Evolutionary history of the extinct wolf population from France in the context of global phylogeographic changes throughout the Holocene

Abstract

Phylogeographic patterns in large mammals result from natural environmental factors and anthropogenic effects, which in some cases include domestication. The grey wolf was once widely distributed across the Holarctic, but experienced phylogeographic shifts and demographic declines during the Holocene. In the 19th-20th centuries, the species became extirpated from large parts of Europe due to direct extermination and habitat loss. We reconstructed the evolutionary history of the extinct Western European wolves based on the mitogenomic composition of 78 samples from France (Neolithic-20th century) in the context of other populations of wolves and dogs worldwide. We found a close genetic similarity of French wolves from ancient, medieval and recent populations, which suggests the long-term continuity of maternal lineages. MtDNA haplotypes of the French wolves showed large diversity and fell into two main haplogroups of modern Holarctic wolves. Our worldwide phylogeographic

Assessment of genetic diversity, population structure and wolf-dog hybridisation in the Eastern Romanian Carpathian wolf population

“…This finding documents the low grade of previous genetic knowledge on wolves in Romania. Moreover, our results indicate that haplotype ROM1 was shared between different regions across Europe before human-induced local extinctions and the strong loss of genetic diversity in Western Europe occurred during the last 200 years, which has already been suggested for most other European wolf haplotypes 31 , 38 . Future studies covering longer mtDNA sequences or ideally complete mitogenomes from all haplogroup 2 wolf populations may help to better understand the evolutionary dynamics and phylogeographic structure of European wolves.…”

“…However, 30 and 29 showed that this wolf haplotype belongs to haplogroup 2 described in 28 . The 361 bp fragment of haplotype ROM1 fully matched to a Sicilian haplotype (ID: MH891616 29 ) and a French haplotype (ID: OM743388 31 ) but differed by only one substitution from a French (ID: OM743385 31 ), a Bulgarian (ID: KU696388), a Polish (ID: KF661045) and the wolf haplotype H6 (this study and 28 ). This finding documents the low grade of previous genetic knowledge on wolves in Romania.…”

“…2 ). Interestingly, haplotype ROM1 matched with sequences (361 bp; ID: MH891616 29 and 356 bp; ID: MK129178 & MK129179 30 ) obtained from museum specimens referable to the extinct wolf population of Sicily and with a sequence obtained from an individual discovered in Southern France in 1954 CE (361 bp; ID: OM743388 31 ). Another haplotype, H6 28 , was found in eight wolf samples (6%) collected in the surrounding area but not within the four core study areas.…”

Large variance in inbreeding within the Iberian wolf population

“…Therefore, large wolf populations, such as the Dinaric-Balkan, have been considered a valuable source of genetic diversity for neighboring populations in Europe ( Hindrikson et al 2017 ). Since the sizes of the wolf populations in the Iberian and Italian Peninsulas were much smaller, population declines and long-term geographical isolation ( Silva et al 2020 ) may have caused more inbreeding in these populations than in north-eastern European wolves ( Lucchini et al 2004 ; Fabbri et al 2007 ; Sastre et al 2011 ; Fan et al 2016 ; Hindrikson et al 2017 ), although recent research about the extinct French wolf population suggested that this isolation was either incomplete or more recent than previously estimated ( Doan et al 2023 ). While recent population expansions have resulted in gene flow between the Italian and other central and eastern European wolf populations increasing the genetic diversity of these expanding populations, the Iberian population has thus far remained genetically isolated ( Hindrikson et al 2017 ).…”

“…Thanks to the advent of next-generation sequencing technologies and the ongoing development of ancient DNA methodology, it has been possible to assess changes in genetic and genomic diversity through time using museum specimens ( Dufresnes et al 2018 ; Taron et al 2021 ; Doan et al 2023 ; Salado et al 2023 ) by directly comparing patterns of diversity in historical populations with those of extant populations. It is known that genetic variability has been lost with historically extirpated wolf populations ( Leonard et al 2005 ; Taron et al 2021 ; Doan et al 2023 ), and genetic diversity could potentially continue to be lost in demographically stable wolf populations, such as that on the Iberian Peninsula, as has been shown for mitochondrial DNA (mtDNA; Salado et al 2023 ). However, the effective population size of mtDNA is smaller than that of nuclear loci, making it more susceptible to losses of diversity.…”