Patterns of reproduction and autozygosity distinguish the breeding from non-breeding gray wolves of Yellowstone National Park

Bridgett M vonHoldt; Alexandra L DeCandia; Kira A Cassidy; Erin E Stahler; Janet S Sinsheimer; Douglas W Smith; Daniel R Stahler

doi:10.1093/jhered/esad062

Patterns of reproduction and autozygosity distinguish the breeding from non-breeding gray wolves of Yellowstone National Park

J Hered. 2023 Oct 4:esad062. doi: 10.1093/jhered/esad062. Online ahead of print.

Authors

Bridgett M vonHoldt¹, Alexandra L DeCandia^{2

3}, Kira A Cassidy⁴, Erin E Stahler⁴, Janet S Sinsheimer⁵, Douglas W Smith⁴, Daniel R Stahler⁴

Affiliations

¹ Department of Ecology and Evolutionary Biology, 106A Guyot Hall, Princeton University, Princeton NJ.
² Department of Biology, Georgetown University, Washington DC.
³ Smithsonian Conservation Biology Institute, National Zoological Park, Washington, DC.
⁴ Yellowstone Wolf Project, PO Box 168, Yellowstone National Park, WY.
⁵ Department of Biostatistics, Fielding School of Public Health and Departments of Human Genetics and Computational Medicine, David Geffen School of Medicine, UCLA, Los Angeles, CA.

PMID: 37793153
DOI: 10.1093/jhered/esad062

Abstract

For species of management concern, accurate estimates of inbreeding and associated consequences on reproduction are crucial for predicting their future viability. However, few studies have partitioned this aspect of genetic viability with respect to reproduction in a group-living social mammal. We investigated the contributions of foundation stock lineages, putative fitness consequences of inbreeding, and genetic diversity of the breeding versus non-reproductive segment of the Yellowstone National Park gray wolf population. Our dataset spans 25 years and seven generations since reintroduction, encompassing 152 nuclear families and 329 litters. We found over 87% of the pedigree foundation genomes persisted and report influxes of allelic diversity from two translocated wolves from a divergent source in Montana. As expected for group-living species, mean kinship significantly increased over time but with minimal loss of observed heterozygosity. Strikingly, the reproductive portion of the population carried a significantly lower genome-wide inbreeding coefficients, autozygosity, and more rapid decay for linkage disequilibrium relative to the non-breeding population. Breeding wolves had significantly longer lifespans and lower inbreeding coefficients than non-breeding wolves. Our model revealed that the number of litters was negatively significantly associated with heterozygosity (R=-0.11). Our findings highlight genetic contributions to fitness, and the importance of the reproductively active individuals in a population to counteract loss of genetic variation in a wild, free-ranging social carnivore. It is crucial for managers to mitigate factors that significantly reduce effective population size and genetic connectivity, which supports the dispersion of genetic variation that aids in rapid evolutionary responses to environmental challenges.

Keywords: autozygosity; genomic variation; pedigree; reproductive status.