On the path to extinction: Inbreeding and admixture in a declining grey wolf population

Abstract

Allee effects reduce the viability of small populations in many different ways, which act synergistically to lead populations towards extinction vortexes. The Sierra Morena wolf population, isolated in the south of the Iberian Peninsula and composed of just one or few packs for decades, represents a good example of how diverse threats act additively in very small populations. We sequenced the genome of one of the last wolves identified (and road-killed) in Sierra Morena and that of another wolf in the Iberian Wolf Captive Breeding Program and compared them with other wolf and dog genomes from around the world (including two previously published genome sequences from northern Iberian wolves). The results showed relatively low overall genetic diversity in Iberian wolves, but diverse population histories including past introgression of dog genes. The Sierra Morena wolf had an extraordinarily high level of inbreeding and long runs of homozygosity, resulting from the long isolation. In addition, about one-third of the genome was of dog origin. Despite the introgression of dog genes, heterozygosity remained low because of continued inbreeding after several hybridization events. The results thus illustrate the case of a small and isolated wolf population where the low population density may have favoured hybridization and introgression of dog alleles, but continued inbreeding may have resulted in large chromosomal fragments of wolf origin completely disappearing from the population, and being replaced by chromosomal fragments of dog origin. The latest population surveys suggest that this population may have gone extinct.

A standardized approach to empirically define reliable assignment thresholds and appropriate management categories in deeply introgressed populations

“…In particular, though some studies documented cases of beneficial introgression of domestic mutations in wild populations of North American wolves 27 and Alpine ibexes 28 , introgressive hybridization with www.nature.com/scientificreports www.nature.com/scientificreports/ domestic forms is globally recognized as a significant risk factor for the conservation of several wild taxa 14,24,28,[60][61][62] . However, though being essential to understand the real impact of the phenomenon and to design sound conservation strategies 16,23 , the identification of hybrids and their backcrosses remains far from trivial even in the genomic era [3][4][5]10,13 . In the common practice, the domestic ancestry of biological samples is usually assessed typing their DNA at presumably neutral molecular markers and probabilistically assigning the obtained genotypes to reference parental populations by Bayesian statistics 57,63 .…”

“…We then tested this approach on an interesting example of AH 16,26 , taking place between the wolf (Canis lupus) and its domestic counterpart, the dog (C. l. familiaris). In particular, we investigated samples from the Italian wolf population (C. l. italicus), which experienced a demographic scenario characterized by protracted isolation south of the Alps and recurrent bottlenecks that made Italian wolves sharply genetically differentiated from any other wolf population 4,24,26,[44][45][46][47] . Although the Italian wolf population is now recovering thanks to legal protection and the increased availability of suitable habitats and prey 48 , it is still threatened by accidental or illegal killings 49,50 , but also by anthropogenic hybridization, as repeatedly documented by genetic and genomic data showing gene flow from the domestic to the wild subspecies [24][25][26]31,33,37,51,52 .…”

Human disturbance as a possible cause of genetic introgression from exotic into native Mauremys turtles

“…Theoretically, after the F1 hybrids backcross with M. reevesii for two generations, the genetic composition of M. sinensis would decrease to 0.125; generations beyond the third generation would be indistinguishable from pure M. reevesii by our microsatellite markers. Therefore, the severity of genetic introgression might be greater than the level we have detected if backcrossing continues: (1) the hybrid rate may be underestimated when the decision is based solely on morphology; (2) even with the inclusion of microsatellite data, the magnitude of genetic introgression may still be underestimated, for example, due to limited genomic representation of the utilized markers (Gómez‐Sánchez et al ., ).…”

Lethal management may hinder population recovery in Iberian wolves

“…Among other key components of population biology, the effective population size (Ne), the number of individuals that contribute to the reproduction every generation (Frankham 1995;Palstra and Fraser 2012), is particularly relevant to evaluate the viability of populations and the outcome of management policies (Shaffer 1981;Laikre et al 2013;Frankham et al 2014). The effective population size of Iberian wolves has been estimated, and at Ne < 60 it is much lower than any estimate of census population size, indicating that the population went through severe bottlenecks not too long ago (Sastre et al 2011;Pilot et al 2014;Gómez-Sánchez et al 2018).…”

“…The recovery and favorable conservation status of wolf populations requires a proper functioning of dispersal. In the Iberian context, dispersal could alleviate the genetic consequences of past bottlenecks (Vilà et al 2003;Sastre et al 2011;Pilot et al 2014;Gómez-Sánchez et al 2018), providing genetic and demographic rescue to the endangered wolves in Portugal (Torres and Fonseca 2016), and reaching Spanish areas where they were recently extirpated or their presence is sporadic (Echegaray and Vilà 2010;López-Bao et al 2015;Gómez-Sánchez et al 2018). Elsewhere, dispersal is helping wolf recovery after historical decline and isolation (Fabbri et al 2007).…”