Friday, September 30, 2022

[Ornithology • 2022] Genome-wide SNPs confirm Plumage Polymorphism and Hybridisation within A Cyornis Flycatcher Species Complex



in Ng, Li, Zhang, Garg, ... et Lei, 2022. 

Abstract
Morphology has been a leading taxonomic guiding light to systematists for the last couple of hundred years. However, the genetic and – more recently – genomic revolution have produced numerous demonstrations of erroneous classifications that were based on labile morphological traits. We used thousands of genome-wide markers to shed light on evolutionary dynamics in a confusing and taxonomically obscure group of Asian Cyornis flycatchers. Using genomic data, we corroborated recent findings based on three mitochrondrial and five nuclear genes that the two taxa hainanus and klossi which were previously treated as separate species (Cyornis hainanus and Cyornis rubeculoides klossi, respectively) are genomically homogeneous and form a single species, C. hainanus. We also uncovered a novel case of interbreeding between C. hainanus and a non-sister species, C. glaucicomans, illustrating these flycatchers' ability to hybridise in marginal situations even after substantial times of divergence. Our study illustrates how genome-wide loci can shed light on complicated taxonomic problems, resulting in a better integration of phenotypic and genotypic data.

Keywords: Cyornis, ddRADseq, introgression, phylogenetics, species complex


(a) Distribution range of Cyornis rubeculoides and C. hainanus. Sampling localities are indicated by coloured circles, and the size of the circles is proportional to sample size. Approximate distributions of subspecies are indicated with dashed lines, but it should be noted that the subspecies distributions are poorly understood, especially the range of dialilaemus. Photographs of C. rubeculoides by Ashutosh Singh are reproduced here with permission from Singh et al. (2019).
(b) Maximum likelihood tree based on 21,283 SNPs, with bootstrap support indicated at major nodes. Colours represent different taxa: red, C. r. rubeculoides; orange, C. r. rogersi; blue, C. hainanus hainanus and C. h. klossi; green, C. glaucicomans; and pink, C. unicolor unicolor (outgroup). Plumage-type assignment for male C. hainanus is indicated by the squares, with typical hainanus in blue squares labelled with a h, typical klossi-type plumage in orange with a k and intermediate plumage types in both orange and blue squares and labelled with a h/k. Females have a brown square without any labels.
 (c) Species tree for all individuals generated with SNAPP


Photos of male Cyornis hainanus showing variability in breast coloration from typical C. h. klossi (a, o, p) to typical C. h. hainanus (l, m, n, s) and birds with intermediate characteristics in between. (a) Dakrong, Quang Tri, Vietnam, 25 March 2004; (b) Dakrong, Quang Tri, Vietnam, 4 April 2004; (c) Xitou, Guangdong, China, 29 September 2014 [IOZ-JM019]; (d) Leizhou, Guangdong, China, 24 October 2014 [IOZ-JM024]; (e) Dakrong, Quang Tri, Vietnam, 4 April 2004; (f) Leizhou, Guangdong, China, 13 November 2013; (g) Sanjia Shan, Guangdong, China, 20 April 2014 [IOZ-JM003]; (h) Weizhou Island, Guangxi, China, 15 April 2013; (i) Longtan, Guangxi, China, 01 June 2015; (j) Leizhou, Guangdong, China, 13 November 2013; (k) Vu Quang National Park, Ha Tinh, Vietnam, 13 March 2005; (l) Xitou, Guangdong, China, 27 September 2014 [JM013]; (m) Yunfu, Guangdong, China, 12 May 2014 [IOZ-JM005]; (n) Heweishan, Guangdong, China, 26 May 2014 [IOZ-JM006]; (o) Tra My, Quang Nam, Vietnam [AMNH833192]; (p) from left to right, Bolovens plateau, Thatèng, Xedong, Laos, 28 November 1931 [MNHN-ZO-MO-1933-72]; Quang Tri, Annam, Vietnam, 22 February 1924 [MNHN-ZO-MO-1924-665]; (q) Trakam, Laos, 29 April 1927 [MNHN-ZO-MO-1929-1100]; Bolovens plateau, Thatèng, Xedong, Laos, 28 November 1931 [MNHN-ZO-MO-1933-73]; Di Linh Plateau, Vietnam, 14 March 1927 [MNHN-ZO-MO-1928-385]; (r) Hainan, China, 9 October 1962 [GIABR-0275]; Ledong, Hainan, China 25 October 1962 [GIABR-0367]; Bawangling, Hainan, China 15 January 1964 [GIABR-2200]; (s) Paksé, Laos, 5 January 1932 [MNHN-ZO-MO-1933-74]; Siem Reap, Cambodia, 27 December 1927 [MNHN-ZO-MO-1929-1092]; Angkor, Siem Reap, Cambodia, December 1927 [MNHN-ZO-MO-1929-1093]; Angkor, Siem Reap, Cambodia, 4 February 1962 [MNHN-ZO-MO-61]. Photos in (a, b, e) by Peter Nilsson at Swedish Museum of Natural History; Photos in (c, d, f, g-j, l-n, p-s) by Jonathan Martinez; Photo in K by Ingrid Cederholm at the Swedish Museum of Natural History; Photo in (o) by Paul Sweet at the American Museum of Natural History. Abbreviations: AMNH – American Museum of Natural History, New York, USA; GIABR – Guangdong Institute of Applied Biological Resources; IOZ – Institute of Zoology, Beijing, China; MNHN – Muséum National d'Histoire Naturelle, Paris, France

