Abstract

Polyploidy, the possession of more than two sets of chromosomes, is a major biological process affecting plant evolution and diversification. In the Cactaceae, genome doubling has also been associated with reproductive isolation, changes in breeding systems, colonization ability, and speciation. Pachycereus pringlei (S. Watson, 1885) Britton & Rose, 1909, is a columnar cactus that has long drawn the attention of ecologists, geneticists, and systematists due to its wide distribution range and remarkable assortment of breeding systems in the Mexican Sonoran Desert and the Baja California Peninsula (BCP). However, several important evolutionary questions, such as the distribution of chromosome numbers and whether the diploid condition is dominant over a potential polyploid condition driving the evolution and diversity in floral morphology and breeding systems in this cactus, are still unclear. In this study, we determined chromosome numbers in 11 localities encompassing virtually the entire geographic range of distribution of P. pringlei. Our data revealed the first diploid (2n = 22) count in this species restricted to the hermaphroditic populations of Catalana (ICA) and Cerralvo (ICE) Islands, whereas the tetraploid (2n = 44) condition is consistently distributed throughout the BCP and mainland Sonora populations distinguished by a non-hermaphroditic breeding system. These results validate a wider distribution of polyploid relative to diploid individuals and a shift in breeding systems coupled with polyploidisation. Considering that the diploid base number and hermaphroditism are the proposed ancestral conditions in Cactaceae, we suggest that ICE and ICA populations represent the relicts of a southern diploid ancestor from which both polyploidy and unisexuality evolved in mainland BCP, facilitating the northward expansion of this species. This cytogeographic distribution in conjunction with differences in floral attributes suggests the distinction of the diploid populations as a new taxonomic entity. We suggest that chromosome doubling in conjunction with allopatric distribution, differences in neutral genetic variation, floral traits, and breeding systems has driven the reproductive isolation, evolution, and diversification of this columnar cactus.

Highlights

  • Polyploidy and hybridisation are major biological events in plant evolution and speciation (Grant 1981, Wendel and Doyle 2005), often leading to complex patterns of genetic diversity, reproductive isolation, and discrepancy in breeding systems (De Wet 1971, Tate et al 2005, Marques et al 2014)

  • Considering that the diploid base number and hermaphroditism are the proposed ancestral conditions in Cactaceae, we suggest that in plants from Cerralvo (ICE) and ICA populations represent the relicts of a southern diploid ancestor from which both polyploidy and unisexuality evolved in mainland Baja California Peninsula (BCP), facilitating the northward expansion of this species

  • We suggest that chromosome doubling in conjunction with allopatric distribution, differences in neutral genetic variation, floral traits, and breeding systems has driven the reproductive isolation, evolution, and diversification of this columnar cactus

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Summary

Introduction

Polyploidy and hybridisation are major biological events in plant evolution and speciation (Grant 1981, Wendel and Doyle 2005), often leading to complex patterns of genetic diversity, reproductive isolation, and discrepancy in breeding systems (De Wet 1971, Tate et al 2005, Marques et al 2014). The Cactaceae, a family with approximately 1,430 species (Hunt et al 2006), exhibits an extensive habitat radiation and reproductive versatility linked to striking specialized floral morphology (Cota-Sánchez and Croutch 2008, Almeida et al 2013) and variation in chromosome numbers (Cota 1991, Baker et al 2009a). Polyploidy, along with variation in breeding systems, has been considered an important factor directing the evolutionary history and disparity of the Cactaceae, often resulting in the formation of new species (Baker and Pinkava 1987, 1999, Baker 2002, 2006). Genome doubling prompts the evolution of some sexual systems in the Cactaceae, i.e., gynodioecy and trioecy (Rebman and Pinkava 2001), and additional chromosome sets have been correlated with physiology and differences in morphological and geographic distribution. For many taxa with wide ecological and geographic distribution the role and extent of polyploidy is still unknown because different ploidy

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