Genomic reconstruction of the successful establishment of a feralized bovine population on the subantarctic island of Amsterdam

Abstract

The feral cattle of the subantarctic island of Amsterdam provide an outstanding case study of a large mammalian population that was established by a handful of founders and thrived within a few generations in a seemingly inhospitable environment. Here, we investigated the genetic history and composition of this population using genotyping and sequencing data. Our inference showed an intense but brief founding bottleneck around the late 19thcentury and revealed contributions from European taurine and Indian Ocean zebu in the founder ancestry. Comparative analysis of whole genome sequences further revealed a moderate reduction in genetic diversity despite high levels of inbreeding. The brief and intense bottleneck was associated with high levels of drift, a flattening of the site frequency spectrum and a slight relaxation of purifying selection on mildly deleterious variants. However, we did not observe any significant purge of highly deleterious variants.Interestingly, the population’s success in the harsh environment can be attributed to pre-adaptation from their European taurine ancestry, suggesting no strong bioclimatic challenge, and also contradicting evidence for insular dwarfism. Genome scan for footprints of selection uncovered a majority of candidate genes related to nervous system function, likely reflecting rapid feralization driven by behavioral changes and complex social restructuring. This unprecedented case study provides valuable insights into rapid population establishment, feralization, and genetic adaptation in challenging environments. It highlights the importance of preserving the unique genetic legacies of feral populations and raises ethical questions in the eyes of conservation efforts.

Predicting species invasiveness with genomic data: is Genomic Offset related to establishment probability?

“…Nevertheless, some studies have shown evidence of genetic load purging in invasive species (Facon et al ., 2011; Tayeh et al ., 2013; Mullarkey et al ., 2013; Marchini et al ., 2016), and gene flow and/or admixture can also mask genetic load (Whiteley et al ., 2015). Furthermore, cases exist where populations, despite showing evidence of high genetic load without a clear purging signal, have successfully established and persisted in new environments (Gautier et al ., 2023; Zayed et al ., 2007). Demographic parameters and stochastic factors can influence genetic load and therefore population persistence in contrasting ways (reviewed in Robinson et al .…”

“…Furthermore, cases exist where populations, despite showing evidence of high genetic load without a clear purging signal, have successfully established and persisted in new environments (Gautier et al, 2023;Zayed et al, 2007). Demographic parameters and stochastic factors can influence genetic load and therefore population persistence in contrasting ways (reviewed in Robinson et al (2023) and Bouzat (2010)).…”

Predicting species invasiveness with genomic data: Is genomic offset related to establishment probability?

“…Nevertheless, some studies have shown evidence of genetic load purging in invasive species (Facon et al., 2011 ; Marchini et al., 2016 ; Mullarkey et al., 2013 ; Tayeh et al., 2013 ), and gene flow and/or admixture can also mask genetic load (Whiteley et al., 2015 ). Furthermore, cases exist where populations, despite showing evidence of high genetic load without a clear purging signal, have successfully established and persisted in new environments (Gautier et al., 2023 ; Zayed et al., 2007 ). Demographic parameters and stochastic factors can influence genetic load and therefore population persistence in contrasting ways (reviewed in Robinson et al.…”

“…showing evidence of high genetic load without a clear purging signal, have successfully established and persisted in new environments (Gautier et al, 2023;Zayed et al, 2007). Demographic parameters and stochastic factors can influence genetic load and therefore population persistence in contrasting ways (reviewed in Robinson et al (2023) and Bouzat (2010)).…”