Rapid polygenic response to secondary contact in a hybrid species

Abstract

Secondary contact between closely related species can have genetic consequences. Competition for essential resources may lead to divergence in heritable traits that reduces interspecific competition leading to increased rate of genetic divergence. Conversely, hybridization and backcrossing can lead to genetic convergence. Here, we study a population of a hybrid species, the Italian sparrow (Passer italiae), before and after it came into secondary contact with one of its parent species, the Spanish sparrow (P. hispaniolensis), in 2013. We demonstrate strong consequences of interspecific competition: Italian sparrows were kept away from a popular feeding site by its parent species, resulting in poorer body condition and a significant drop in population size. Although no significant morphological change could be detected, after only 3 years of sympatry, the Italian sparrows had diverged significantly from the Spanish sparrows across a set of 81 protein-coding genes. These temporal genetic changes are mirrored by genetic divergence observed in older sympatric Italian sparrow populations within the same area of contact. Compared with microallopatric birds, sympatric ones are genetically more diverged from Spanish sparrows. Six significant outlier genes in the temporal and spatial comparison (i.e. showing the greatest displacement) have all been found to be associated with learning and neural development in other bird species.

Keywords: Passer; character displacement; cognition; hybrid species; interspecific competition; learning.

Figure 1.

Species composition in the general zone of secondary contact and test for introgressive hybridization. (a) Map showing the six sampling localities. Blue points indicate microallopatric localities and blue and red points indicate sympatric localities. The Lago Salso locality (grey point) was sampled in 2012 when Italian sparrows lived microallopatrically and in 2015, the third year after Spanish sparrows established there and the population became sympatric. (b,c) Density of assignment probability to the Italian sparrow genetic cluster according to structure analysis [15]. Blue colour indicates phenotypic Italian sparrows and red colour indicates phenotypic Spanish sparrows.

Figure 2.

Temporal changes in feeding ecology, body condition and population size of an Italian sparrow population before and after it experienced secondary contact with the Spanish sparrow in Lago Salso station. (a) Map of Lago Salso station. Dark grey rectangles are buildings where nest-boxes had been put up and where Italian sparrows were breeding; Spanish sparrows were breeding in stork nests (dark orange hexagons); the main feeding sites used by sparrows were a cereal field (light orange) and a poultry pen (yellow circle); green dots represent trees and bushes and light grey represent roads and parking lots. (b) Habitat segregation. The number of birds captured in mist nets strategically placed near two main feeding sites, a cereal field and a poultry pen. (c) Change in body condition measured as body mass/tarsus length. ANOVA: F_1,167 = 20.8, p < 0.0001***. (d) Changes in effective population size (Ne). (e) Changes in census population size (Nc).

Figure 3.

Genetic changes following secondary contact and genetic differences between microallopatric and sympatric Italian sparrows. In all panels, genetic divergence refers to the algebraic difference between locus-specific divergence from Spanish sparrows (F_ST) in sympatry and microallopatry. Positive values indicate evolution towards genetic displacement (purple colour) and negative values indicate evolution towards genetic convergence (green colour). (a,b) The density-distribution of the algebraic difference between locus-specific divergence from Spanish sparrows (F_ST) in sympatry and microallopatry for the temporal and spatial comparison, respectively, is shown. Black arrows indicate significantly displaced loci and the red arrow indicates a locus (PTPRM) that is significantly displaced in both the temporal and spatial comparison. (c) Positive displacement of the spatial outliers in the temporal comparison. (d) Positive displacement of the temporal outliers in the spatial comparison. (e) Genetic divergence among chromosomes in the temporal comparison. (f) Genetic divergence among chromosomes in the spatial comparison. Asterisks indicate chromosomes that were significantly displaced.