High kinship and runs of homozygosity characterize walleye Sander vitreus metapopulation diversity in Lake Champlain, USA.

Abstract

Understanding the roles of philopatry and geography in determining genetic population structure is an important part of managing species characterized by metapopulations. In this study, we examined population structure, kinship, and runs of homozygosity in walleye (Sander vitreus) from Lake Champlain, a large, fragmented lake with four main spawning tributaries that form a metapopulation. Using microsatellite genotyping at 12 loci, we investigated population genetic structure among the four tributaries to examine how spawning site fidelity influenced pairwise genetic distances. Using a high-density Rapture dataset containing thousands of reference-aligned SNP genotypes, we estimated evidence of inbreeding based on runs of homozygosity (ROH) in Lake Champlain and compared findings to four other large walleye populations in North America. The Lamoille and Poultney Rivers were genetically distinct from the Missisquoi and Winooski Rivers, despite evidence of 10% straying among rivers. Within-site kinship and the number of runs of homozygosity (ROH) in the Lamoille and Poultney Rivers were elevated compared to Missisquoi and Winooski Rivers, suggesting ongoing or recent inbreeding at these locations. Comparisons with other large-lake walleye populations revealed that the elevated number of ROHs in Lake Champlain was specific to the Lamoille and Poultney Rivers. We suggest that this inbreeding may be driven by demographic bottlenecks and small effective population sizes (<50 based on microsatellite data) that were potentially facilitated by hatchery practices. Our findings indicate that when combined with other factors, philopatry can have powerful impacts on fine-scale population structure and genomic diversity. We emphasize that metapopulations composed of philopatric sub-populations may be more vulnerable to localized inbreeding than systems with more random dispersal. Our results demonstrate how genetic data can inform conservation strategies, particularly in the face of habitat fragmentation and declining population sizes.