Phylogeography of theOenanthe hispanica-pleschanka-cypriacacomplex (Aves, Muscicapidae: Saxicolinae): Diversification history of open-habitat specialists based on climate niche models, genetic data, and morphometric data

Abstract

The succession of glacials and interglacials during the Pleistocene strongly influenced the diversification and distribution patterns in birds. In contrast to species of temperate regions, open‐habitat specialists should have experienced range expansion during the longer glacial periods, while range contractions occurred during the shorter interglacials. However, only few studies have tested this prediction so far. We studied the Oenanthe hispanica–pleschanka–cypriaca (Aves, Muscicapidae: Saxicolinae) complex characteristic of open habitats in the Palearctic. Based on three mitochondrial and one Z‐linked nuclear marker, we inferred its phylogeny, historical diversification, and demography. Ecological niche modeling was used to reconstruct potential distributions during the last glacial maximum and the last interglacial. Using 19 morphological traits, we tested for morphometric differences among the different taxa. Mitochondrial markers revealed strong genetic differences between O. h. hispanica and the other taxa with a divergence event at around 1.7 million years ago. No consistent genetic differences were revealed between O. cypriaca, O. h. melanoleuca, and O. pleschanka. The latter two hybridize in contact zones, which might explain partly the lack of genetic differentiation; yet, further analyses using genomic data are needed to infer the true divergence history of the complex. Signs of population expansions in the clade comprising O. h. melanoleuca, O. pleschanka, and O. cypriaca at 90,000 years ago coincided with the last glacial as predicted. Population expansion then was also supported by ecological climate niche models. O. h. hispanica was not consistently separated from the other taxa in morphometrics. It might nonetheless warrant species status, pending further analyses.

Parallel plumage colour evolution and introgressive hybridization in wheatears

“…Multispecies coalescent analyses revealed an unambiguously resolved species tree (Bayesian posterior probabilities for all nodes: 1), with an unexpected topology that is discordant with similarities in colour patterns (Figure 1a). In line with previously reported mitochondrial divergence patterns (Alaei Kakhki et al, 2016Kakhki et al, , 2018Aliabadian et al, 2012), the deepest divergence is between western black-eared wheatear and the other three taxa. Within the latter, our analyses identified eastern blackeared wheatear and Cyprus wheatear as sister species, contrary to original taxonomy that treated Cyprus wheatear as a subspecies of pied wheatear based on these species' highly similar coloration ( Figure 1a).…”

“…However, a scenario of introgression from pied into Cyprus wheatear (or its common ancestor with eastern black‐eared wheatear) cannot be completely dismissed. First, mitochondrial lineages are shared between all but western black‐eared wheatears (Alaei Kakhki et al., ; Randler et al., ). Second, proportions of introgression inferred from pied into eastern black‐eared wheatear are twice the potential ones among western and eastern black‐eared wheatears (Table ).…”

“…Based mainly on their distinct colour phenotypes, these taxa are currently assigned to three species (Gill & Donsker, ), although species rank was proposed for all by some authors (Sangster, Hazevoet, Van den Berg, Roselaar, & Sluys, ): (a) the island endemic Cyprus wheatear ( O. cypriaca ); (b) pied wheatear ( O. pleschanka ), breeding from the western shores of the Black Sea to eastern China; (c) and black‐eared wheatear ( O. hispanica ), with a western subspecies ( O. h. hispanica ) breeding in the western Mediterranean and North Africa, and an eastern subspecies ( O. h. melanoleuca ) breeding from southern Italy and the Balkans to central Iran (Figure ). The four taxa overlap morphometrically (Alaei Kakhki et al., ; Kaboli, Aliabadian, Guillaumet, Roselaar, & Prodon, ) , but males differ in patters of black‐and‐whitish (or pale) coloration. Cyprus and pied wheatear, formerly treated as conspecific, display black mantle and neck sides, while these are white in both subspecies of black‐eared wheatear (Figure ).…”

“…A particularly interesting group of wheatears that displays the same phenotypic mosaic at smaller phylogenetic scale is composed of four taxa ( Figure 1) with yet unclear phylogenetic relationships. Based mainly on their distinct colour phenotypes, these taxa are currently assigned to three species (Gill & Donsker, 2018), although species rank was proposed for all by some authors (Sangster, Hazevoet, Van den Berg, Roselaar, & Sluys, 1999) Kakhki et al, 2018;Kaboli, Aliabadian, Guillaumet, Roselaar, & Prodon, 2007), but males differ in patters of black-and-whitish (or pale) coloration. Cyprus and pied wheatear, formerly treated as conspecific, display black mantle and neck sides, while these are white in both subspecies of black-eared wheatear ( Figure 1).…”

Significant Asia‐Europe divergence in the middle spotted woodpecker (Aves, Picidae)

“…Many Holarctic temperate and boreal plants and animals showed range contraction and could survive in only one or a few refugia in the south of the continent during cold and arid glacials, but expanded their ranges and colonized areas to the north during warmer and wetter interglacials (Hewitt, ; Taberlet, Fumagalli, Wust‐Saucy, & Cosson, ; Weir & Schluter, ). In contrast, the ranges of arid‐adapted species in ice‐free areas contracted during interglacials and expanded during glacials (Alaei Kakhki et al, ; Garcia, Alda, et al, ; Garcia, Mañosa, et al, ). Some species also could have survived the glacial maxima at higher temperate latitudes in so‐called cryptic refugia (Provan & Bennett, ).…”