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)(1994)(1995)(1996)(1997)(1998)(1999)(2000)(2001)(2002)(2003)(2004)(2005)(2006)(2007)(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.

Genomic erosion in the assessment of species extinction risk and recovery potential

“…However, the genetic load, maladaptation, and genetic introgression also pose a considerable threat to many species 8,58,59 . Genomics-informed conservation can make a quantitative assessment of the impacts of recent changes in evolutionary forces on individual fitness and population viability.…”

“…The long-term success of such programs hinges critically on our understanding about genomic erosion and the intrinsic links between genetic variation, adaptive evolutionary potential, the genetic load, and the ecological history and present biology of the species. The recent debate about the optimal size of the donor population in genetic rescue is a likely foreshadow of many future discussions 8,97,98,99,100,101,102,103,104 .…”

“…These plans should be based on the best-available information, and this should include data about the genomic erosion inflicted on the population during its recent decline. Even after a population has recovered demographically, genomic erosion may continue due to a “drift debt” 7,8 , changes to the composition of its genetic load 9 and reduced adaptive potential 10 . In the long-term, genomic erosion reduces population viability, and thus should be also included in species recovery plans 11 .…”

“…Genomic erosion is manifested as: (1) a loss of genetic diversity, (2) an elevated realised load (that is, the component of genetic load whose fitness effects is expressed 9 , and which is caused by an increased number of homozygous loci with recessive deleterious alleles), (3) a mismatch between genetic adaptations and the prevailing environmental conditions (i.e., maladaptation), and (4) genetic introgression due to hybridisation. All four aspects of genomic erosion can reduce individual fitness and undermine viability of populations, both in the short-and long-term 8,29,37,38,39,40 . Although genomic erosion is rarely the primary cause for species extinction, it is tightly coupled to other (external) threats.…”

“…Accordingly, genomic erosion often plays a critical role during the later stages of population decline, when the fate of a population or species is ultimately decided 44,45 . Furthermore, the impacts of genomic erosion can be felt long after the primary threats have been abated i.e., "drift debt" 7,8,46 .…”