A two-locus hybrid incompatibility is widespread, polymorphic, and active in natural populations of <i>Mimulus</i>

Zuellig, Matthew P.; Sweigart, Andrea L.

doi:10.1101/339986

Cited by 10 publications

(20 citation statements)

References 40 publications

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“…Many case studies of RI are conducted across short time spans, yet shifting environmental conditions can affect the relative importance of different pre-pollination barriers in different years (Briscoe Runquist et al 2014;Roccaforte et al 2015). Similarly, population specific loci may be responsible for intrinsic incompatibility (Sweigart and Flagel 2015;Zuellig and Sweigart 2018), so crossing results from specific population pairs may not accurately extend to the species level, particularly when demographic or environmental interactions drive these outcomes (Barnard-Kubow and Galloway 2017). The potentially transitory nature of isolating barriers (we observed prezygotic variability between years, and postzygotic variability across space), as well as possible error in empirical data used to calculate mean estimates of RI, motivated us to further explore the ramifications of barrier strength uncertainty using a bootstrapping approach.…”

Section: Species Boundariesmentioning

confidence: 99%

Reproductive isolation and the maintenance of species boundaries in two serpentine endemic Jewelflowers

Christie

Strauss

2019

Evolution

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Speciation occurs when reproductive barriers substantially reduce gene flow between lineages. Understanding how specific barriers contribute to reproductive isolation offers insight into the initial forces driving divergence and the evolutionary and ecological processes responsible for maintaining diversity. Here, we quantified multiple pre‐ and post‐pollination isolating barriers in a pair of closely related California Jewelflowers (Streptanthus, Brassicaceae) living in an area of sympatry. S. breweri and S. hesperidis are restricted to similar serpentine habitats; however, populations are spatially isolated at fine‐scales and rarely co‐occur in intermixed stands. Several intrinsic postzygotic barriers were among the strongest we quantified, yet, postzygotic barriers currently contribute little to overall reproductive isolation due to the cumulative strength of earlier‐acting extrinsic barriers, including spatial isolation, and flowering time and pollinator differences. Data from multiple years suggest that pre‐pollination barriers may have different strengths depending on annual environmental conditions. Similarly, crossing data suggest that the strength of intrinsic isolation may vary among different population pairs. Estimates of total reproductive isolation in S. breweri and S. hesperidis are robust to uncertainty and variability in individual barrier strength estimates, demonstrating how multiple barriers can act redundantly to prevent gene flow between close relatives living in sympatry.

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Section: Species Boundariesmentioning

confidence: 99%

Reproductive isolation and the maintenance of species boundaries in two serpentine endemic Jewelflowers

Christie

Strauss

2019

Evolution

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“…Further, it also suggests that the crossing barrier has been degraded in sympatry. This result is significant because, although the degradation of reproductive isolation in sympatry is supported by theory (Barton and Hewitt 1985, Butlin 1987, Virdee and Hewitt 1994, Kelly and Noor 1996) and is implied by patterns of genetic variation in many systems (e.g., Borge et al 2005, Sander et al 2014), studies in which the strength of reproductive barriers have been explicitly quantified and shown to be degraded in sympatry are rare (but see Carney et al 2000, Collins and Rawlins 2013, Virdee and Hewitt 1994, Saetre et al 1999, 2003, Zuellig and Sweigart 2019).…”

Section: Resultsmentioning

confidence: 99%

Morning glory species co-occurrence is associated with asymmetrically decreased and cascading reproductive isolation

Ostevik

Rifkin

Xia

et al. 2019

Preprint

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1The interplay between hybridization and reproductive isolation is critical to the origin and 2 maintenance of species. Hybridization between species is known to affect reproductive barrier 3 strength. An extension of this relationship is the expectation that asymmetric hybridization and gene 4 flow will have asymmetric effects on reproductive barrier strength. We tested this hypothesis in a pair 5 of morning glory species which exhibit asymmetric gene flow in sympatry from highly selfing Ipomoea 6 lacunosa into mixed mating I. cordatotriloba. Because of the direction of hybridization, we predicted 7 that reproductive barrier strength would change to a greater extent in I. cordatotriloba than I. 8 lacunosa. We tested this prediction by measuring the strength of a barrier to seed set between these 9 species across their ranges. Consistent with our prediction, we found that sympatric I. cordatotriloba 10 was more compatible with range-wide I. lacunosa than allopatric I. cordatotriloba, whereas sympatric 11 and allopatric I. lacunosa were equally compatible with I. cordatotriloba. This difference likely reflects 12 an asymmetric decrease in reproductive barriers in sympatric I. cordatotriloba. We further 13 demonstrated that changes to sympatric I. cordatotriloba have decreased compatibility with allopatric 14 populations. Thus, in a manner analogous to cascade reinforcement, introgression associated with 15 asymmetric hybridization not only influences between-species isolation but also contributes to 16 isolation within a species. 17 18 Introduction 19 Reproductive barriers are fundamental to the evolution and maintenance of biological diversity. They 20 maintain the integrity of species by preventing the homogenizing effect of gene flow. However, 21 incomplete reproductive isolation is common, and consequently hybridization between species in 22 sympatry is frequent (Mallet 2005, Whitney et al. 2010). When hybridization occurs, it can affect the 23 reproductive barriers that separate species, which, in turn, affects the potential for future 24 hybridization between those species. Species that initially hybridize in sympatry may collapse into a 25 single species, complete speciation by undergoing reinforcement, or coexist in stable hybrid zones 26 (Abbott et al. 2013, Todesco et al. 2016). Whether reproductive isolation increases, decreases, or 27 remains unchanged during hybridization thus determines species boundaries in contact zones. 28 29Hybridization affects reproductive barrier strength in two major ways: by homogenizing genotypes 30 and traits and through interactions with natural selection. First, hybridization that results in 31 introgression can cause traits that were previously differentiated between species to converge. If 32 those traits underlie reproductive barriers, the strength of reproductive isolation between species will 33 change. For example, when a trait that causes assortative mating on its own (e.g., self-referential 34 mating preferences, selfing) spreads to a new species, reproductive...

