Species Selection Maintains Self-Incompatibility

Goldberg, Emma E.; Kohn, Joshua R.; Lande, Russell; Robertson, Kelly A.; Smith, Stephen A.; Igić, Boris

doi:10.1126/science.1194513

Cited by 431 publications

(509 citation statements)

References 33 publications

(6 reference statements)

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“…8c), suggesting that major diversification of the types predated separation of genera in Solanaceae. This is consistent with the extensive trans-specific polymorphism found in Solanaceae S-RNases 17,18 (Fig. 4b, Supplementary Fig.…”

Section: Allelic Slfs Are Much Younger Than S-rnase Alleles and Thansupporting

confidence: 88%

Gene duplication and genetic exchange drive the evolution of S-RNase-based self-incompatibility in Petunia

et al. 2015

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Self-incompatibility (SI) systems in flowering plants distinguish self-and non-self pollen to prevent inbreeding. While other SI systems rely on the self-recognition between specific male-and femaledeterminants, the Solanaceae family has a non-self recognition system resulting in the detoxification of female-determinants of S-ribonucleases (S-RNases), expressed in pistils, by multiple male-determinants of S-locus F-box proteins (SLFs), expressed in pollen. It is not known how many SLF components of this non-self recognition system there are in Solanaceae species, or how they evolved. We identified 16-20 SLFs in each S-haplotype in SI Petunia, from a total of 168 SLF sequences using large-scale nextgeneration sequencing and genomic polymerase chain reaction (PCR) techniques. We predicted the target S-RNases of SLFs by assuming that a particular S-allele must not have a conserved SLF that recognizes its own S-RNase, and validated these predictions by transformation experiments. A simple mathematical model confirmed that 16-20 SLF sequences would be adequate to recognize the vast majority of target S-RNases. We found evidence of gene conversion events, which we suggest are essential to the constitution of a non-self recognition system and also contribute to self-compatible mutations. Self-incompatibility (SI) systems in flowering plants distinguish self and non-self pollen to prevent inbreeding. While all other SI systems studied to date rely on the self-recognition between each single male-and female-determinants, the Solanaceae plants has a non-self recognition system that functions through the detoxification of non-self female-determinants of S-ribonucleases (S-RNases), expressed in pistils, by multiple male-determinants of S-locus F-box proteins (SLFs), expressed in pollen.However, little is known about how many SLF components constitute such a non-self recognition system and how they evolve. Here we conducted large-scale next-generation sequencing and genomic PCR and identified 16-20 SLFs in each S-haplotype in SI Petunia, for a total of 168 SLF sequences. We predicted the target S-RNases of SLFs by assuming that a particular S-allele must not have a conserved SLF that recognizes its own S-RNase, and validated them by transformation experiments. A simple mathematical model showed that 16-20 SLF sequences would be adequate to recognize the vast majority of target S-RNases. We found evidence of gene conversion events, which we suggest are essential to constitute a non-self recognition system and as well as contributed to self-compatible mutations.SI is a genetically controlled reproductive barrier in angiosperms that allows the pistil to reject self (genetically-related) pollen and accept non-self (genetically-unrelated) pollen [1][2][3][4] . In most cases, this self/non-self discrimination is controlled by male-and

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Section: Allelic Slfs Are Much Younger Than S-rnase Alleles and Thansupporting

confidence: 88%

Gene duplication and genetic exchange drive the evolution of S-RNase-based self-incompatibility in Petunia

et al. 2015

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“…Transitions in locomotory and life history strategies are important traits that may underlie major shifts in diversification (Leclère et al ., 2009; Goldberg et al ., 2010; Ikeda et al ., 2012; Cieslak et al ., 2014; de Vos et al ., 2014). Changes in life history may also drive shifts in locomotion (or vice versa) to optimally match these traits, which are often linked in microbial eukaryotes (Hoek et al ., 1995).…”

Section: Discussionmentioning

confidence: 99%

“…Numerous life history traits have been linked to net diversification (birth − death, r = b − d ) in vascular plants. These include features associated with longevity (annual vs perennial, Drummond et al ., 2012), seed dispersal (Leslie et al ., 2013; Beaulieu & O'Meara, 2016) and mechanisms that promote outcrossing, such as self‐incompatibility (Goldberg et al ., 2010) and heterostyly (de Vos et al ., 2014). Similar patterns are also evident in animals.…”

