Estimating demographic contributions to effective population size in an age-structured wild population experiencing environmental and demographic stochasticity

Abstract

A population's effective size (N_e ) is a key parameter that shapes rates of inbreeding and loss of genetic diversity, thereby influencing evolutionary processes and population viability. However, estimating N_e , and identifying key demographic mechanisms that underlie the N_e to census population size (N) ratio, remains challenging, especially for small populations with overlapping generations and substantial environmental and demographic stochasticity and hence dynamic age-structure. A sophisticated demographic method of estimating N_e /N, which uses Fisher's reproductive value to account for dynamic age-structure, has been formulated. However, this method requires detailed individual- and population-level data on sex- and age-specific reproduction and survival, and has rarely been implemented. Here, we use the reproductive value method and detailed demographic data to estimate N_e /N for a small and apparently isolated red-billed chough (Pyrrhocorax pyrrhocorax) population of high conservation concern. We additionally calculated two single-sample molecular genetic estimates of N_e to corroborate the demographic estimate and examine evidence for unobserved immigration and gene flow. The demographic estimate of N_e /N was 0.21, reflecting a high total demographic variance (σ2dg) of 0.71. Females and males made similar overall contributions to σ2dg. However, contributions varied among sex-age classes, with greater contributions from 3 year-old females than males, but greater contributions from ≥5 year-old males than females. The demographic estimate of N_e was ~30, suggesting that rates of increase of inbreeding and loss of genetic variation per generation will be relatively high. Molecular genetic estimates of N_e computed from linkage disequilibrium and approximate Bayesian computation were approximately 50 and 30, respectively, providing no evidence of substantial unobserved immigration which could bias demographic estimates of N_e . Our analyses identify key sex-age classes contributing to demographic variance and thus decreasing N_e /N in a small age-structured population inhabiting a variable environment. They thereby demonstrate how assessments of N_e can incorporate stochastic sex- and age-specific demography and elucidate key demographic processes affecting a population's evolutionary trajectory and viability. Furthermore, our analyses show that N_e for the focal chough population is critically small, implying that management to re-establish genetic connectivity may be required to ensure population viability.

Keywords: conservation genetics; evolutionary potential; iteroparity; life-history variation; population connectivity; population management; reproductive skew.