Parental Ploidy Strongly Affects Offspring Fitness in Heteroploid Crosses among Three Cytotypes of Autopolyploid Jacobaea carniolica (Asteraceae)

Abstract

Reproductive interactions among cytotypes in their contact zones determine whether these cytotypes can co-exist and form stable contact zones or not. In autopolyploids, heteroploid cross-compatibilities might depend on parental ploidy, but tests of this hypothesis in autopolyploid systems with more than two ploidies are lacking. Here, we study Jacobaea carniolica, which comprises diploid, tetraploid, and hexaploid individuals regularly forming contact zones. Seeds obtained from in situ cross-pollinations within and among cytotypes were subjected to DNA flow cytometry and greenhouse germination experiments. Hybrid fitness and parental effects on hybrid fitness were tested with regression models comparing fitness parameters of early life stages. Irrespective of the direction of crosses, seed viability and seedling survival in diploid-polyploid crosses were substantially lower than in tetraploid-hexaploid crosses. In contrast, seedling growth traits indicated neither transgressive character expression nor any selection against hybrid offspring. Congruent with a model of genome dosage effects, these traits differed between reciprocal crosses, especially of diploids and tetraploids, where trait values resembled those of the maternal parent. The strong effect of parental ploidy on offspring fitness in heteroploid crosses may cause contact zones involving exclusively polyploid cytotypes to be less stable over longer terms than those involving diploids and polyploids.

The “Polyploid Hop”: Shifting Challenges and Opportunities Over the Evolutionary Lifespan of Genome Duplications

“…This corresponds well with the explanation of maternal: paternal genome imbalance in the endosperm as a primary cause of the postzygotic barrier (Köhler et al, 2010;Greiner and Oberprieler, 2012). Because the magnitude of endosperm imbalance in tetraploid-hexaploid hybrids is approximately one third lower than in diploidtetraploid hybrids (Sonnleitner et al, 2013) these higher-ploidy hybrids may be more fit than diploid-tetraploid hybrids.…”

“…they may hybridize with the tetraploid or among one another and further enhance variation of the polyploid lineages. The few empirical studies available show that the postzygotic barrier, both in terms of rate of hybrid formation and its fitness, is lower among the various polyploid cytotypes than it is between diploids and their polyploid derivatives (Greiner and Oberprieler, 2012;Sonnleitner et al, 2013;Hülber et al, 2015;Sutherland and Galloway, 2017). This corresponds well with the explanation of maternal: paternal genome imbalance in the endosperm as a primary cause of the postzygotic barrier (Köhler et al, 2010;Greiner and Oberprieler, 2012).…”

Phylogenetic relationships and evolution of high mountain buttercups (Ranunculus) in North America and Central Asia

“…brotherusii) has a documented ploidy differentiation, whereby no exhaustive studies on cytotype diversity are available. Moreover, reproductive isolation between different high ploidy levels tends to be weaker than between diploid and polyploid cytotypes (Sonnleitner et al, 2013). Therefore, the Southern Central Asian network probably reflects incomplete species boundaries, which have been also observed in the Himalayan/Tibetan genus Leontopodium (Edelweiss; Blöch et al, 2010) and some taxa of the Tibetan flora (e.g., Liu et al, 2002Liu et al, , 2006Wang and Liu, 2004;Wang et al, 2005).…”

“…However, present distribution patterns and case studies suggest that also sympatric speciation has to be considered for alpine plant evolution (Baack, 2004;Kadereit et al, 2008;Sonnleitner et al, 2010Sonnleitner et al, , 2013. In sympatry, species can evolve either via ecological differentiation or via postzygotic isolation, the latter being often a result of chromosomal rearrangements or of polyploidy (Coyne and Orr, 2004).…”

“…Polyploidy establishes immediate postzygotic crossing barriers against the diploid progenitor because of meiotic disturbances and sterility in backcrosses (Comai, 2005;Rieseberg and Willis, 2007). Postzygotic reproductive isolation between cytotypes, however, is not necessarily complete in plant populations (Baack, 2004;Sonnleitner et al, 2013). In high mountain systems, spontaneous polyploidization is frequent because of two factors: first, range fluctuations of plant species during glaciation/interglaciation cycles, and secondary contacts of previously isolated species triggered hybridization and polyploidy (Comes and Kadereit, 1998;Hewitt, 2004); second, cold temperatures can increase frequencies of formation of unreduced gametes, and may therefore enhance polyploidization (Ramsey and Schemske, 1998;Brochmann et al, 2004).…”