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A comparative study of population genetic structure reveals patterns consistent with selection at functional microsatellites in common sunflower

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Abstract

Microsatellites, also known as short tandem repeats (STRs), have long been considered non-functional, neutrally evolving regions of the genome. Recent findings suggest that they can function as drivers of rapid adaptive evolution. Previous work on the common sunflower identified 479 transcribed microsatellites where allele length significantly correlates with gene expression (eSTRs) in a stepwise manner. Here, a population genetic approach is used to test whether eSTR allele length variation is under selection. Genotypic variation among and within populations at 13 eSTRs was compared with that at 19 anonymous microsatellites in 672 individuals from 17 natural populations of sunflower from across a cline running from Saskatchewan to Oklahoma (distance of approximately 1600 km). Expected heterozygosity, allelic richness, and allelic diversity were significantly lower at eSTRs, a pattern consistent with higher relative rates of purifying selection. Further, an analysis of variation in microsatellite allele lengths (lnRV), and heterozygosities (lnRH), indicate recent selective sweeps at the eSTRs. Mean microsatellite allele lengths at four eSTRs within populations are significantly correlated with latitude consistent with the predictions of the tuning-knob model which predicts stepwise relationships between microsatellite allele length and phenotypes. This finding suggests that shorter or longer alleles at eSTRs may be favored in climatic extremes. Collectively, our results imply that eSTRs are likely under selection and that they may be playing a role in facilitating local adaptation across a well-defined cline in the common sunflower.

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Acknowledgements

The authors wish to thank E. L. Drummond and E. V. McAssey for providing some of the plant material and DNA samples for the population genetic study, S. Pramod and J. L. Martin for help with the initial sampling for the common garden experiment, and A. Andersson, M. M. Kennedy, N. R. Torres for assistance with genotyping. This study was supported by the National Science Foundation grant MCB- 1158521 to M. E. Welch and the Department of Biological Sciences at Mississippi State University.

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  1. Chathurani Ranathunge

    Present address: School of Health Professions, Eastern Virginia Medical School, Norfolk, VA, 23507, USA

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  1. Department of Biological Sciences, Mississippi State University, Starkville, MS, 39762, USA

    Chathurani Ranathunge, Melody E. Chimahusky & Mark E. Welch

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Supplementary file1 (XLSX 330 KB)

438_2022_1920_MOESM2_ESM.tiff

Supplementary file2 Figure S1. Delta K values calculated according to Evanno’s method showing the number of clusters best supported at (a) anonymous and (b) transcribed microsatellites (eSTRs). The number of clusters best supported at anonymous and transcribed microsatellite loci (eSTRs) was K = 2 and K = 5, respectively (TIFF 17579 KB)

438_2022_1920_MOESM3_ESM.png

Supplementary file3 Figure S2. Population genetic structure of 17 natural populations of common sunflower (Helianthus annuus L.) at (a) anonymous and (b) transcribed microsatellite loci (eSTRs). The number of clusters (K) best supported at anonymous microsatellites (a) and eSTRs (b) was K = 2 and K = 5, respectively (PNG 312 KB)

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Ranathunge, C., Chimahusky, M.E. & Welch, M.E. A comparative study of population genetic structure reveals patterns consistent with selection at functional microsatellites in common sunflower. Mol Genet Genomics 297, 1329–1342 (2022). https://doi.org/10.1007/s00438-022-01920-3

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