Photos of male Cyornis hainanus showing variability in breast coloration from typical C. h. klossi (a, o, p) to typical C. h. hainanus (l, m, n, s) and birds with intermediate characteristics in between.

CONCLUSIONS: 
The classification of Cyornis flycatchers has undergone substantial change over the last two decades, resulting in taxonomic rearrangements, in particular the synonymisation of the genus Rhinomyias with Cyornis (Sangster et al., 2010; Zhang et al., 2016; Zuccon & Ericson, 2010). Our study demonstrates that population-genomic and phylogenomic methodologies can effectively be applied to disentangle the complicated evolutionary history of cryptic species complexes such as the Cyornis flycatchers. Our ddRADseq data set confirms the remarkable case of incongruence between plumage and genomic divergence that has misled previous taxonomists into erroneous classifications (Zhang et al., 2016). Our results also show a novel interbreeding event between two non-sister species.

 
Elize Y. X. Ng, Siqi Li, Dezhi Zhang, Kritika M. Garg, Gang Song, Jonathan Martinez, Le Manh Hung, Vuong Tan Tu, Jérôme Fuchs, Lu Dong, Urban Olsson, Yuan Huang, Per Alström, Frank E. Rheindt and Fumin Lei. 2022. Genome-wide SNPs confirm Plumage Polymorphism and Hybridisation within A Cyornis Flycatcher Species Complex. Zoologica Scripta. DOI: 10.1111/zsc.12568

• Using genome wide markers, our study confirmed that 𝘊𝘺𝘰𝘳𝘯𝘪𝘴 𝘩𝘢𝘪𝘯𝘢𝘯𝘶𝘴 𝘬𝘭𝘰𝘴𝘴𝘪 was the same species as 𝘊. 𝘩. 𝘩𝘢𝘪𝘯𝘢𝘯𝘶𝘴.
• Based on plumage alone, 𝘊. 𝘩. 𝘬𝘭𝘰𝘴𝘴𝘪 was historically placed in the same species as 𝘊. 𝘳𝘶𝘣𝘦𝘤𝘶𝘭𝘰𝘪𝘥𝘦𝘴. 
• Furthermore, in the same study, we also uncovered the first reported instance of hybridization between 𝘊. 𝘩𝘢𝘪𝘯𝘢𝘯𝘶𝘴 and 𝘊 𝘨𝘭𝘢𝘶𝘤𝘪𝘤𝘰𝘮𝘢𝘯𝘴