Abstract

Hybridisation and polyploidy are major forces contributing to plant speciation. Homoploid (2x) and heteroploid (3x) hybrids, however, represent critical stages for evolution due to disturbed meiosis and reduced fertility. Apomixis – asexual reproduction via seeds – can overcome hybrid sterility, but requires several concerted alterations of developmental pathways to result in functional seed formation.Here, we analyse the reproductive behaviours of homo- and heteroploid synthetic hybrids from crosses between sexual diploid and tetraploid Ranunculus auricomus species to test the hypothesis that developmental asynchrony in hybrids triggers the shift to apomictic reproduction.Evaluation of male and female gametophyte development, viability and functionality of gametes shows developmental asynchrony, whereas seed set and germinability indicate reduced fitness in synthetic hybrids compared to sexual parents. We present the first experimental evidence for spontaneous apospory in most hybrids as an alternative pathway to meiosis, and the appearance of functional apomictic seeds in triploids. Bypassing meiosis permits these triploid genotypes to form viable seed and new polyploid progeny.Asynchronous development causes reduced sexual seed set and emergence of apospory in synthetic Ranunculus hybrids. Apomixis is functional in triploids and associated with drastic meiotic abnormalities. Selection acts to stabilise developmental patterns and to tolerate endosperm dosage balance shifts which facilitates successful seed set and establishment of apomictic lineages.

Highlights

  • Hybridisation and polyploidisation have long been recognised as motors of speciation and evolution in plants (Stebbins, 1950; Grant, 1981; Soltis & Soltis, 2009; Jiao et al, 2011)

  • Fifty individuals were derived from R. notabilis (2x) 9 R. carpaticola (2x), whereas 32 originated from R. notabilis (2x) 9 R. cassubicifolius (4x)

  • Sexual reproduction is entrenched among flowering plants, the Polygonum type of female gametophyte development is prevalent (Maheshwari, 1950; Huang & Russell, 1992), and is characteristic of the diploid Ranunculus notabilis, R. carpaticola and autotetraploid R. cassubicifolius materials analysed here

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Summary

Introduction

Hybridisation and polyploidisation have long been recognised as motors of speciation and evolution in plants (Stebbins, 1950; Grant, 1981; Soltis & Soltis, 2009; Jiao et al, 2011). Natural polyploids (i.e. individuals having more than two haploid sets of chromosomes or genomes), which are common in most angiosperm families (Grant, 1981), can spontaneously arise multiple times in diploid populations by unilateral or bilateral sexual polyploidisation (Bretagnolle & Thompson, 1995). Unilateral sexual polyploidisation is a recurrent mechanism in nature associated with unreduced gamete formation (Bretagnolle & Thompson, 1995; Ramsey & Schemske, 1998; Mallet, 2007). Via the fusion of reduced gametes from one parent and unreduced ones from the other, triploid offspring can be formed

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