Inbreeding depression and drift load in small populations at demographic disequilibrium

Abstract

Inbreeding depression is a major driver of mating system evolution and has critical implications for population viability. Theoretical and empirical attention has been paid to predicting how inbreeding depression varies with population size. Lower inbreeding depression is predicted in small populations at equilibrium, primarily due to higher inbreeding rates facilitating purging and/or fixation of deleterious alleles (drift load), but predictions at demographic and genetic disequilibrium are less clear. In this study, we experimentally evaluate how lifetime inbreeding depression and drift load, estimated by heterosis, vary with census (N ) and effective (estimated as genetic diversity, H ) population size across six populations of the biennial Sabatia angularis as well as present novel models of inbreeding depression and heterosis under varying demographic scenarios at disequilibrium (fragmentation, bottlenecks, disturbances). Our experimental study reveals high average inbreeding depression and heterosis across populations. Across our small sample, heterosis declined with H , as predicted, whereas inbreeding depression did not vary with H and actually decreased with N . Our theoretical results demonstrate that inbreeding depression and heterosis levels can vary widely across populations at disequilibrium despite similar H and highlight that joint demographic and genetic dynamics are key to predicting patterns of genetic load in nonequilibrium systems.

Phenotypic selection varies with pollination intensity across populations ofSabatia angularis

“…We also note that in the case of variance in self‐pollen deposition, via either autonomous or pollinator‐mediated selfing, issues of pollen quality are not confounded with quantity in our study. There is no early‐acting inbreeding depression in S. angularis ; fruit set and number of seeds per fruit resulting from outcrossed and selfed pollinations are identical (Dudash, ; Spigler et al ., ). Finally, we note that neither population size nor density is correlated with mean pollen receipt across our study populations ( r = 0.18, P = 0.65, and r = 0.47, P = 0.20, respectively).…”

Bottlenecks and inbreeding depression in autotetraploids

“…Individual‐based simulations are also well equipped to model demographic disequilibria that are thought to have important consequences on inbreeding depression (Spigler et al. ). Moreover, the model developed here may be extended relatively easily to higher levels of ploidy beyond tetraploids.…”

“…When considering many loci that contribute to inbreeding depression, simulations permit the development of linkage disequilibria that are known to be important in small populations (Charlesworth et al 1992;Bataillon and Kirkpatrick 2000)-an important biological reality during the formation of neopolyploid lineages. Individual-based simulations are also well equipped to model demographic disequilibria that are thought to have important consequences on inbreeding depression (Spigler et al 2016). Moreover, the model developed here may be extended relatively easily to higher levels of ploidy beyond tetraploids.…”

Selfing ability and drift load evolve with range expansion

“…In these cases, an accumulation of deleterious mutations known as the expansion load (or drift load) may occur (Peischl et al 2013;Henn et al 2016;Peischl et al 2018). Crosses between populations with high expansion load should yield heterosis or hybrid vigor, particularly for those with the smallest effective sizes (Whitlock et al 2000;Oakley et al 2015;Spigler et al 2017;Willi et al 2018). Evolution of the mating system has been associated with reductions in effective population size (Busch et al 2011;Willi et al 2018), which is supported by the robust association between island colonization and self-fertility (Pannell et al 2015;Grossenbacher et al 2017).…”