Journal Article

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

Hensen, Isabell, Mráz, Patrik, Rosche, Christoph, Durka, Walter, Lachmuth, Susanne, Hartmann, Matthias

2017

Overview

1. 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). 2. 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. 3. 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. 4. 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.

• Publisher: John Wiley & Sons Ltd,Blackwell Publishing Ltd
• Subject: alleles / Centaurea / Centaurea stoebe / coefficient of relationship / Colonization / colonizing ability / cytotypes / diploidy / founder effect / founder effects / genetic bottleneck / genetic load / genetic markers / geocytotype / Inbreeding / inbreeding depression / Invasion ecology / Invasive species / loci / mutation / Nonnative species / Offspring / outcrossing / Plant reproduction / Polyploidy / progeny / purging / sporophytic self‐incompatibility / spotted knapweed / S‐alleles / tetraploidy