to investigate the origin of chicken breeds and studied the skeletons and skulls of several breeds. In one breed – the Cochin – he observed certain features that did not occur in Red Junglefowl or any of the other breeds. Despite the aberrant morphology of the Cochin breed, Darwin focused on the similarities between the other breeds and concluded that these chicken breeds probably had a monophyletic origin.

The Cochin, with its deeply furrowed frontal bones, peculiarly shaped occipital
foramen, short wing-feathers, short tail containing more than fourteen feathers, broad nail to the middle toe, fluffy plumage, rough and dark-coloured eggs, and especially from its peculiar voice, is probably the most distinct of all the breeds. If any one of our breeds has descended from some unknown species, distinct from G. bankiva [Gallus gallus], it is probably the Cochin; but the balance of evidence does not favour this view.

The peculiar Cochin breed. © Willem & Martijn Hoekstra

 

The Genomic Picture

The morphological studies of Darwin and other naturalists did not completely settle the debate about the polyphyletic or monophyletic origin of chicken breeds. The uncertainty is obvious in Darwin’s quotes cited above. Nowadays we can turn to genomic data to answer questions about the domestication of certain animals and plants. And that is exactly what Raman Akinyanju Lawal and his colleagues did. They sequenced the genomes of 53 domestic chickens and several individuals of four wild species: the Red Junglefowl, the Grey Junglefowl (G. sonneratii), the Ceylon Junglefowl (G. lafayettii) and the Green Junglefowl (G. varius).

Phylogenomic analyses revealed that the domestic chickens clustered with the Red Junglefowl (see figure below), suggesting that they all originated from a single ancestor. However, D-statistics pointed to gene flow between between domestic chickens and the Grey, Ceylon, and Green Junglefowl species (see this blog post for details on D-statistics). A closer look at particular introgressed regions suggested that they were recently exchanged between the species. For example, some introgressed tracts were relatively long and have thus not been broken down by recombination. Taken together, these patterns show that domestic chicken breeds originated from a single ancestor (the Red Junglefowl) and received genetic material from other species later on. So, while the origin of domestic chickens is monophyletic, their current genetic make-up is polyphyletic.

The evolutionary tree of chicken breeds and species based on genomic data. Notice that all domestic chickens (darkblue) cluster with Red Junglefowl (red). Adapted from: Lawal et al. (2020) BMC Biology

 

References

Lawal, R. A., et al. 2020). The wild species genome ancestry of domestic chickens. BMC Biology, 18(1), 1-18.

van Grouw, H., & Dekkers, W. (2020). Temminck’s Gallus giganteus; a gigantic obstacle to Darwin’s theory of domesticated fowl origin?. Bulletin of the British Ornithologists’ Club, 140(3), 321-334.

Featured picture: Feral rooster on Kauaʻi © Frank Schulenburg | Wikimedia Commons

 

The papers have been added to the Galliformes page.