Genetic load, eco-evolutionary feedback, and extinction in metapopulations

Habitat fragmentation poses a significant risk to population survival, causing both demographic stochasticity and genetic drift within local populations to increase, thereby increasing genetic load. Higher load causes population numbers to decline, which reduces the efficiency of selection and further increases load, resulting in a positive feedback that may drive entire populations to extinction. Here, we investigate this eco-evolutionary feedback in a metapopulation consisting of local demes connected via migration, with individuals subject to deleterious mutation at a large number of loci. We first analyze the determinants of load under soft selection, where population sizes are fixed, and then build on this to understand hard selection, where population sizes and load coevolve. We show that under soft selection, very little gene flow (less than one migrant per generation) is enough to prevent fixation of deleterious alleles. By contrast, much higher levels of migration are required to mitigate load and prevent extinction when selection is hard, with critical migration thresholds for metapopulation persistence increasing sharply as the genome-wide deleterious mutation rate becomes comparable to the baseline population growth rate. Moreover, critical migration thresholds are highest if deleterious mutations have intermediate selection coefficients but lower if alleles are predominantly recessive rather than additive (due to more efficient purging of recessive load within local populations). Our analysis is based on a combination of analytical approximations and simulations, allowing for a more comprehensive understanding of the factors influencing load and extinction in fragmented populations.