Many studies have quantified the distribution of heterozygosity and relatedness in natural populations, but few have examined the demographic processes driving these patterns. In this study, we take a novel approach by studying how population structure affects both pairwise identity and the distribution of heterozygosity in a natural population of the self-incompatible plant Antirrhinum majus. Excess variance in heterozygosity between individuals is due to identity disequilibrium, which reflects the variance in inbreeding between individuals; it is measured by the statistic g2. We calculated g2 together with FST and pairwise relatedness (Fij) using 91 SNPs in 22,353 individuals collected over 11 years. We find that pairwise Fij declines rapidly over short spatial scales, and the excess variance in heterozygosity between individuals reflects significant variation in inbreeding. Additionally, we detect an excess of individuals with around half the average heterozygosity, indicating either selfing or matings between close relatives. We use 2 types of simulation to ask whether variation in heterozygosity is consistent with fine-scale spatial population structure. First, by simulating offspring using parents drawn from a range of spatial scales, we show that the known pollen dispersal kernel explains g2. Second, we simulate a 1,000-generation pedigree using the known dispersal and spatial distribution and find that the resulting g2 is consistent with that observed from the field data. In contrast, a simulated population with uniform density underestimates g2, indicating that heterogeneous density promotes identity disequilibrium. Our study shows that heterogeneous density and leptokurtic dispersal can together explain the distribution of heterozygosity.
Part of this work was funded by Marie Curie COFUND Doctoral Fellowship and Austrian Science Fund FWF (grant P32166). We thank the many volunteers and friends who have contributed to data collection in the field site over the years, in particular those who have managed field seasons: Barbora Trubenova, Maria Clara Melo, Tom Ellis, Eva Cereghetti, Lenka Matejovicova, Beatriz Pablo Carmona. Frederic Ferrer and Eva Salmerón Mateu have been immensely helpful with logistics at our informal field station, El Serrat de Planoles. We thank Sean Stankowski for technical help in producing figure 1. This research was also supported by the Scientific Service Units (SSU) of IST Austria through resources provided by Scientific Computing (SciComp).
Surendranadh P, Arathoon LS, Baskett C, Field D, Pickup M, Barton NH. Effects of fine-scale population structure on the distribution of heterozygosity in a long-term study of Antirrhinum majus. Genetics. 2022;221(3). doi:10.1093/genetics/iyac083
Surendranadh, P., Arathoon, L. S., Baskett, C., Field, D., Pickup, M., & Barton, N. H. (2022). Effects of fine-scale population structure on the distribution of heterozygosity in a long-term study of Antirrhinum majus. Genetics. Oxford University Press. https://doi.org/10.1093/genetics/iyac083
Surendranadh, Parvathy, Louise S Arathoon, Carina Baskett, David Field, Melinda Pickup, and Nicholas H Barton. “Effects of Fine-Scale Population Structure on the Distribution of Heterozygosity in a Long-Term Study of Antirrhinum Majus.” Genetics. Oxford University Press, 2022. https://doi.org/10.1093/genetics/iyac083.
P. Surendranadh, L. S. Arathoon, C. Baskett, D. Field, M. Pickup, and N. H. Barton, “Effects of fine-scale population structure on the distribution of heterozygosity in a long-term study of Antirrhinum majus,” Genetics, vol. 221, no. 3. Oxford University Press, 2022.
Surendranadh P, Arathoon LS, Baskett C, Field D, Pickup M, Barton NH. 2022. Effects of fine-scale population structure on the distribution of heterozygosity in a long-term study of Antirrhinum majus. Genetics. 221(3), iyac083.
Surendranadh, Parvathy, et al. “Effects of Fine-Scale Population Structure on the Distribution of Heterozygosity in a Long-Term Study of Antirrhinum Majus.” Genetics, vol. 221, no. 3, iyac083, Oxford University Press, 2022, doi:10.1093/genetics/iyac083.
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