Section: Introductionmentioning

confidence: 99%

Accelerated diversification is related to life history and locomotion in a hyperdiverse lineage of microbial eukaryotes (Diatoms, Bacillariophyta)

2018

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Summary Patterns of species richness are commonly linked to life history strategies. In diatoms, an exceptionally diverse lineage of photosynthetic heterokonts important for global photosynthesis and burial of atmospheric carbon, lineages with different locomotory and reproductive traits differ dramatically in species richness, but any potential association between life history strategy and diversification has not been tested in a phylogenetic framework.We constructed a time‐calibrated, 11‐gene, 1151‐taxon phylogeny of diatoms – the most inclusive diatom species tree to date. We used this phylogeny, together with a comprehensive inventory of first–last occurrences of Cenozoic fossil diatoms, to estimate ranges of expected species richness, diversification and its variation through time and across lineages.Diversification rates varied with life history traits. Although anisogamous lineages diversified faster than oogamous ones, this increase was restricted to a nested clade with active motility in the vegetative cells.We propose that the evolution of motility in vegetative cells, following an earlier transition from oogamy to anisogamy, facilitated outcrossing and improved utilization of habitat complexity, ultimately leading to enhanced opportunity for adaptive divergence across a variety of novel habitats. Together, these contributed to a species radiation that gave rise to the majority of present‐day diatom diversity.

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“…Compared to self‐fertilization, outcrossing entails substantial costs, including the twofold cost of males or the cost of meiosis (Lively & Lloyd, 1990; Maynard Smith, 1978; Williams, 1975). The ubiquity of outcrossing in the face of such costs suggests that outcrossing lineages enjoy significant benefits over evolutionary time, relative to selfing (Goldberg et al., 2010) or asexual lineages (Bell, 1982; Maynard Smith, 1978). The Red Queen hypothesis predicts that host–parasite coevolution can favor the long‐term maintenance of outcrossing (Bell, 1982; Hamilton, 1980; Jaenike, 1978).…”

Section: Introductionmentioning

confidence: 99%

Turnover in local parasite populations temporarily favors host outcrossing over self‐fertilization during experimental evolution

Lynch

Penley

Morran

2018

Ecology and Evolution

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The ubiquity of outcrossing in plants and animals is difficult to explain given its costs relative to self‐fertilization. Despite these costs, exposure to changing environmental conditions can temporarily favor outcrossing over selfing. Therefore, recurring episodes of environmental change are predicted to favor the maintenance of outcrossing. Studies of host–parasite coevolution have provided strong support for this hypothesis. However, it is unclear whether multiple exposures to novel parasite genotypes in the absence of coevolution are sufficient to favor outcrossing. Using the nematode Caenorhabditis elegans and the bacterial parasite Serratia marcescens, we studied host responses to parasite turnover. We passaged several replicates of a host population that was well‐adapted to the S. marcescens strain Sm2170 with either Sm2170 or one of three novel S. marcescens strains, each derived from Sm2170, for 18 generations. We found that hosts exposed to novel parasites maintained higher outcrossing rates than hosts exposed to Sm2170. Nonetheless, host outcrossing rates declined over time against all but the most virulent novel parasite strain. Hosts exposed to the most virulent novel strain exhibited increased outcrossing rates for approximately 12 generations, but did not maintain elevated levels of outcrossing throughout the experiment. Thus, parasite turnover can transiently increase host outcrossing. These results suggest that recurring episodes of parasite turnover have the potential to favor the maintenance of host outcrossing. However, such maintenance may require frequent exposure to novel virulent parasites, rapid rates of parasite turnover, and substantial host gene flow.

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Species Selection Maintains Self-Incompatibility

Cited by 431 publications

References 33 publications

Gene duplication and genetic exchange drive the evolution of S-RNase-based self-incompatibility in Petunia

Gene duplication and genetic exchange drive the evolution of S-RNase-based self-incompatibility in Petunia

Accelerated diversification is related to life history and locomotion in a hyperdiverse lineage of microbial eukaryotes (Diatoms, Bacillariophyta)

Turnover in local parasite populations temporarily favors host outcrossing over self‐fertilization during experimental evolution

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