Ancient mitogenomes unravel massive genetic diversity loss during near extinction of Alpine ibex

Population bottlenecks can have dramatic consequences for the health and long-term survival of a species. A recent bottleneck event can also largely obscure our understanding of standing variation prior to the contraction. Historic population sizes can be modeled based on extant genomics, however uncertainty increases with the severity of the bottleneck. 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 {+/-} 33 BP to 1919 CE and combine these with 60 published modern genomes. Coalescent demography simulations based on modern genomes indicate population fluctuations matching major climatic change over the past millennia. Using ancient genomes, we show that mitochondrial haplotype diversity has been reduced to a fifth of the pre-bottleneck diversity with several highly differentiated mitochondrial lineages having co-existed historically. The main collapse of mitochondrial diversity coincided with human settlement expansions in the Middle Ages. The near extinction severely reduced the mitochondrial diversity. After recovery, one lineage was spread and nearly fixed across the Alps due to recolonization efforts. Contrary to expectations, we show that a second ancestral mitochondrial lineage has survived in an isolated population further south. Our study highlights that a combined approach integrating genomic data of ancient, historic and extant populations unravels major long-term population fluctuations.