Strength in numbers? Cytotype frequency mediates effect of reproductive barriers in mixed‐ploidy arrays

Abstract

When differentiated lineages come into contact, their fates depend on demographic and reproductive factors. These factors have been well-studied in taxa of the same ploidy, but less is known about sympatric lineages that differ in ploidy, particularly with respect to demographic factors. We assessed prezygotic, postzygotic, and total reproductive isolation in naturally pollinated arrays of diploid-tetraploid and tetraploid-hexaploid population mixes of Campanula rotundifolia by measuring pollinator transitions, seed yield, germination rate, and proportion of hybrid offspring. Four frequencies of each cytotype were tested, and pollinators consistently overvisited rare cytotypes. Seed yield and F1 hybrid production were greater in 4X-6X arrays than 2X-4X arrays, whereas germination rates were similar, creating two distinct patterns of reproductive isolation. In 2X-4X arrays, postzygotic isolation was near complete (3% hybrid offspring), and prezygotic isolation associated with pollinator preference is expected to facilitate the persistence of minority cytotypes. However, in 4X-6X arrays where postzygotic isolation permitted hybrid formation (44% hybrids), pollinator behavior drove patterns of reproductive isolation, with rare cytotypes being more isolated and greater gene flow expected from rare into common cytotypes. In polyploid complexes, both the specific cytotypes in contact and local cytotype frequency, likely reflecting spatial demography, will influence likelihood of gene exchange.

Do pentaploid hybrids mediate gene flow between tetraploid Senecio disjunctus and hexaploid S. carniolicus s. str. (S. carniolicus aggregate, Asteraceae)?

“…Their hybrid origin was confirmed in many cases, whereas little is known about their role in enabling gene flow between and introgression into their parental cytotypes (Kolář et al 2017). This is especially true for ploidies higher than tetraploid as studied here; previous studies have mostly focussed on triploids originating in diploid-tetraploid contact zones (Ramsey and Schemske 1998; but see Kolář et al 2009;Greiner and Oberprieler 2012;Sutherland and Galloway 2017;Sutherland et al 2020).…”

Differences in Floral Scent and Petal Reflectance Between Diploid and Tetraploid Chamerion angustifolium

“…Natural selection could also act on floral traits for differentiated pollinator signals (e.g., Nuismer and Cunningham, 2005). For pollinators to act as a mechanism to facilitate coexistence of cytotypes (Kolář et al, 2017;Sutherland et al, 2020;Laport et al, 2021), the flowers of the cytotypes must differ in ways that pollinators can perceive (e.g., Segraves and Thompson, 1999) or have sufficient morphological differences to facilitate isolation (e.g., Borges et al, 2012). For Gymnadenia conopsea (Orchidaceae), cytotypes differ in floral signals, mainly floral scent (Jersáková et al, 2010;Gross and Schiestl, 2015), and assortative mating has also been observed in some populations (Gross and Schiestl, 2015), suggesting that these mechanisms may function as reproductive isolation mechanisms in mixed populations of autotetraploids.…”

“…Alternatively, post-pollination mechanisms of isolation may be more important in keeping polyploids distinctive, as in Aster amellus (Asteraceae) (Castro et al, 2011) and for some species little evidence of reproductive isolation is observed (e.g., Barringer and Galloway, 2017). Although pollinator-mediated reproductive isolation between cytotypes has strong theorical support and empirical evidence for some species where it has been measured (e.g., Kennedy et al, 2006;Thompson and Merg, 2008;Roccaforte et al, 2015;Sutherland et al, 2020;Laport et al, 2021), few studies have examined differences in multifaceted floral signals between cytotypes making generalisations challenging.…”

Variation in heteroploid reproduction and gene flow across a polyploid complex: One size does not fit all

“…Reproductive barriers between parental populations, as well as between those populations and heteroploid hybrids, differed with cytotype, with parental and F1 barriers stronger between diploids and tetraploids than between different polyploids. Pollinators show a preference for rare cytotypes in this system, which increases the likelihood of gene flow between a rare cytotype and a common one in contact zones (Sutherland et al, 2020). This preference, coupled with differences in reproductive barriers across cytotypes, sets up two expectations for C. rotundifolia contact zones.…”