The divergence history of the perennial plant <i>Linaria cavanillesii</i> confirms a recent loss of self‐incompatibility

Voillemot, Marie; Rougemont, Quentin; Roux, Camille; Pannell, John R.

doi:10.1111/jeb.13209

Cited by 5 publications

(9 citation statements)

References 123 publications

(155 reference statements)

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“…This second possibility would be consistent with the observation that populations of L. cavanillesii are extremely isolated from one another, with F ST between 0.56 and 0.75 (Voillemot and Pannell ), implying that there has been no gene flow between the SC and SI population for a long time (Voillemot et al. ). Moreover, individuals in some of the SI populations of L. cavanillesii show incomplete self‐incompatibility (Voillemot and Pannell ), yet selfing appears not to have increased in frequency in these populations.…”

Section: Discussionsupporting

confidence: 81%

“…; Voillemot et al. ), perhaps in response to selection for reproductive assurance or after a series of population bottlenecks that purged the population of its inbreeding depression (Kirkpatrick and Jarne ; Guo et al. ; Foxe et al.…”

Section: Discussionmentioning

confidence: 99%

“…It thus seems likely that self‐compatibility in L. cavanillesii evolved recently (Voillemot et al. ), so that there may have been sufficient time for the purging of inbreeding depression but not for the evolution of a selfing syndrome.…”

Section: Methodsmentioning

confidence: 99%

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Rapid loss of self‐incompatibility in experimental populations of the perennial outcrossing plantLinaria cavanillesii

2019

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Transitions from self‐incompatibility to self‐compatibility in angiosperms may be frequently driven by selection for reproductive assurance when mates or pollinators are rare, and are often succeeded by loss of inbreeding depression by purging. Here, we use experimental evolution to investigate the spread of self‐compatibility from one such population of the perennial plant Linaria cavanillesii into self‐incompatible (SI) populations that still have high inbreeding depression. We introduced self‐compatible (SC) individuals at different frequencies into replicate experimental populations of L. cavanillesii that varied in access to pollinators. Our experiment revealed a rapid shift to self‐compatibility in all replicates, driven by both greater seed set and greater outcross siring success of SC individuals. We discuss our results in the light of computer simulations that confirm the tendency of self‐compatibility to spread into SI populations under the observed conditions. Our study illustrates the ease with which self‐compatibility can spread among populations, a requisite for species‐wide transitions from self‐incompatibility to self‐compatibility.

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Section: Discussionsupporting

confidence: 81%

Section: Discussionmentioning

confidence: 99%

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Rapid loss of self‐incompatibility in experimental populations of the perennial outcrossing plantLinaria cavanillesii

2019

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“…By selfing, the incidence of deleterious alleles is expected to rise, but this can be overcome through DNA purging, for example due to bottlenecks after extreme environmental events (Cooper and Cooper 1995). Furthermore, plant phylogenies clearly showed that plants transitioned from self-incompatibility to self-compatibility multiple times, independently (Igic et al 2008;Goldberg et al 2010), and this is even confirmed by cases of recent acquisition of the selfing (Voillemot et al 2018). These aspects indicate the adaptive nature of the selfing trait, that could be advantageous at least in the short term (Cheptou 2019).…”

Section: Introductionmentioning

confidence: 99%

Investigating pollination strategies in disturbed habitats: the case of the narrow-endemic toadflax Linaria tonzigii (Plantaginaceae) on mountain screes

