Genetic load and adaptive potential of a recovered avian species that narrowly avoided extinction

Abstract

High genetic diversity is often a good predictor of long-term population viability, yet some species persevere despite having low genetic diversity. Here we study the genomic erosion of the Seychelles paradise flycatcher (Terpsiphone corvina), a species that narrowly avoided extinction after having declined to 28 individuals in the 1960s. The species recovered unassisted to over 250 individuals in the 1990s and was downlisted from Critically Endangered to Vulnerable in the IUCN Red List in 2020. By comparing historical, pre-bottleneck (130+ years old) and modern genomes, we uncovered a 10-fold loss of genetic diversity. The genome shows signs of historical inbreeding during the bottleneck in the 1960s, but low levels of recent inbreeding after the demographic recovery. We show that the proportion of severely deleterious mutations has reduced in modern individuals, but mildly deleterious mutations have remained unchanged. Computer simulations suggest that the Seychelles paradise flycatcher avoided extinction and recovered due to its long-term small Ne. This reduced the masked load and made the species more resilient to inbreeding. However, we also show that the chronically small Ne and the severe bottleneck resulted in very low genetic diversity in the modern population. Our simulations show this is likely to reduce the species' adaptive potential when faced with environmental change, thereby compromising its long-term population viability. In light of rapid global rates of population decline, our work highlights the importance of considering genomic erosion and computer modelling in conservation assessments.

Multinational evaluation of genetic diversity indicators for the Kunming‐Montreal Global Biodiversity Framework

“…In other words, our proxy‐based assessment, which was completed in less than one year, obtained more estimates of Ne than a decade of hundreds of DNA‐based studies. We acknowledge that Ne quantified using genetic data may, in some cases, be more accurate than that estimated using proxy data, and that genetic data is crucial for assessing the effect of genomic erosion (e.g., Femerling et al., 2023). However, using proxies, we have shown that estimates of Ne can be obtained in a rapid and efficient manner, which can enable the tracking and reporting of genetic information on large scales in all countries.…”

Can genetic rescue help save Arabia's last big cat?

“…Third, we complemented our Vortex analyses with computer simulations in SLiM (Haller & Messer, 2019). Like Vortex, this forward‐in‐time, individual‐based‐model enabled us to simulate the impacts of conservation action on population viability many generations into the future (Bertorelle et al., 2022; Femerling et al., 2023; Jackson et al., 2022). Using SLiM, we were also able to simulate the ancestral population size, rates of decline, and contemporary population sizes based on the known demographic history of the Arabian leopard (Al Hikmani et al., 2023).…”

Four centuries of commercial whaling eroded 11,000 years of population stability in bowhead whales

“…This is expected, as genetic diversity loss has a time-lag relative to demographic decline, particularly in long-lived species 47 . Genetic diversity loss in collapsed populations (e.g., Svalbard) is expected to continue even if there is demographic recovery 48,49 , because small populations continue to pay a ‘genetic drift debt’ 50 . This sustained genomic erosion, especially in the ‘East Greenland Svalbard Barents Sea’ stock, brings into question the long-term resilience of the population.…”