Disentangling Timing of Admixture, Patterns of Introgression, and Phenotypic Indicators in a Hybridizing Wolf Population

Abstract

Hybridization is a natural or anthropogenic process that can deeply affect the genetic make-up of populations, possibly decreasing individual fitness but sometimes favoring local adaptations. The population of Italian wolves (Canis lupus), after protracted demographic declines and isolation, is currently expanding in anthropic areas, with documented cases of hybridization with stray domestic dogs. However, identifying admixture patterns in deeply introgressed populations is far from trivial. In this study, we used a panel of 170,000 SNPs analyzed with multivariate, Bayesian and local ancestry reconstruction methods to identify hybrids, estimate their ancestry proportions and timing since admixture. Moreover, we carried out preliminary genotype–phenotype association analyses to identify the genetic bases of three phenotypic traits (black coat, white claws, and spur on the hind legs) putative indicators of hybridization. Results showed no sharp subdivisions between nonadmixed wolves and hybrids, indicating that recurrent hybridization and deep introgression might have started mostly at the beginning of the population reexpansion. In hybrids, we identified a number of genomic regions with excess of ancestry in one of the parental populations, and regions with excess or resistance to introgression compared with neutral expectations. The three morphological traits showed significant genotype–phenotype associations, with a single genomic region for black coats and white claws, and with multiple genomic regions for the spur. In all cases the associated haplotypes were likely derived from dogs. In conclusion, we show that the use of multiple genome-wide ancestry reconstructions allows clarifying the admixture dynamics even in highly introgressed populations, and supports their conservation management.

Genomic consequences of a recent three‐way admixture in supplemented wild brown trout populations revealed by local ancestry tracts

“…Using extensive individual genomic data and the brown trout as a case study, we hereby showed that the information contained in local ancestry blocks might improve the detection of admixture patterns at both the individual and population levels. Few others studies (Galaverni et al, 2017;Nelson et al, 2017;VonHoldt et al, 2016) also explored this issue, but this certainly has to be expanded further. For example, an in-depth analysis of the genomewide landscape of introgression would be useful to further identify genomic regions where introgression departs from neutral expectations and is potentially adaptive or maladaptive (Duranton et al, 2018;Edmands, 2007;Hedrick, 2013;Racimo et al, 2015;Sankararaman et al, 2014;Steinrücken, Spence, Kamm, Wieczorek, & Song, 2018; reviewed in Dannemann & Racimo, 2018).…”

“…The development of next‐generation sequencing (NGS) technologies has offered an unprecedented way to study admixture and introgression in many hybridizing taxa including both model and nonmodel species (Allendorf, Hohenlohe, & Luikart, ; Angeloni, Wagemaker, Vergeer, & Ouborg, ; Hoffmann et al., ; Kohn, Murphy, Ostrander, & Wayne, ; Narum, Buerkle, Davey, Miller, & Hohenlohe, ; Ouborg, Pertoldi, Loeschcke, Bijlsma, & Hedrick, ; Primmer, ; Steiner, Putnam, Hoeck, & Ryder, ). However, only few studies have used local ancestry blocks to characterize the genomic landscape of admixture in conservation genomics (but see Duranton et al., ; Galaverni et al., ; VonHoldt, Kays, Pollinger, & Wayne, ).…”

“…However, only few studies have used local ancestry blocks to characterize the genomic landscape of admixture in conservation genomics (but see Duranton et al, 2018;Galaverni et al, 2017;VonHoldt, Kays, Pollinger, & Wayne, 2016).…”

Unravelling the Scientific Debate on How to Address Wolf-Dog Hybridization in Europe

“…First, due to the technical problem of identification of hybrid individuals (VonHoldt et al, 2011;Lorenzini et al, 2014;Randi et al, 2014;Godinho et al, 2015), the scientific debate has lagged behind contemporary management. While hybridization is increasingly detectable through the advent of genetic markers, phenotypic cues of hybridization are less reliable and more difficult to interpret (e.g., Hindrikson et al, 2012;Galaverni et al, 2017). In addition, even though first generations hybrids (F1s), F2s, and first-and second-generation backcrosses (B1s, B2s) may be genetically conspicuous enough to be reliably identified (Lorenzini et al, 2014;Randi et al, 2014;Godinho et al, 2015), further generations of backcrosses into the parental wolf population are increasingly difficult to detect.…”

“…In addition, even though first generations hybrids (F1s), F2s, and first-and second-generation backcrosses (B1s, B2s) may be genetically conspicuous enough to be reliably identified (Lorenzini et al, 2014;Randi et al, 2014;Godinho et al, 2015), further generations of backcrosses into the parental wolf population are increasingly difficult to detect. Under these conditions, the risks of erroneously classifying an admixed individual as a wolf (i.e., Type II error) are substantial and higher than the complementary error (i.e., erroneously classifying a wolf as an admixed individual, or Type I error; Lorenzini et al, 2014;Randi et al, 2014;Galaverni et al, 2017).…”