Mutations in two pollen self‐incompatibility factors in geographically marginal populations of <i>Solanum habrochaites</i> impact mating system transitions and reproductive isolation

Markova, Dragomira N.; Petersen, Jennifer J.; Qin, Xiaoqiong; Short, D.; Valle, Matthew J.; Tovar‐Méndez, Alejandro; McClure, Bruce; Chetelat, Roger T.

doi:10.3732/ajb.1600208

Cited by 21 publications

(49 citation statements)

References 81 publications

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“…) and Solanum habrochaites (Markova et al. ) populations. In the selfer A. thaliana , three different causal segregating SC mutations have been identified, possibly associated with distinct ancient glacial refugia (Shimizu et al.…”

Section: Discussionmentioning

confidence: 99%

“…Several lines of evidence suggest that the breakdown of SI has occurred in spatially structured populations in several plant species. For instance, North American populations of A. lyrata show multiple independent breakdowns of SI (Foxe et al 2010) and distinct SC mutations have been found across Leavenworthia alabamica and Solanum habrochaites (Markova et al 2016) populations. In the selfer A. thaliana, three different causal segregating SC mutations have been identified, possibly associated with distinct ancient glacial refugia (Shimizu et al 2008;Durvasula et al 2017;Tsuchimatsu et al 2017).…”

Section: Discussionmentioning

confidence: 99%

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Breakdown of gametophytic self‐incompatibility in subdivided populations

2020

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In many hermaphroditic flowering plants, self‐fertilization is prevented by self‐incompatibility (SI), often controlled by a single locus, the S‐locus. In single isolated populations, the maintenance of SI depends chiefly on inbreeding depression and the number of SI alleles at the S‐locus. In subdivided populations, however, population subdivision has complicated effects on both the number of SI alleles and the level of inbreeding depression, rendering the maintenance of SI difficult to predict. Here, we explore the conditions for the invasion of a self‐compatible mutant in a structured population. We find that the maintenance of SI is strongly compromised when a population becomes subdivided. We show that this effect is mainly caused by the decrease in the local diversity of SI alleles rather than by a change in the dynamics of inbreeding depression. Strikingly, we also find that the diversity of SI alleles at the whole population level is a poor predictor of the maintenance of SI. We discuss the implications of our results for the interpretation of empirical data on the loss of SI in natural populations.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Breakdown of gametophytic self‐incompatibility in subdivided populations

2020

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“…Of course, for self‐compatibility to spread throughout a species’ range, it must first become established locally, for example, in marginal populations (Busch ; Griffin and Willi ; Markova et al. ), potentially accompanied by the local purging of inbreeding depression (Busch ; Pujol et al. ).…”

Section: Discussionmentioning

confidence: 99%

“…Similarly, Stone et al (2014) found complete seed discounting in their study of selfcompatibility versus self-incompatibility in W. solanacea, as well as evidence for strong inbreeding depression in SC plants. Of course, for self-compatibility to spread throughout a species' range, it must first become established locally, for example, in marginal populations (Busch 2005b;Griffin and Willi 2014;Markova et al 2016), potentially accompanied by the local purging of inbreeding depression (Busch 2005a;Pujol et al 2009). With the purging of inbreeding depression in part of a species' range, self-compatibility may then spread more easily if at least some of the purged loci are linked to the locus conferring selfcompatibility, thus giving those alleles an additional advantage over those still carrying load in populations that are still SI (Uyenoyama 1997(Uyenoyama , 2004.…”

Section: Reproductive Assurance In Sc Plantsmentioning

confidence: 99%

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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“…Despite the loss of S-RNase , however, most SC populations of these wild species still exhibit UI against interspecific pollen, indicating UI can also have S-RNase-independent mechanisms. Nonetheless, the degree to which natural intraspecific variation in genes involved in SI might simultaneously affect interspecific isolation via UI remains to be directly investigated in most cases (but see Broz et al 2017, Markova et al 2016).…”

Section: Introductionmentioning

confidence: 99%

Intraspecific genetic variation underlying postmating reproductive barriers between species in the wild tomato clade (Solanumsect.Lycopersicon)

Jewell

Zhang

Gibson

et al. 2019

Preprint

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23A goal of speciation genetics is to understand how the genetic components underlying 24 interspecific reproductive barriers originate within species. Unilateral incompatibility (UI) is a 25 postmating prezygotic barrier in which pollen rejection in the female reproductive tract (style) 26 occurs in only one direction of an interspecific cross. Natural variation in the strength of UI has 27 been observed among populations within species in the wild tomato clade. In some cases, 28 molecular loci underlying self-incompatibility (SI) are associated with this variation in UI, but the 29 mechanistic connection between these intra-and inter-specific pollen rejection behaviors is 30 poorly understood in most instances. We generated an F 2 population between SI and SC 31 genotypes of a single species, Solanum pennellii, to examine the genetic basis of intraspecific 32 variation in the strength of UI against other species, and to determine whether loci underlying 33 SI are genetically associated with this variation. We found that F 2 individuals vary in the rate at 34 which UI rejection occurs. One large effect QTL detected for this trait co-localized with the SI-35 determining S-locus. Moreover, individuals that expressed S-RNase-the S-locus protein 36 involved in SI pollen rejection-in their styles had much more rapid UI responses compared to 37 those without S-RNase protein. Our analysis shows that intraspecific variation at mate choice 38 loci-in this case at loci that prevent self-fertilization-can contribute to variation in the 39 strength of interspecific isolation, including postmating prezygotic barriers. Understanding the 40 nature of such standing variation can provide insight into the accumulation of these barriers 41 between diverging lineages. 42 43 49reproducing organisms-reproductive isolation, among diverging lineages. Accordingly, loci that 50 contribute to this cumulative process between species must first arise within an individual 51 population prior to spreading to other conspecific populations within their own lineage. During 52 this process, populations of a single species are expected to show varying strengths of 53 reproductive isolation against other lineages; that is, there will be intraspecific genetic variation 54 for the magnitude of interspecific reproductive isolation from other lineages. Intraspecific 55 phenotypic variation in the strength of hybrid incompatibility has been observed in many 56 systems including mammals (Good, Handel and Nachman, 2007; Vyskočilová, Pražanová and 57 60 Sweigart, Mason and Willis, 2007). Understanding the nature, origin, and accumulation of this 61 variation, including the underlying molecular genetic variants responsible, can provide insight 62 into the evolutionary dynamics of lineage divergence (Cutter, 2012), including the order in 63 which alleles contributing to interspecific reproductive isolation arise and fix within diverging 64 lineages. 66The genetic basis of intraspecific variation for interspecific barriers has been 67 in...

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Mutations in two pollen self‐incompatibility factors in geographically marginal populations of Solanum habrochaites impact mating system transitions and reproductive isolation

Cited by 21 publications

References 81 publications

Breakdown of gametophytic self‐incompatibility in subdivided populations

Breakdown of gametophytic self‐incompatibility in subdivided populations

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

Intraspecific genetic variation underlying postmating reproductive barriers between species in the wild tomato clade (Solanumsect.Lycopersicon)

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