Fitness costs associated with ancestry to isolated populations of an endangered species

Habitat fragmentation from urban development leaves species vulnerable to inbreeding depression and genomic erosion. Restoring gene flow can reduce inbreeding and preserve genetic diversity, but a common concern is that genomic incompatibilities may lead to outbreeding depression. The introduction of deleterious genetic load is less commonly considered. The endangered Pacific pocket mouse ( Perognathus longimembris pacificus ) persists in three isolated populations in southern California. Mitochondrial and microsatellite data indicated that effective population sizes were extremely small (N e < 50), and continued declines prompted a conservation breeding program founded by individuals from each population. We tracked genetic diversity and individual fitness (measured by reproductive success) in a captive setting over six generations of admixture. Although we observed an increase in fitness in the F1 and F2 generations relative to the founding populations, inbreeding depression alone did not explain the fitness patterns, and outbreeding depression was difficult to rule out as reproductive success waned after F2. However, reproductive success was consistently higher in admixed individuals than founders from Dana Point, the smallest population with the lowest heterozygosity. Across generations, we saw a strong negative correlation between individual reproductive success and ancestry to Dana Point, leading to a rapid decrease of Dana Point alleles. Although the genomic underpinnings remain to be determined, reduced fitness associated with Dana Point ancestry is consistent with high deleterious genetic load in this population, and thus any facilitated migration should be unidirectional. Our findings highlight that, even in the absence of outbreeding depression, there may be a cost to restoration of gene flow if populations harbor high genetic load.