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“…It is presumed that purifying selection may also be helpful for polymorphism. Hl13 and hl14 cause hybrid lethality between Mimulus guttatus and M. nasutus and both loci are polymorphic in the two species (Zuellig and Sweigart, 2018). The incompatibility alleles are maintained for decades.…”

Section: Discussionmentioning

confidence: 99%

“…Barriers that lead to RI are classified as pre- or postzygotic for practical (Baack et al, 2015; Futuyma, 2013; Lafon-Placette et al, 2016; Rieseberg and Willis, 2007; Widmer et al, 2009). Many genes related to RI have been identified in various species (Fishman and Sweigart, 2018; Masly et al, 2006; Nadir et al, 2018; Ouyang and Zhang, 2018; Zuellig and Sweigart, 2018), yet studies that aim to elucidate the evolutionary histories of RI genes are still rare.…”

Section: Introductionmentioning

confidence: 99%

Independent domestications shape the genetic pattern of a reproductive isolation system in rice

Zhang

2020

Preprint

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14Severe reproductive isolation (RI) exists between the two subspecies of rice, 15 Indica and Japonica, but in the wild ancestors no post-zygotic RI was found. The 16 studies about the establishment of the interspecies RI of rice are still rear. A pair of 17 rice hybrid sterility genes, DOPPELGANGER 1 (DPL1) and DOPPELGANGER 2 18 (DPL2), offers a convenient example to study the evolutionary history of RI genes. 19 Either of the two loci has one non-functional allele . The hybrid 20 pollen carrying both DPL1-and DPL2-will be sterility. 21 We collected 811 individuals: Oryza sativa (132), the two wild ancestors O. 22 nivara (296) and O. rufipogon (383) as well as 20 DPL1 and 34 DPL2 sequences of O. 23 sativa from on-line databases. We analysed the genetic and geographic pattern of 24DPLs in all three species to determine the origination regions of DPL1-and DPL2-. 25 The neutral test as well as the diversities of nucleotide and haplotype were used to 26 detect if selection shaped the pattern of DPLs. 27 We found that DPL1-and DPL2-of rice emerged from wild ancestor populations 28 in South Asia and South China through two respective domestications. Comparing 29 with the ancestral populations, DPL1-and DPL2-both showed reduce of diversities, 30 however their frequencies increased in rice. We assume that the reduce of diversities 31 due to the bottleneck effect of domestication while the loss of one copy was preferred 32 by artificial selection for cost savings. 33Reproductive isolation (RI) is considered a failure to transmit genetic materials 36 (Futuyma, 2013). Barriers that lead to RI are classified as pre-or postzygotic for 37 practical (Baack et al, 2015; Futuyma, 2013; Lafon-Placette et al, 2016; Rieseberg 38 and Willis, 2007; Widmer et al, 2009). Many genes related to RI have been identified 39 in various species (Fishman and Sweigart, 2018; Masly et al, 2006; Nadir et al, 2018; 40 Ouyang and Zhang, 2018; Zuellig and Sweigart, 2018), yet studies that aim to 41 elucidate the evolutionary histories of RI genes are still rare. 42 Rice (Oryza sativa) is an important crop as well as a model species. Strong 43 postzygotic RI was found between two subspecies of rice, Japonica and Indica. Many 44 loci answering for the hybrid incompatibility have been found (Ouyang et al, 2010; 45 Wang et al, 2014). Hundreds of loci were found related to hybrid incompatibility, 46 indicating that the incompatibility between Japonica and Indica has a complex 47 48 detected: S5 (Chen et al, 2008; Yang et al, 2012b), Sa (Long et al, 2008) and DPLs 49 (Mizuta et al, 2010). S5 leads to endoplasmic reticulum stress. Sa and DPLs both lead 50 to hybrid pollen sterility. On the contrary, the two wild ancestors of rice, O. nivara 51 and O. rufipogon, are compatible (Cai et al, 2019). Rice and the two wild ancestors 52 constitute a excellent system for studying the evolution history of RI genes. 53The DPL system offers a suitable example for exploring this phenomenon. The 54 DPL system contains only two genes, DOPPELGANGER 1 (DPL1)...

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A two-locus hybrid incompatibility is widespread, polymorphic, and active in natural populations of Mimulus

Cited by 10 publications

References 40 publications

Reproductive isolation and the maintenance of species boundaries in two serpentine endemic Jewelflowers

Reproductive isolation and the maintenance of species boundaries in two serpentine endemic Jewelflowers

Morning glory species co-occurrence is associated with asymmetrically decreased and cascading reproductive isolation

Independent domestications shape the genetic pattern of a reproductive isolation system in rice

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