Translocations spur population growth but fail to prevent genetic erosion in imperiled Florida Scrub-Jays

Land and natural resource use that supports human society can restrict populations to degraded and fragmented habitat, which catalyzes extinction and biodiversity loss through the interplay of small population size and genetic decay. Translocating individuals is a powerful approach for overcoming direct threats from human development and reconnecting isolated populations, although this strategy is not without risks. Consequently, there is a pressing need to understand the demographic and genetic outcomes of translocations in order to determine their conservation efficacy. We achieved this by leveraging the rare opportunity of having a nearly complete population pedigree from two decades of intensive demographic monitoring coupled with temporal genomic sequencing and simulations to evaluate how translocating Federally Threatened Florida Scrub-Jays from five subpopulations into an area of restored habitat with a small recipient population influenced their recovery. Translocations led to an expanding core population that rapidly grew 10-fold in size, primarily fueled by a small subset of highly successful translocated individuals, with one breeding pair responsible for ~24% of the population’s expected genetic ancestry for 15 years on average. This high reproductive skew led to increased inbreeding and genetic erosion, despite the population expansion and simulation results showing that the variance of ancestral genetic contributions was likely reduced by translocations. These mixed conservation outcomes stress the importance of genomic and demographic monitoring, as well as the potential need for genetic rescue to offset the consequences of reproductive skew in isolated populations following translocations, regardless of demographic recovery, in order to achieve long-term species viability.

Methods
Every year we monitored and collected demographic information for Florida Scrub-Jays (Aphelocoma coerulescens, hereafter FSJ) in the M4 Core Region (abbreviated "CR", comprised of the Duette Preserve, Coker Tract, Mosaic Wellfield), Florida, United States, prior to and following translocations of FSJs from Sites 1, 12, 13, 18, and Texaco into the CR. We used this demographic monitoring data to construct a nearly complete CR population pedigree, which we used to estimate the expected genetic contributions of individuals to the CR population over time. We also extracted DNA from blood collected for genetic analysis, which we used to sequence whole genomes of 87 FSJs, including resident individuals inhabiting the CR prior to translocations and individuals born into this population 18 years after the first translocations, as well as translocated individuals and individuals from peripheral M4 subpopulations (Duette Headwaters, West Balm, Sun City, Golden Aster Scrub, Brigman) in order to determine the impact of translocations on CR population inbreeding and genetic diversity. Additionally, we simulated multiple demographic scenarios to estimate expected levels of reproductive variance and skew from demographic stochasticity.