Invasion success in polyploids: the role of inbreeding in the contrasting colonization abilities of diploid versus tetraploid populations of Centaurea stoebe s.l. (25th October 2016)

• Record Type: Journal Article
• Authors: Rosche, Christoph; Hensen, Isabell; Mráz, Patrik; Durka, Walter; Hartmann, Matthias; Lachmuth, Susanne
• Editors: Bonser, Stephen
• Is Part Of: Journal of ecology. Volume 105:Number 2(2017:Mar.)
• Page Start: 425
• Page End: 435
• Publication Date: 2016-10-25
• Subjects: coefficient of relationship -- founder effects -- genetic bottleneck -- geocytotype -- inbreeding depression -- invasion ecology -- purging -- S‐alleles -- sporophytic self‐incompatibility -- spotted knapweed; Plant ecology -- Periodicals; 577.05
• DOI: 10.1111/1365-2745.12670
• Languages: English
• ISSNs: 0022-0477

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. Abstract : Centaurea stoebe comprises two cytotypes: Diploids prevail over tetraploids in the native range, whereas exclusively tetraploids became invasive. We conducted a breeding experiment and found striking results that contribute to explaining this drastic cytotype shift. In particular, we highlight the considerably reduced inbreeding depression in tetraploids as compared to diploids, which may increase the probability of tetraploid founder populations to outlast phases of demographic disequilibrium.