Ecological differentiation, lack of hybrids involving diploids, and asymmetric gene flow between polyploids in narrow contact zones of Senecio carniolicus (syn. Jacobaea carniolica, Asteraceae)

Abstract

Areas of immediate contact of different cytotypes offer a unique opportunity to study evolutionary dynamics within heteroploid species and to assess isolation mechanisms governing coexistence of cytotypes of different ploidy. The degree of reproductive isolation of cytotypes, that is, the frequency of heteroploid crosses and subsequent formation of viable and (partly) fertile hybrids, plays a crucial role for the long-term integrity of lineages in contact zones. Here, we assessed fine-scale distribution, spatial clustering, and ecological niches as well as patterns of gene flow in parental and hybrid cytotypes in zones of immediate contact of di-, tetra-, and hexaploid Senecio carniolicus (Asteraceae) in the Eastern Alps. Cytotypes were spatially separated also at the investigated microscale; the strongest spatial separation was observed for the fully interfertile tetra- and hexaploids. The three main cytotypes showed highly significant niche differences, which were, however, weaker than across their entire distribution ranges in the Eastern Alps. Individuals with intermediate ploidy levels were found neither in the diploid/tetraploid nor in the diploid/hexaploid contact zones indicating strong reproductive barriers. In contrast, pentaploid individuals were frequent in the tetraploid/hexaploid contact zone, albeit limited to a narrow strip in the immediate contact zone of their parental cytotypes. AFLP fingerprinting data revealed introgressive gene flow mediated by pentaploid hybrids from tetra- to hexaploid individuals, but not vice versa. The ecological niche of pentaploids differed significantly from that of tetraploids but not from hexaploids.

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

“…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).…”

Postzygotic isolation varies by ploidy level within a polyploid complex

“…Increased interploid gene flow among higher cytotypes may also help explain why pentaploids are found more commonly in mixed tetraploid–hexaploid populations than triploids are found in mixed diploid–tetraploid populations (e.g. Stevens et al ., ; Hülber et al ., ; B. L. Sutherland, unpublished). Our results also caution against assumptions of little to no gene flow in diploid–tetraploid populations based on absence of triploids.…”

“…In particular, recent work suggests that reproductive barriers between higher order polyploids may be weaker than those between diploids and polyploids (Hersch-Green, 2012;Sonnleitner et al, 2013;H€ ulber et al, 2015). If interploid reproductive isolation is incomplete, gene flow between cytotypes could slow diversification and speciation among polyploid lineages (Costa et al, 2014).…”

Pure polyploidy: Closing the gaps in autopolyploid research

“…Most studies address the common hypothesis that polyploids will evolve to occupy wider or more extreme ranges than their diploid progenitors (Husband et al, 2013). Numerous studies of niche differentiation in autopolyploid complexes have supported this hypothesis (e.g., Baack & Stanton, 2005;Thompson et al, 2014;Arnold et al, 2015;H€ ulber et al, 2015;Liu et al, 2015;Visger et al, 2016), but many others have found little to no abiotic niche differentiation between cytotypes (e.g., Godsoe et al, 2013;Casazza et al, 2016;Duchoslav et al, 2016), including studies that compared different cytotypes in multiple species (Glennon et al, 2014). Similarly, allopolyploids also show variable amounts of climatic niche divergence-and often broad niche overlap-when compared to their diploid progenitors (Marchant et al, 2016).…”