Strong selection on male plumage in a hybrid zone between a hybrid bird species and one of its parents

Abstract

Homoploid hybrid speciation (HHS) requires reproductive barriers between hybrid and parent species, despite incomplete reproductive isolation (RI) between the parents. Novel secondary sexual trait values in hybrids may cause prezygotic isolation from both parents, whereas signals inherited by the hybrid from one parent species may cause prezygotic isolation with the other. Here we investigate whether differences in male plumage function as a premating barrier between the hybrid Italian sparrow and one of its parent species, the house sparrow, in a narrow Alpine hybrid zone. Italian sparrow male plumage is a composite mosaic of the parental traits, with its head plumage most similar to its other parent, the Spanish sparrow. We use geographical cline analysis to examine selection on three plumage traits, 75 nuclear single nucleotide polymorphisms (SNPs) and hybrid indices based on these SNPs. Several SNPs showed evidence of restricted introgression in the Alps, supporting earlier findings. Crown colour exhibited the narrowest plumage cline, representing a 37% (range 4-65%) drop in fitness. The cline was too narrow to be due to neutral introgression. Only crown colour was significantly bimodal in the hybrid zone. Bimodality may be due to RI or a major QTL, although fitness estimates suggest that selection contributes to the pattern. We discuss the implications with respect to HHS and the species status of the Italian sparrow.

The genomic mosaicism of hybrid speciation

“…For the PI genes, one of the significantly enriched classes was “dorsoventral pattern formation,” which encompasses a wide range of anatomical features, from body plan to color patterning. Plumage coloration constitutes a strong mating barrier in many bird species and is the most conspicuous phenotypic trait separating males of the focal species ( 27 ). Furthermore, the PI windows included four genes known to be associated with melanogenesis in vertebrates (table S10) ( 28 ), and a total of 13 such genes were identified in the other species comparisons, significantly more than expected by chance (one-sided permutation test; P < 0.044).…”

Differential introgression of a female competitive trait in a hybrid zone between sex‐role reversed species

“…This plumage difference in sympatry with a heterospecific is suggestive of reproductive character displacement. Whereas clines for plumage traits involved in reproductive isolation are often more narrow than genome-wide markers (Bailey et al 2015;Semenov et al 2017), it is possible that near-complete reproductive isolation due to intrinsic incompatibilities between the two jacana species results in similar patterns of introgression of plumage traits as background genome-wide markers.…”

Genetic admixture despite ecological segregation in a North African sparrow hybrid zone (Aves, Passeriformes, Passer domesticus × Passer hispaniolensis)

“…In previous studies, phenotypic diagnosis of the house sparrow, Spanish sparrow, and the Italian sparrow has mainly relied on male plumage color patterns mostly of the crown, the cheek, and the back (Bailey et al, ; Hermansen et al, ; Runemark, Bailey, Bache‐Mathiesen, & Sætre, ). Compared to Italian sparrow populations, Rothschild and Hartert () described a great phenotypic diversity of North African sparrow populations and distinguished 20 different head color patterns.…”

“…In previous studies, phenotypic diagnosis of the house sparrow, Spanish sparrow, and the Italian sparrow has mainly relied on male plumage color patterns mostly of the crown, the cheek, and the back (Bailey et al, 2015;Hermansen et al, 2011; F I G U R E 1 Palearctic distribution of the house sparrow (Passer domesticus: allopatric = gray shape), the Spanish sparrow (Passer hispaniolensis: light brown shape = allopatric; dark brown shape = sympatric with the house sparrow), and hybrid populations (yellow): stabilized hybrid form Italian sparrow (Passer italiae, on the Italian Peninsula, Corsica, Sicily, Malta, Crete, and other Mediterranean islands; zone A: hybrid zone with the house sparrow); mixed populations of phenotypic hybrids and the two parental species in North Africa (predominantly Algeria, zone B); red dots: sampled populations for genetic analysis cheek, breast, flanks, and back; as done by Belkacem et al, 2016).…”

“…In contrast, local contact between the Italian sparrow and its second parent is limited to a small introduced population of Spanish sparrows on Gargano Peninsula, where gene flow between the two taxa is restricted by strong ecological segregation and divergence of behavioral traits (Sætre et al, ). Previous field studies and genomic analyses show a scenario with a clear‐cut zoogeographic pattern of sympatry and parapatry of the two parental species and the Italian hybrid on the Eurasian continent that was shaped by complex interaction of (a) parental genetic incompatibilities (Elgvin et al, ; Eroukhmanoff et al, ; Hermansen et al, ; Trier, Hermansen, Sætre, & Bailey, ); (b) sexual selection on phenotypic traits (Bailey, Tesaker, Trier, & Sætre, ; Runemark, Fernández, Eroukhmanoff, & Sætre, ); and (c) selection on functional traits associated with ecological preferences (such as beak size and shape; Eroukhmanoff, Hermansen, Bailey, Sæther, & Sætre, ).…”