Asymmetric allelic introgression across a hybrid zone of the coal tit (Periparus ater) in the central Himalayas

Abstract

In the Himalayas, a number of secondary contact zones have been described for vicariant vertebrate taxa. However, analyses of genetic divergence and admixture are missing for most of these examples. In this study, we provide a population genetic analysis for the coal tit (Periparus ater) hybrid zone in Nepal. Intermediate phenotypes between the distinctive western "spot-winged tit" (P. a. melanolophus) and Eastern Himalayan coal tits (P. a. aemodius) occur across a narrow range of <100 km in western Nepal. As a peculiarity, another distinctive cinnamon-bellied form is known from a single population so far. Genetic admixture of western and eastern mitochondrial lineages was restricted to the narrow zone of phenotypically intermediate populations. The cline width was estimated 46 km only with a center close to the population of the cinnamon-bellied phenotype. In contrast, allelic introgression of microsatellite loci was asymmetrical from eastern P. a. aemodius into far western populations of phenotypic P. a. melanolophus but not vice versa. Accordingly, the microsatellite cline was about 3.7 times wider than the mitochondrial one.

Keywords: Nepal; birds; cline analysis; hybridization; microsatellites; mitochondrial DNA.

FIGURE 1

Hybrid zone models, modified and extended from Curry (2015), parental forms in black and white, hybrids in gray. (a) clinal zone, bimodal (e.g., crows, great tits); (b) clinal zone, unimodal (hybrids dominate); (c) mosaic hybrid zone (e.g., sparrows in North Africa); (d) microallopatry (e.g., coal tits in the Himalayas, this study)

FIGURE 2

Areas of secondary overlap in the Western Himalayas for three passerine taxon pairs, each represented by two distinct genetic mtDNA lineages (western = yellow; eastern = red). (a) orange bullfinch, Pyrrhula aurantiaca, and red‐headed bullfinch, P. erythrocephala (data from eBird, ; Töpfer et al., ; Wunderlich, 1992a, 1992b), local sympatry: orange circles); (b) white‐throated bushtit, Aegithalos niveogularis, and black‐browed tit, Ae. iouschistos (data from eBird, ; Päckert et al., ; Wunderlich, 1989, 1991); (c) greenish warbler, P. trochiloides, pie charts show local frequencies of haplotypes from the eastern (P. t. trochiloides: red) and western (P. t. ludlowi: yellow) mtDNA lineage; data modified from Irwin et al. (2001) and Irwin et al. (2005); distribution shape files from BirdLife International (2020); Shape file for P. trochiloides modified according to Irwin et al. (2001) and Irwin et al. (2005); maps produced with QGIS v. 3.10

FIGURE 3

The Himalayan contact zone of western and eastern subspecific taxa of the coal tit. Parental taxa: Periparus ater melanolophus (phenotype 1, population i) and P. a. aemodius (phenotype 4, population vi); pie charts show local frequencies of CR haplotypes from the western (yellow; n = 9) and eastern (red; n = 8) lineages (compare Figure 4); putative hybrid populations with intermediate phenotypes exist in a narrow area of overlap in Central Nepal (from west to east): spot‐winged‐type hybrids (population ii), cinnamon‐bellied hybrids (phenotype 2, population iii, occurrence at Dhorpatan in local sympatry with the spot‐winged‐type), pale‐bellied hybrids (population iv, at Myagdi Khola) and P. a. martensi (phenotype 3, population v); symbolization: brightly‐colored dots = own samples, pale dots = records by Martens and Eck (1995), triangles = data from online databases (sound recordings from xeno‐canto, ; photographs revisited at Oriental Bird Club, 2017), red‐shaded area = distribution according to BirdLife International (2021); drawings by K. Rehbinder

FIGURE 4

Genetic differentiation of coal tits across and beyond the Himalayan contact zone. (a) minimum‐spanning haplotype network of mtDNA CR sequences (324 bp), including mitochondrial lineages from the Himalayas (western = yellow; eastern = red) and adjacent lineages from China (blue) and from the Russian Far East (white; including sequence data from Pentzold et al., 2013); (b) PCA of microsatellite data (all ten loci; x‐axis = PC1, y‐axis = PC2; boxes = centroids for the three groups); first three principal components each explain 4.58%, 4.03% and 3.66% of variation (Eigenvalues shown in square lower left); drawings by K. Rehbinder

FIGURE 5

Time‐calibrated phylogeny for 30 control‐region haplotypes (324 bp) of Asian coal tit (Periparus ater) populations and two outgroups (Pardaliparus venustulus; Cyanistes caeruleus). Bayesian tree inferred from MCMC run with BEAST for 50 million generations, trees sampled every 5000 generation, uncorrelated lognormal clock model, Yule tree prior, burnin 30%; node support from posterior probabilities shown above nodes (except internal topology of each of the four Asian clades; most values < 0.9)

FIGURE 6

Genetic variation of Himalayan coal tit populations (Periparus ater; n = 67) based on 10 microsatellite loci. STRUCTURE analysis under the admixture‐frequency‐correlated model without locpriors a priori defined, STRUCTURE plot for most plausible K = 2; threshold q > 0.8 for assignment of individuals to genetic clusters according to Randi (2008); colored bars above the plot indicate individual assignment to the western (P. a. melanolophus) and eastern (P. a. aemodius) mitochondrial lineage, respectively; bars below the plot indicate phenotypically distinct populations along the east‐west gradient; asterisks at the top highlight genetic hybrid individuals

FIGURE 7

Cline analysis for Himalayan coal tits, Periparus ater. Based on mitochondrial CR sequences (a) shape, (c) center, (e) width and based on 10 microsatellite loci (b) shape, (d) center, (f) width; shape of the cline, (a, b): crosses indicate observed values (haplotype and allele frequencies) for each population; solid curves indicate maximum‐likelihood estimates of the cline with gray shapes indicating 95% CI of the estimates; solid lines indicate cline center estimates with dashed lines indication 95% CI of the estimates; major areas of origin indicated above: AFG, Afghanistan; HUM, Humla Distr.; DOL, Dolpo Distr.; DHO, Dhorpatan (Baglung Distr.); MYA, Myagdi Distr.; RAS, Rasuwa Distr.; SIN, Sindhu Palchok Distr.; TAP, Taplejung Distr