Genetic Load and Adaptive Potential of a Recovered Avian Species that Narrowly Avoided Extinction.

High genetic diversity is 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 International Union for the Conservation of Nature Red List in 2020. By comparing historical, prebottleneck (130+ years old) and modern genomes, we uncovered a 10-fold loss of genetic diversity. Highly deleterious mutations were partly purged during the bottleneck, but mildly deleterious mutations accumulated. The genome shows signs of historical inbreeding during the bottleneck in the 1960s, but low levels of recent inbreeding after demographic recovery. Computer simulations suggest that the species long-term small Ne reduced the masked genetic load and made the species more resilient to inbreeding and extinction. However, the reduction in genetic diversity due to the chronically small Ne and the severe bottleneck is likely to have reduced the species adaptive potential to face environmental change, which together with a higher load, compromises its long-term population viability. Thus, small ancestral Ne offers short-term bottleneck resilience but hampers long-term adaptability to environmental shifts. In light of rapid global rates of population decline, our work shows that species can continue to suffer the effect of their decline even after recovery, highlighting the importance of considering genomic erosion and computer modeling in conservation assessments.

Comparison of historical bottleneck effects and genetic consequences of re-introduction in a critically endangered island passerine.

Re-introduction is an important tool for recovering endangered species; however, the magnitude of genetic consequences for re-introduced populations remains largely unknown, in particular the relative impacts of historical population bottlenecks compared to those induced by conservation management. We characterize 14 microsatellite loci developed for the Seychelles paradise flycatcher and use them to quantify temporal and spatial measures of genetic variation across a 134-year time frame encompassing a historical bottleneck that reduced the species to ~28 individuals in the 1960s, through the initial stages of recovery and across a second contemporary conservation-introduction-induced bottleneck. We then evaluate the relative impacts of the two bottlenecks, and finally apply our findings to inform broader re-introduction strategy. We find a temporal trend of significant decrease in standard measures of genetic diversity across the historical bottleneck, but only a nonsignificant downward trend in number of alleles across the contemporary bottleneck. However, accounting for the different timescales of the two bottlenecks (~40 historical generations versus <1 contemporary generation), the loss of genetic diversity per generation is greater across the contemporary bottleneck. Historically, the flycatcher population was genetically structured; however, extinction on four of five islands has resulted in a homogeneous contemporary population. We conclude that severe historical bottlenecks can leave a large footprint in terms of sheer quantity of genetic diversity lost. However, severely depleted genetic diversity does not render a species immune to further genetic erosion upon re-introduction. In some cases, the loss of genetic diversity per generation can, initially at least, be greater across re-introduction-induced bottlenecks.

Molecular phylogeny of the Indian Ocean Terpsiphone paradise flycatchers: undetected evolutionary diversity revealed amongst island populations.

We construct a molecular phylogeny of Terpsiphone flycatchers of the Indian Ocean and use this to investigate their evolutionary relationships. A total of 4.4 kb of mitochondrial (cyt-b, ND3, ND2, control region) and nuclear (G3PDH, MC1R) sequence data were obtained from all species, sub-species and island populations of the region. Colonisation of the western Indian Ocean has been within the last two million years and greatly postdates the formation of the older islands of the region. A minimum of two independent continent-island colonisation events must have taken place in order to explain the current distribution and phylogenetic placement of Terpsiphone in this region. While five well-diverged Indian Ocean clades are detected, the relationship between them is unclear. Short intermodal branches are indicative of rapid range expansion across the region, masking exact routes and chronology of colonisation. The Indian Ocean Terpsiphone taxa fall into five well supported clades, two of which (the Seychelles paradise flycatcher and the Mascarene paradise flycatcher) correspond with currently recognised species, whilst a further three (within the Madagascar paradise flycatcher) are not entirely predicted by taxonomy, and are neither consistent with distance-based nor island age-based models of colonisation. We identify the four non-Mascarene clades as Evolutionarily Significant Units (ESUs), while the Mascarene paradise flycatcher contains two ESUs corresponding to the Mauritius and Réunion subspecies. All six ESUs are sufficiently diverged to be worthy of management as if they were separate species. This phylogenetic reconstruction highlights the importance of sub-specific molecular phylogenetic reconstructions in complex island archipelago settings in clarifying phylogenetic history and ESUs that may otherwise be overlooked and inadvertently lost. Our phylogenetic reconstruction has identified hidden pockets of evolutionary distinctiveness, which provide a valuable platform upon which to re-evaluate investment of conservation resources within the Terpsiphone flycatchers of the Indian Ocean.