Bayesian estimation of the timing and severity of a population bottleneck from ancient DNA

Abstract

In this first application of the approximate Bayesian computation approach using the serial coalescent, we demonstrated the estimation of historical demographic parameters from ancient DNA. We estimated the timing and severity of a population bottleneck in an endemic subterranean rodent, Ctenomys sociabilis, over the last 10,000 y from two cave sites in northern Patagonia, Argentina. Understanding population bottlenecks is important in both conservation and evolutionary biology. Conservation implications include the maintenance of genetic variation, inbreeding, fixation of mildly deleterious alleles, and loss of adaptive potential. Evolutionary processes are impacted because of the influence of small populations in founder effects and speciation. We found a decrease from a female effective population size of 95,231 to less than 300 females at 2,890 y before present: a 99.7% decline. Our study demonstrates the persistence of a species depauperate in genetic diversity for at least 2,000 y and has implications for modes of speciation in the incredibly diverse rodent genus Ctenomys. Our approach shows promise for determining demographic parameters for other species with ancient and historic samples and demonstrates the power of such an approach using ancient DNA.

Figure 1. Model of the Population Bottleneck of C. sociabilis Showing a Constant Ancient Female Effective Population Size and Exponential Growth following a Decline in Population Size

Figure 2. The Observed Ancient and Modern Diversity Plotted below (•) with Standard Error Bars Shows the Rejection of the Null Model of a Constant Population with Sizes Ranging from 100 to 200,000 for the Modern and Ancient Nucleotide Diversity in C. sociabilis Found in Cueva Traful

The 95% confidence hulls at each population size assume a single panmictic population based on 1,000 iterations of Serial Simcoal [4] for modern and ancient nucleotide diversity.

Figure 3. Posterior Density Curves of Model Parameters Based on 1,000 Accepted Values from 1,000,000 Iterations of the Bottleneck Model

Thick black line is the posterior density curve of the bottleneck model which includes multiple time points, dashed line is the posterior based on modern data only, and dotted line is the posterior based on two time points, modern and ancient. The mode is indicated with a vertical line and labeled. Thin line is the prior density curve based on 1 million simulated values. (A) Bottleneck time in generations. Assuming a 2-y generation time the peak of the posterior density curve is at 3,118 ybp. Only multiple time points allow reasonable estimation of the bottleneck time. (B) Bottleneck size. (C) Modern population size. (D) Ancient population size. The modern data alone do not provide an estimate the ancient population size; however, with two time points, an estimate of the magnitude of the decline from the ancient population size is possible. (E) Mutation rate expressed as mutations per 253-bp region per generation.

Figure 4. Map of Sampling Sites and Modern Range of C. sociabilis with Table of Temporal Sampling

Listed are number of samples per sampling time and observed values for segregating sites and nucleotide diversity used in the bottleneck model. Numbers on map indicate locations of modern populations [8].