et al. 2021

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Plant mating systems may reflect an adaptation to a habitat type, with self-pollination being potentially common in unstable and disturbed conditions. We investigated the reproductive ecology of an Alpine, narrow-range toadflax, Linaria tonzigii Lona (Plantaginaceae), occurring in steep and dynamic mountain screes. We explored self-compatibility and spontaneous autogamy, seed viability, daily nectar production, pollinator behaviour and pollen transfer in wild populations, using hand pollination treatments, quantification of nectar volume, viability Tetrazolium assay, active pollinator sampling and video recordings, and UV-bright dust for pollen substitution. After ex novo sequencing of several genetic regions of L. tonzigii, we performed a multi-marker phylogenetic analysis of 140 Linaria species and tracked the occurrence of the self-compatibility trait. Our results showed that this species is self-compatible, pollinated mostly via spontaneous autogamy and pollinator-mediated geitonogamy, and self-pollinated seeds are as viable as cross-pollinated ones. Selfing could be due to pollinator rarity because, despite the studied species providing a high nectar volume, wild bees, moths and small beetles infrequently visited its flowers in the sparsely vegetated scree slopes. In addition, a preliminary survey showed a low genetic haplotype diversity in the study plant. Moreover, the phylogeny shows that self-compatibility is scattered in the tree, suggesting the adaptive nature of this reproductive trait in the genus Linaria. This study supports for theories that high prevalence of selfing is an adaptation to environments unfavourable for cross-pollination, and particularly where pollinators are rare, such as in perturbed, poorly vegetated high-elevation habitats.

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“…It would be especially informative to compare estimates of outcrossing rates and inbreeding depression in the three known SC lineages ( T. barbata and T. coronopifolia with highly developed selfing syndromes and the undescribed species with slightly smaller floral parts) with SI plants (Crawford et al, 2008, 2019). Voillemot et al (2018) showed that a recent transition to SC in Linaria cavanillesii (Plantaginaceae) occurred without development of the selfing syndrome and that the population had a mixed mating system rather than being highly selfing. In addition, there was high inbreeding depression in an SI population, but it was not detectable in the aforementioned SC population (Voillemot and Pannell, 2017).…”

Section: Discussionmentioning

confidence: 99%

Genome‐wide genotyping estimates mating system parameters and paternity in the island species Tolpis succulenta

Gibson

Crawford

Holder

et al. 2020

American J of Botany

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Premise The mating system has profound consequences, not only for ecology and evolution, but also for the conservation of threatened or endangered species. Unfortunately, small populations are difficult to study owing to limits on sample size and genetic marker diversity. Here, we estimated mating system parameters in three small populations of an island plant using genomic genotyping. Although self‐incompatible (SI) species are known to often set some self‐seed, little is known about how “leaky SI” affects selfing rates in nature or the role that multiple paternity plays in small populations. Methods We generalized the BORICE mating system program to determine the siring pattern within maternal families. We applied this algorithm to maternal families from three populations of Tolpis succulenta from Madeira Island and genotyped the progeny using RADseq. We applied BORICE to estimate each individual offspring as outcrossed or selfed, the paternity of each outcrossed offspring, and the level of inbreeding of each maternal plant. Results Despite a functional self‐incompatibility system, these data establish T. succulenta as a pseudo‐self‐compatible (PSC) species. Two of 75 offspring were strongly indicated as products of self‐fertilization. Despite selfing, all adult maternal plants were fully outbred. There was high differentiation among and low variation within populations, consistent with a history of genetic isolation of these small populations. There were generally multiple sires per maternal family. Twenty‐two percent of sib contrasts (between outcrossed offspring within maternal families) shared the same sire. Conclusions Genome‐wide genotyping, combined with appropriate analytical methods, enables estimation of mating system and multiple paternity in small populations. These data address questions about the evolution of reproductive traits and the conservation of threatened populations.

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The divergence history of the perennial plant Linaria cavanillesii confirms a recent loss of self‐incompatibility

Cited by 5 publications

References 123 publications

Rapid loss of self‐incompatibility in experimental populations of the perennial outcrossing plantLinaria cavanillesii

Rapid loss of self‐incompatibility in experimental populations of the perennial outcrossing plantLinaria cavanillesii

Investigating pollination strategies in disturbed habitats: the case of the narrow-endemic toadflax Linaria tonzigii (Plantaginaceae) on mountain screes

Genome‐wide genotyping estimates mating system parameters and paternity in the island species Tolpis succulenta

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