Invasion success in polyploids: the role of inbreeding in the contrasting colonization abilities of diploid versus tetraploid populations of Centaurea stoebe s.l.

Abstract

Summary As a consequence of founder effects, inbreeding can hamper colonization success: First, in species with self‐incompatibility controlled by an S‐locus, inbreeding may decrease cross‐compatibility, mainly due to the sharing of identical S‐alleles between closely related mating partners. Secondly, inbreeding can reduce fitness of inbred relative to outbred offspring (i.e. inbreeding depression). Polyploids often show reduced inbreeding depression compared to diploids, which may contribute to the overrepresentation of polyploids among invasive species. This is the first study that tests how the effects of inbreeding differ between geocytotypes (i.e. ploidy levels within a given range). Our model organism, Centaurea stoebe, is strictly self‐incompatible and comprises three geocytotypes: diploids are more frequent than tetraploids in the native range, while only tetraploids occur in the invasive range. We conducted a breeding experiment (sib‐mating vs. outcrossing) with 14 native diploid, 13 native tetraploid and 15 invasive tetraploid populations. We recorded cross‐compatibility and estimated a cumulative index for offspring fitness. Since frequent inbreeding can result in purging of genetic load responsible for inbreeding depression, our analyses included a metric for within‐population relatedness, based on eight microsatellite markers, to assess the effect of purging. Inbreeding was found to reduce cross‐compatibility, which was similarly pronounced in diploids and tetraploids. It also caused inbreeding depression in cumulative fitness, which was significant in diploids but not in tetraploids. No evidence of purging was observed as inbred fitness was not affected by within‐population relatedness. Synthesis. Our results provide new insights into the contrasting invasion success of the cytotypes of C. stoebe. As the effects of cross‐compatibility and purging were comparable between cytotypes, both processes can be ruled out to affect the colonization success of diploids versus tetraploids. Our findings are consistent with the hypothesis that polyploidy increases the masking of recessive mutations, which maintains high fitness in inbred tetraploids and may thus facilitate colonization of new ranges. We highlight that reduced inbreeding depression may add to previously acknowledged advantages of polyploids in range expansions, a mechanism that may hitherto have been underestimated due to a lack of data on variation in inbreeding depression across geocytotypes.

Bottlenecks and inbreeding depression in autotetraploids

“…Regardless, the formation of neopolyploids through the union of unreduced gametes should cause dramatic declines in inbreeding depression, far beyond those expected for population bottlenecks in general (Otto and Whitton 2002; Rosche et al. ). This results from the decrease in the number of segregating mutations due to bottleneck effects combined with the masking of partially recessive mutations in several heterozygous genotypes.…”

Interspecific variation in ploidy as a key plant trait outlining local extinction risks and community patterns in fragmented landscapes

“…Tetra‐ and polyploid populations may also benefit from the additional gene flow on fragments close by semi‐natural grassland fragments. Yet, contrary to diploids, they may depend far less upon it for their long‐term persistence, possibly because polyploidy buffers genetic erosion in spite of fragmentation (Moody et al., ; Rosche et al., ; Soltis & Soltis, ). Hence, the absence of a response to increasing spatial isolation in tetra‐ and polyploid diversity observed here.…”

“…Therefore, ploidy may capture the summed effects of these mechanisms on local extinction risk. Moreover, other possible pathways by which increasing ploidy may diminish species' local extinction risks may also exist (see te Beest et al., ; Birchler et al., ; Kirchheimer et al., ; Rosche et al., ). Still, the combined evidence here clearly suggests that polyploids hold key biological attributes which contribute to ecological success in fragmented landscapes irrespective of the dominant pathway(s) (te Beest et al., ), although diploids appear particularly vulnerable when populations are small and fragmented (Pandit, ).…”

“…Diploid plant species are overrepresented among threatened species worldwide (Pandit, Pocock, & Kunin, ), suggesting that ploidy may be linked to species extinction risks and therefore differential diversity losses and plant community dynamics (Guignard et al., ; Šmarda et al., ). Hence, we hypothesize that interspecific variation in ploidy may influence plant species distributions and community composition in fragmented landscapes, over ecological time‐scales (Lumaret, Guillerm, Maillet, & Verlaque, ; Rosche et al., ). Aguilar et al.…”

“…This is unexpected, however, given the biological advantages which polyploids possess over diploids in attributes facilitating persistence in fragmented landscapes. For instance, autopolyploids experience slower decay of heterozygosity than diploids (Moody, Mueller, & Soltis, ; Soltis & Soltis, ), helping buffer detrimental population genetic effects of habitat loss and isolation, and therefore reducing extinctions caused by genetic erosion and inbreeding (Aguilar et al., ; Breed et al., ; Jacquemyn et al., ; Rosche et al., ). Moreover, heterosis effects may confer offspring vigour (Birchler, Yao, Chudalayandi, Vaiman, & Veitia, ), recessive deleterious alleles are easily masked (Otto & Whitton, ; Rosche et al., ; Soltis & Soltis, ) and, over longer evolutionary time‐scales, genes duplicated by polyploidy may develop new functions, enabling niche expansion or increasing flexibility to environmental change (Kirchheimer et al., ; Rosche et al., ), ultimately leading to speciation (Jiao et al., ).…”