Ancient mitochondrial and modern whole genomes unravel massive genetic diversity loss during near extinction of Alpine ibex

Abstract

Population bottlenecks can have dramatic consequences for the health and long‐term survival of a species. Understanding of historic population size and standing genetic variation prior to a contraction allows estimating the impact of a bottleneck on the species' genetic diversity. Although historic population sizes can be modelled based on extant genomics, uncertainty is high for the last 10–20 millenia. Hence, integrating ancient genomes provides a powerful complement to retrace the evolution of genetic diversity through population fluctuations. Here, we recover 15 high‐quality mitogenomes of the once nearly extinct Alpine ibex spanning 8601 BP to 1919 CE and combine these with 60 published modern whole genomes. Coalescent demography simulations based on modern whole genomes indicate population fluctuations coinciding with the last major glaciation period. Using our ancient and historic mitogenomes, we investigate the more recent demographic history of the species and show that mitochondrial haplotype diversity was reduced to a fifth of the prebottleneck diversity with several highly differentiated mitochondrial lineages having coexisted historically. The main collapse of mitochondrial diversity coincides with elevated human population growth during the last 1–2 kya. After recovery, one lineage was spread and nearly fixed across the Alps due to recolonization efforts. Our study highlights that a combined approach integrating genomic data of ancient, historic and extant populations unravels major long‐term population fluctuations from the emergence of a species through its near extinction up to the recent past.

A paleogenomic investigation of overharvest implications in an endemic wild reindeer subspecies

“…Median heterozygosity was reduced by 26% over the time spanning the prehunting and the post-hunting periods. This decrease is congruent with results obtained from previous studies comparing modern to historic/ancient vertebrates that underwent largescale population declines due to anthropogenic near-extirpation events, for example the white rhinoceros (Ceratotherium simum (Burchell, 1817))((Sánchez-Barreiro et al, 2021)), alpine ibex (Capra ibex, Linnaeus, 1758) ( (Robin et al, 2022)), eastern gorilla (Gorilla beringei Matschie, 1903)(van der Valk et al, 2019 and iberian lynx (Casas-Marce et al, 2017). The Svalbard reindeer's decrease of heterozygosity over time is of similar severity to that measured following drastic population declines in the Iberian lynx (heterozygosity reduction of 10% based on microsatellite data, (Casas-Marce et al, 2017) and in two overharvested populations of white rhinoceros (heterozygosity reductions of 10% and 37% respectively, (Sánchez-Barreiro et al, 2021).…”

“…Our measurements of temporal change in mitogenome diversity did not suggest a strong decrease in genetic diversity. The relatively high diversity of modern haplogroups ( n = 7) contrasts with other ungulate species heavily hunted in the past, like the Alpine ibex, where only two modern haplogroups are now widespread across their range (Robin et al, 2022).…”

“…Ancient DNA is therefore a powerful tool that allows for direct temporal comparisons, setting a “baseline” for the state of the species before anthropogenic intrusions (Díez-Del-Molino et al, 2018; Jensen et al, 2022). The respective measures of genetic change through time are valuable in ecological, evolutionary and conservation contexts, with a potential to inform future conservation efforts (Jensen et al, 2022), for example by studying genomic erosion (Robin et al, 2022; Sánchez-Barreiro et al, 2021), the sum of genetic threats to small populations, such as decreasing genome-wide diversity, increasing genetic load and inbreeding, and reduced genome wide heterozygosity (Díez-Del-Molino et al, 2018; Frankham, 2005; Kohn et al, 2006). By comparing the genomes of different temporal populations, regions of high genomic divergence can be identified.…”

Assessing the genetic composition of cotton‐top tamarins (Saguinus oedipus) before sweeping anthropogenic impact

“…While initially studies were constrained to the analysis of single markers, such as mitochondrial DNA (mtDNA), to study population structure of various species including Alpine ibex, Iberian lynx and multiple fish species (Casas-Marce et al, 2017;Robin et al, 2022;Rodrigues et al, 2018;Star et al, 2017), in recent years, whole genome resequencing has started to be applied, also including ancient DNA (aDNA) and historical DNA (hDNA) in order to characterize how genetic diversity has changed through time (Feng et al, 2019;Pinsky et al, 2021;Sánchez-Barreiro et al, 2021;van der Valk et al, 2019).…”

“…The analysis of DNA generated from time series of specimens is key to monitoring genetic diversity in species or their populations. While initially studies were constrained to the analysis of single markers, such as mitochondrial DNA (mtDNA), to study population structure of various species including Alpine ibex , Iberian lynx and multiple fish species (Casas‐Marce et al, 2017; Robin et al, 2022; Rodrigues et al, 2018; Star et al, 2017), in recent years, whole genome resequencing has started to be applied, also including ancient DNA (aDNA) and historical DNA (hDNA) in order to characterize how genetic diversity has changed through time (Feng et al, 2019; Pinsky et al, 2021; Sánchez‐Barreiro et al, 2021; van der Valk et al, 2019). Importantly, these types of studies can in theory provide baseline information that predates heavy negative anthropogenic impacts, thus establishing the genetic diversity against which levels of genomic erosion can be compared (Díez‐del‐Molino et al, 2018).…”