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Genomic trajectories of a near-extinction event in the Chatham Island black robin

von Seth, Johanna ; van der Valk, Tom ; Lord, Edana ; Sigeman, Hanna LU ; Olsen, Remi André ; Knapp, Michael ; Kardailsky, Olga ; Robertson, Fiona ; Hale, Marie and Houston, Dave , et al. (2022) In BMC Genomics 23(1).
Abstract

Background: Understanding the micro-­evolutionary response of populations to demographic declines is a major goal in evolutionary and conservation biology. In small populations, genetic drift can lead to an accumulation of deleterious mutations, which will increase the risk of extinction. However, demographic recovery can still occur after extreme declines, suggesting that natural selection may purge deleterious mutations, even in extremely small populations. The Chatham Island black robin (Petroica traversi) is arguably the most inbred bird species in the world. It avoided imminent extinction in the early 1980s and after a remarkable recovery from a single pair, a second population was established and the two extant populations have... (More)

Background: Understanding the micro-­evolutionary response of populations to demographic declines is a major goal in evolutionary and conservation biology. In small populations, genetic drift can lead to an accumulation of deleterious mutations, which will increase the risk of extinction. However, demographic recovery can still occur after extreme declines, suggesting that natural selection may purge deleterious mutations, even in extremely small populations. The Chatham Island black robin (Petroica traversi) is arguably the most inbred bird species in the world. It avoided imminent extinction in the early 1980s and after a remarkable recovery from a single pair, a second population was established and the two extant populations have evolved in complete isolation since then. Here, we analysed 52 modern and historical genomes to examine the genomic consequences of this extreme bottleneck and the subsequent translocation. Results: We found evidence for two-fold decline in heterozygosity and three- to four-fold increase in inbreeding in modern genomes. Moreover, there was partial support for temporal reduction in total load for detrimental variation. In contrast, compared to historical genomes, modern genomes showed a significantly higher realised load, reflecting the temporal increase in inbreeding. Furthermore, the translocation induced only small changes in the frequency of deleterious alleles, with the majority of detrimental variation being shared between the two populations. Conclusion: Our results highlight the dynamics of mutational load in a species that recovered from the brink of extinction, and show rather limited temporal changes in mutational load. We hypothesise that ancestral purging may have been facilitated by population fragmentation and isolation on several islands for thousands of generations and may have already reduced much of the highly deleterious load well before human arrival and introduction of pests to the archipelago. The majority of fixed deleterious variation was shared between the modern populations, but translocation of individuals with low mutational load could possibly mitigate further fixation of high-frequency deleterious variation.

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organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Bottleneck, Genomics, Inbreeding, Mutational load, Near-extinction, Translocation
in
BMC Genomics
volume
23
issue
1
article number
747
publisher
BioMed Central (BMC)
external identifiers
  • scopus:85141614528
  • pmid:36357860
ISSN
1471-2164
DOI
10.1186/s12864-022-08963-1
language
English
LU publication?
yes
id
62ce4b34-e1c7-4da9-aa7e-da5ba8b48247
date added to LUP
2022-12-05 11:48:59
date last changed
2024-04-18 15:46:18
@article{62ce4b34-e1c7-4da9-aa7e-da5ba8b48247,
  abstract     = {{<p>Background: Understanding the micro-­evolutionary response of populations to demographic declines is a major goal in evolutionary and conservation biology. In small populations, genetic drift can lead to an accumulation of deleterious mutations, which will increase the risk of extinction. However, demographic recovery can still occur after extreme declines, suggesting that natural selection may purge deleterious mutations, even in extremely small populations. The Chatham Island black robin (Petroica traversi) is arguably the most inbred bird species in the world. It avoided imminent extinction in the early 1980s and after a remarkable recovery from a single pair, a second population was established and the two extant populations have evolved in complete isolation since then. Here, we analysed 52 modern and historical genomes to examine the genomic consequences of this extreme bottleneck and the subsequent translocation. Results: We found evidence for two-fold decline in heterozygosity and three- to four-fold increase in inbreeding in modern genomes. Moreover, there was partial support for temporal reduction in total load for detrimental variation. In contrast, compared to historical genomes, modern genomes showed a significantly higher realised load, reflecting the temporal increase in inbreeding. Furthermore, the translocation induced only small changes in the frequency of deleterious alleles, with the majority of detrimental variation being shared between the two populations. Conclusion: Our results highlight the dynamics of mutational load in a species that recovered from the brink of extinction, and show rather limited temporal changes in mutational load. We hypothesise that ancestral purging may have been facilitated by population fragmentation and isolation on several islands for thousands of generations and may have already reduced much of the highly deleterious load well before human arrival and introduction of pests to the archipelago. The majority of fixed deleterious variation was shared between the modern populations, but translocation of individuals with low mutational load could possibly mitigate further fixation of high-frequency deleterious variation.</p>}},
  author       = {{von Seth, Johanna and van der Valk, Tom and Lord, Edana and Sigeman, Hanna and Olsen, Remi André and Knapp, Michael and Kardailsky, Olga and Robertson, Fiona and Hale, Marie and Houston, Dave and Kennedy, Euan and Dalén, Love and Norén, Karin and Massaro, Melanie and Robertson, Bruce C. and Dussex, Nicolas}},
  issn         = {{1471-2164}},
  keywords     = {{Bottleneck; Genomics; Inbreeding; Mutational load; Near-extinction; Translocation}},
  language     = {{eng}},
  number       = {{1}},
  publisher    = {{BioMed Central (BMC)}},
  series       = {{BMC Genomics}},
  title        = {{Genomic trajectories of a near-extinction event in the Chatham Island black robin}},
  url          = {{http://dx.doi.org/10.1186/s12864-022-08963-1}},
  doi          = {{10.1186/s12864-022-08963-1}},
  volume       = {{23}},
  year         = {{2022}},
}