Rethinking pathways to the dioecy-polyploidy association: Genera with many dioecious species have fewer polyploids

Wilhelm H A Osterman; Adrian Hill; James G Hagan; Jeannette Whitton; Christine D Bacon; Anne D Bjorkman

doi:10.1002/ajb2.16318

Rethinking pathways to the dioecy-polyploidy association: Genera with many dioecious species have fewer polyploids

Am J Bot. 2024 Apr 23:e16318. doi: 10.1002/ajb2.16318. Online ahead of print.

Authors

Wilhelm H A Osterman^{1

2}, Adrian Hill^{1

2}, James G Hagan^{2

3}, Jeannette Whitton⁴, Christine D Bacon^{1

2}, Anne D Bjorkman^{1

2}

Affiliations

¹ Department of Biological and Environmental Sciences, University of Gothenburg, Gothenburg, Sweden.
² Gothenburg Global Biodiversity Centre, Gothenburg, Sweden.
³ Department of Marine Sciences, University of Gothenburg, Gothenburg, Sweden.
⁴ Department of Botany and Biodiversity Research Centre, The University of British Columbia, Vancouver, Canada.

PMID: 38654555
DOI: 10.1002/ajb2.16318

Abstract

Premise: Numerous studies have found a positive association between dioecy and polyploidy; however, this association presents a theoretical conflict: While polyploids are predicted to benefit from self-reproduction for successful establishment, dioecious species cannot self-reproduce. We propose a theoretical framework to resolve this apparent conflict. We hypothesize that the inability of dioecious species to self-reproduce hinders their establishment as polyploids. We therefore expect that genera with many dioecious species have fewer polyploids, leading to a negative association between polyploidy and dioecy across genera.

Methods: We used three publicly available databases to determine ploidy and sexual systems for 131 genera and 546 species. We quantified (1) the relationship between the frequency of polyploid species and the frequency of dioecious species across genera, and (2) the proportion of polyploids with hermaphroditism and dioecy across species, adjusting for phylogenetic history.

Results: Across genera, we found a negative relationship between the proportion of polyploids and the proportion of dioecious species, a consistent trend across clades. Across all species, we found that sexual system (dioecious or not) was not associated with polyploidy.

Conclusions: Polyploids are rare in genera in which the majority of species are dioecious, consistent with the theory that self-reproduction favors polyploid establishment. The low frequency of polyploidy among dioecious species indicates the association is not as widespread as previously suggested. Our findings are consistent with previous studies identifying a positive relationship between the two traits, but only if polyploidy promotes a transition to dioecy, and not the reverse.

Keywords: correlated evolution; dioecy; hermaphroditis; minority cytotype exclusion; polyploidy; population establishment; self pollination; sexual dimorphism; sexual systems; whole genome duplication.