STRONG INBREEDING DEPRESSION IN TWO SCANDINAVIAN POPULATIONS OF THE SELF-INCOMPATIBLE PERENNIAL HERB<i>ARABIDOPSIS LYRATA</i>

Sletvold, Nina; Mousset, Mathilde; Hagenblad, Jenny; Hansson, Bengt; Ågren, Jon

doi:10.1111/evo.12174

Cited by 22 publications

(48 citation statements)

References 90 publications

(129 reference statements)

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“…These populations thus could be in a transition to inbreeding, possibly because of mate limitation, which has been suggested as a primary driver of transitions from outcrossing to inbreeding (Byers and Meagher, 1992; Vekemans et al , 1998, 2014). If mate limitation occurred during a colonisation bottleneck (that is, after the last ice age), high levels of biparental inbreeding could have purged deleterious mutations that maintain outcrossing in other parts of the range of A. lyrata (Sletvold et al , 2013). …”

Section: Discussionmentioning

confidence: 99%

What causes mating system shifts in plants? Arabidopsis lyrata as a case study

et al. 2016

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The genetic breakdown of self-incompatibility (SI) and subsequent mating system shifts to inbreeding has intrigued evolutionary geneticists for decades. Most of our knowledge is derived from interspecific comparisons between inbreeding species and their outcrossing relatives, where inferences may be confounded by secondary mutations that arose after the initial loss of SI. Here, we study an intraspecific breakdown of SI and its consequences in North American Arabidopsis lyrata to test whether: (1) particular S-locus haplotypes are associated with the loss of SI and/or the shift to inbreeding; (2) a population bottleneck may have played a role in driving the transition to inbreeding; and (3) the mutation(s) underlying the loss of SI are likely to have occurred at the S-locus. Combining multiple approaches for genotyping, we found that outcrossing populations on average harbour 5 to 9 S-locus receptor kinase (SRK) alleles, but only two, S1 and S19, are shared by most inbreeding populations. Self-compatibility (SC) behaved genetically as a recessive trait, as expected from a loss-of-function mutation. Bulked segregant analysis in SC × SI F2 individuals using deep sequencing confirmed that all SC plants were S1 homozygotes but not all S1 homozygotes were SC. This was also revealed in population surveys, where only a few S1 homozygotes were SC. Together with crossing data, this suggests that there is a recessive factor that causes SC that is physically unlinked to the S-locus. Overall, our results emphasise the value of combining classical genetics with advanced sequencing approaches to resolve long outstanding questions in evolutionary biology.

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Section: Discussionmentioning

confidence: 99%

What causes mating system shifts in plants? Arabidopsis lyrata as a case study

et al. 2016

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“…Given the complexity of our experimental design (including repeated herbivory trials), which logistically prohibited the estimation of more direct fitness measures, we limited our comparison of performance to germination rate and seedling performance (growth rate). Previous evidence in two populations of the European subspecies A. lyrata petraea had indicated the importance of early life history traits for inbreeding depression, with sig nificant inbreeding depression effects throughout the life cycle, but most pronounced effects (*60 %) for seed production (Sletvold et al 2013). In a single outcrossing pop ulation of North American A. lyrata, there was strong inbreeding depression (up to 40 %) for germination rate, and less severe but still significant inbreeding depression (up to 10 %) for relative growth rate (Stift et al 2013).…”

Section: Discussionmentioning

confidence: 97%

Costs associated with the evolution of selfing in North American populations of Arabidopsis lyrata?

2015

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Selfing can evolve if the transmission advantage of selfers outweighs the negative effects of inbreeding depression. It has been hypothesised that on the long term, selfing lineages are an evolutionary dead end, in part due to genetic degradation resembling that of Muller's ratchet in asexual lineages. There is a lack of empirical evidence for costs of selfing due to genetic degradation in recently evolved selfers. We tested whether such costs are apparent in recently established selfing populations of the generally outcrossing species Arabidopsis lyrata. Specifically, we compared selfing and outcrossing populations in their growth performance, and for traits that play a putative role in defence against herbivores. In line with our expectations, selfing populations had reduced germination rates, growth however was similar to outcrossing populations. Plants from selfing popu lations showed no consistent reduction in herbivore defence traits, and were equally palatable to caterpillars of the moth Mamestra brassicae. There were also no differences between outcrossers and selfers in phenotypic plasticity for putative defence traits and palatability after induction by herbivores. Overall, we interpret our results as showing some evidence for persistent costs of selfing due to drift or inbreeding load in terms of reduced seedling establishment, but providing no support for the hypothesis that selfing populations should be more susceptible to generalist herbivores, or rely more on induced defence.

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“…In European populations of A. lyrata (ssp. petraea ), which are all self‐incompatible and obligately outcrossing, inbreeding depression based on the same cumulative performance traits averaged δ per seed = 0.51 and δ per pollination = 0.81 (Sletvold et al ., ). Our results therefore suggest that the barrier to the evolution of higher selfing rates is lower in North American than in European outcrossing populations.…”

Section: Discussionmentioning

confidence: 97%

“…These methods most commonly involve bud self‐pollination (e.g. Busch, ; Sletvold et al ., ; Willi, ) or self‐pollination in a CO 2 ‐enriched environment (e.g. Stift et al ., and this paper).…”

Section: Discussionmentioning

confidence: 99%

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Relatively weak inbreeding depression in selfing but also in outcrossing populations of North American Arabidopsis lyrata

Carleial

Kleunen

Stift

2017

J of Evolutionary Biology

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Hermaphroditic plants can potentially self-fertilize, but most possess adaptations that promote outcrossing. However, evolutionary transitions to higher selfing rates are frequent. Selfing comes with a transmission advantage over outcrossing, but self-progeny may suffer from inbreeding depression, which forms the main barrier to the evolution of higher selfing rates. Here, we assessed inbreeding depression in the North American herb Arabidopsis lyrata, which is normally self-incompatible, with a low frequency of self-compatible plants. However, a few populations have become fixed for self-compatibility and have high selfing rates. Under greenhouse conditions, we estimated mean inbreeding depression per seed (based on cumulative vegetative performance calculated as the product of germination, survival and aboveground biomass) to be 0.34 for six outcrossing populations, and 0.26 for five selfing populations. Exposing plants to drought and inducing defences with jasmonic acid did not magnify these estimates. For outcrossing populations, however, inbreeding depression per seed may underestimate true levels of inbreeding depression, because self-incompatible plants showed strong reductions in seed set after (enforced) selfing. Inbreeding-depression estimates incorporating seed set averaged 0.63 for outcrossing populations (compared to 0.30 for selfing populations). However, this is likely an overestimate because exposing plants to 5% CO to circumvent self-incompatibility to produce selfed seed might leave residual effects of self-incompatibility that contribute to reduced seed set. Nevertheless, our estimates of inbreeding depression were clearly lower than previous estimates based on the same performance traits in outcrossing European populations of A. lyrata, which may help explain why selfing could evolve in North American A. lyrata.

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STRONG INBREEDING DEPRESSION IN TWO SCANDINAVIAN POPULATIONS OF THE SELF-INCOMPATIBLE PERENNIAL HERBARABIDOPSIS LYRATA

Cited by 22 publications

References 90 publications

What causes mating system shifts in plants? Arabidopsis lyrata as a case study

What causes mating system shifts in plants? Arabidopsis lyrata as a case study

Costs associated with the evolution of selfing in North American populations of Arabidopsis lyrata?

Relatively weak inbreeding depression in selfing but also in outcrossing populations of North American Arabidopsis lyrata

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