Genomic erosion in a demographically recovered bird species during conservation rescue

Abstract

The pink pigeon (Nesoenas mayeri) is an endemic species of Mauritius that has made a remarkable recovery after a severe population bottleneck in the 1970s to early 1990s. Prior to this bottleneck, an ex situ population was established from which captive-bred individuals were released into free-living subpopulations to increase population size and genetic variation. This conservation rescue led to rapid population recovery to 400-480 individuals, and the species was twice downlisted on the International Union for the Conservation of Nature (IUCN) Red List. We analyzed the impacts of the bottleneck and genetic rescue on neutral genetic variation during and after population recovery (1993-2008) with restriction site-associated sequencing, microsatellite analyses, and quantitative genetic analysis of studbook data of 1112 birds from zoos in Europe and the United States. We used computer simulations to study the predicted changes in genetic variation and population viability from the past into the future. Genetic variation declined rapidly, despite the population rebound, and the effective population size was approximately an order of magnitude smaller than census size. The species carried a high genetic load of circa 15 lethal equivalents for longevity. Our computer simulations predicted continued inbreeding will likely result in increased expression of deleterious mutations (i.e., a high realized load) and severe inbreeding depression. Without continued conservation actions, it is likely that the pink pigeon will go extinct in the wild within 100 years. Conservation rescue of the pink pigeon has been instrumental in the recovery of the free-living population. However, further genetic rescue with captive-bred birds from zoos is required to recover lost variation, reduce expression of harmful deleterious variation, and prevent extinction. The use of genomics and modeling data can inform IUCN assessments of the viability and extinction risk of species, and it helps in assessments of the conservation dependency of populations.

Keywords: Nesoenas mayeri; captive breeding; diversidad genética; genetic diversity; genetic management; genetic rescue; manejo genético; reproducción en cautiverio; rescate genético.

FIGURE 1

(a) Location of 5 subpopulations of pink pigeon (pictured) on Mauritius in 2008 (squares) (black polygon, Black River Gorges National Park; shading, forest; inset, adult bird), (b) population size, derived from field monitoring, of the free‐living Mauritius pink pigeon population over time (bottleneck and recovery), and (c) number of captive‐bred pink pigeons released in the Ile aux Aigrettes (IAA) population and in other free‐living populations during the species recovery program

FIGURE 2

Relationship between genetic divergence (pairwise F _ST) and (a) geographic distance between populations (regression: F _1,8 = 42.14, p < 0.001, R ² = 84.0%) and (b) genetic divergence (mean and SE) between the Ile aux Aigrettes (IAA) population and Bel Ombre, Combo, Pigeon Wood, and Plaine Lievre populations of pink pigeon over time; (c) observed heterozygosity (H _o) between the parent (H _o = 0.314) and offspring (H _o = 0.294) generations over time, based on RAD‐seq data, in the IAA population of pink pigeons; (d) heterozygosity in birds hatched from 1994 to 2008, based on RAD‐seq data, in the IAA population (regression: F _1,73 = 21.41, p < 0.001, R ² = 22.7%); (e) temporal change in inbreeding coefficient (F _IS) (mean and SE) (i.e., observed heterozygosity) for pink pigeons from the (IAA) population; and (f) neighbor‐net network of 133 pink pigeon samples (tips colored by population)

FIGURE 3

Runs of homozygosity (ROH) in the pink pigeon genome across chromosome scaffolds 1–27. Highly inbred individuals (F _ROH > 0.25, i.e., a level of inbreeding higher than after a single full‐sib mating) show long ROH, occasionally spanning the length of nearly half a chromosome. Numbers and letters above F _ROH refer to pink pigeon identification number in the studbook

FIGURE 4

Longevity of a pink pigeon (in days) relative to its inbreeding coefficient (F _{1, 1111} = 33.550, p < 0.0001). The mean number of lethal equivalents (LEs) equals 15.13 (5–95% CI, 10.00–20.25)

FIGURE 5

Predicted mean (SE) census population size (N) over 1000 iterations of free‐living pink pigeons modeled in Vortex (Lacy & Pollak, 2014) for each year of the model and 3 management scenarios (black line, scenario 1 no supplementation; dark gray line, scenario 2 demographic rescue [i.e., populaiton supplementation with hypothetical gene pool similar to the free‐living metapopulation]; light gray line, scenario 3 genetic rescue [i.e., supplementation with zoo‐bred captive birds]). The supplementation regimes for scenarios 2 and 3 are identical, that is, 10 birds for each subpopulaiton every 5 years

FIGURE 6

Relationship between the genetic load (expressed in lethal equivalents [LEs]), inbreeding coefficient (F), and the probability of extinction after 100 years for the free‐living population of pink pigeon modeled in Vortex (Lacy & Pollak, 2014). The population increased in mean (5–95% CI) inbreeding coefficient between 1995 (white bars) and 2020 (gray bars), which also increased its extinction probability

FIGURE 7

(a) Proportion of replicates that went extinct by year 2120. (b‐c) Mean (dots) and standard deviation (bars) of (b) nucleotide diversity and (c) fitness effect of the genetic load (i.e., realized load; Bertorelle et al., 2022) across replicates in genomic simulations with SLiM (Haller & Messer, 2019) of the free‐living pink pigeon population. Metrics include the effect of extinct replicates (a) by taking their last recorded values into account for the mean and standard deviation calculations in subsequent steps. The simulated population experienced a severe bottleneck and was subjected to different management scenarios: no intervention (yellow), demographic rescue (blue), genetic rescue (green) and demographic + genetic rescue (pink) (see Appendix S4 for details).