Paternity analysis reveals constraints on hybridization potential between native and introduced bluebells (Hyacinthoides)

Abstract

The native UK bluebell Hyacinthoides non-scripta is considered to be at risk from hybridization with naturalised non-native bluebells. The non-natives, likely to be hybrid themselves (H. x massartiana) between H. non-scripta and H. hispanica, occur in relatively small numbers throughout the UK range of natives. Full interfertility between taxa has been repeatedly asserted in reporting spread of non-natives and predicting genetic erosion or assimilation of the native. However, there have been no published data to support suppositions that non-natives arose from in-situ hybridization, or that natural hybridization represents an ongoing threat to the native bluebell. Here we first investigated hybridization potential via reciprocal hand-crosses and observed overlap in flowering periods of native and non-native bluebells, finding that flowering was largely synchronous and that seed set and early seedling survival were equivalent for between-taxon crosses. We then established an experimental array allowing natural pollination to occur among flowering plants, and determined the paternity of offspring using microsatellite markers. We found that natives were more likely to produce seeds than non-natives, and that paternities approximated three native to one non-native, regardless of the identity of the maternal parent. Our results demonstrate that hybridization in natural populations and introgression between natives and non-natives are possible. However, lower reproductive success of non-natives coupled with the massive numerical advantage of natives represents a substantial constraint against ‘extinction-by-hybridization’ of H. non-scripta in the UK.

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Acknowledgements

This work was supported by a Daphne Jackson Fellowship to DDK funded by the Natural Environment Research Council, the European Union FP 6 Integrated Project ALARM: Assessing LArgescale environmental Risks for biodiversity with tested Methods (GOCE-CT-2003-506675), the Botanical Society of the British Isles, the National Botanic Gardens of Scotland Membership Programme Small Projects Fund, and a Discovery Grant from the Natural Sciences and Engineering Research Council of Canada to SCHB. Our thanks to Jane Squirrell for work on pollen and chromosomes at RBGE, to Alex Clark for translating Geerinck (1996), and to landowners for permissions. The Royal Botanic Garden Edinburgh is supported by the Scottish Government’s Rural and Environmental Science and Analytical Services Division.

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Supplementary Fig. 1

Design of the experimental array established at the Royal Botanic Garden Edinburgh to investigate natural crossing between native and non-native bluebells. (A) A group of 16 flowering plants, showing pattern of individually-potted natives (8) and non-natives (8). The triploid plant was a non-native. (B) Schematic field layout of experimental array (not to scale). The seven groups (shaded boxes), of 16 bluebells each, occupied a total area of 75 m x 40 m, with each group 23.5-35 m from the nearest other group (DOCX 53 KB)

Supplementary Fig. 2

. Example of stained and unstained bluebell pollen, showing 100% viability (native, left) and 14% viability (non-native, right). Size bars on the images are 100 µm at lower magnification (left) and 50 µm at the higher magnification (right) (DOCX 822 KB)

Supplementary Table 1

Statistics and results (in bold) for interfertility and early seedling survival in experimental hand-crosses between native and non-native Hyacinthoides taxa. See Figure 4 for plots of these data. Crosses are maternal taxon x paternal taxon; crosses in 2009 and 2010 comprised native maternal plants only. (DOCX 17 KB)

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Kohn, D.D., Ruhsam, M., Hulme, P.E. et al. Paternity analysis reveals constraints on hybridization potential between native and introduced bluebells (Hyacinthoides). Conserv Genet 20, 571–584 (2019). https://doi.org/10.1007/s10592-019-01158-4

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Keywords

  • Invasive species
  • Congenerics
  • Flowering phenology
  • Genetic erosion
  • Introgression
  • Paternity analysis