The population bottleneck of the Iberian wolf impacted genetic diversity but not admixture with domestic dogs: A temporal genomic approach

Abstract

After decades of intense persecution, the Iberian wolf subspecies faced a severe bottleneck in the 1970s that considerably reduced its range and population size, nearly leading to its extinction in central and southern Iberian Peninsula. Such population decline could have impacted the genetic diversity of Iberian wolves through different processes, namely genetic drift and dynamics of hybridization with domestic dogs. By contrasting the genomes of 68 contemporary with 54 historical samples spanning the periods before and immediately after the 1970s bottleneck, we found evidence of its impact on genetic diversity and dynamics of wolf–dog hybridization. Our genome‐wide assessment revealed that wolves and dogs form two well‐differentiated genetic groups in Iberia and that hybridization rates did not increase during the bottleneck. However, an increased number of hybrid individuals was found over time during the population re‐expansion, particularly at the edge of the wolf range. We estimated a low percentage of dog ancestry (~1.4%) in historical samples, suggesting that dog introgression was not a key driver for wolf extinction in central and southern Iberia. Our findings also unveil a significant decline in genetic diversity in contemporary samples, with the highest proportion of homozygous segments in the genome being recently inherited. Overall, our study provides unprecedented insight into the impact of a sharp decline on the Iberian wolf genome and refines our understanding of the ecological and evolutionary drivers of wolf–dog hybridization in the wild.

Imputation of ancient canid genomes reveals inbreeding history over the past 10,000 years

“…This, in combination with intensive human driven selective breeding to develop and maintain specific breed traits in more recent periods, have shaped dog genetic diversity through time. Previous studies on wolves have also found past and recent demographic events, including bottlenecks and within and between-species admixture ( Pilot et al 2014 , 2019 , 2021 ; Fan et al 2016 ; Loog et al 2020 ; Bergström et al 2022 ; Lobo et al 2023 ). Even though wolves have not undergone the same human selective breeding as dogs, they have been subjected to a high degree of human induced pressures via habitat loss and systematic persecution ( Wayne et al 1992 ; Fredrickson et al 2007 ; Sastre et al 2011 ; Pilot et al 2014 ; Kuijper et al 2016 ).…”

Large variance in inbreeding within the Iberian wolf population

“…The population increased after partial legal protection in the 1970s ( Valverde 1971 ; Grande del Brío 1984 ; Blanco et al 1992 ) and has been stable for the last 30 years, at around 350 packs or about 2,000 to 2,500 individuals ( MITECO 2016 ; Torres and Fonseca 2016 ). Despite this demographically healthy population condition, population genetic estimates using a small panel of microsatellites suggested an effective population size of about just 50 individuals ( Sastre et al 2011 ), and previous analyses showed a loss of mtDNA diversity during population expansion ( Salado et al 2023 ), and a reduction in genome-wide diversity due to the 1970s population bottleneck ( Lobo et al 2023 ).…”

“…The high levels of inbreeding that we observe suggest that inbreeding depression could locally be an issue in modern Iberian wolves if the fragmentation continues in the population. Inbreeding depression has not been documented or suggested in Iberian wolves ( Lobo et al 2023 ), but it is possible that this may simply be due to a lack of data. Relevant data that could be collected include morphological data, behavioral data, and reproductive success since these traits have been shown to be impacted by inbreeding depression in other wolf populations.…”