scholarly journals Parallel patterns of development between independent cases of hybrid seed inviability in Mimulus

2018 ◽  
Author(s):  
Jenn M. Coughlan ◽  
John H. Willis

SummaryRationaleHybrid seed inviability (HSI) is a common reproductive barrier in angiosperms, yet the evolutionary and developmental drivers of HSI remain largely unknown. We test whether conflict between maternal and paternal interests in resource allocation to developing offspring (i.e. parental conflict) are associated with HSI and determine the degree of developmental parallelism between independent incidences of HSI in Mimulus.MethodsWe quantified HSI between M. guttatus and two clades of M. decorus with oppositely asymmetric incompatibilities and surveyed development of hybrid and parental seeds.Key ResultsCrosses between M. guttatus and both clades of M. decorus show parent-of-origin effects on reciprocal F1 seed development, but in opposing directions. Inviable hybrid seeds exhibit paternal excess phenotypes, wherein endosperm is large and chaotic while viable hybrid seeds produce endosperm cells that are smaller and less prolific (i.e. maternal-excess phenotypes).Main ConclusionsWe find strong parent-of-origin effects on development in reciprocal F1s in multiple incidences of HSI in Mimulus. These patterns suggest that parental conflict may be an important force generating HSI in this group, and mismatches between maternal and paternal contributions to developing seeds result in repeatable developmental defects in hybrids.

2018 ◽  
Author(s):  
Jenn M. Coughlan ◽  
Maya Wilson Brown ◽  
John H. Willis

SummaryGenomic conflicts may play a central role in the evolution of reproductive barriers. Theory predicts that early-onset hybrid inviability may stem from conflict between parents for resource allocation to offspring. Here we describe M. decorus; a group of cryptic species within the M. guttatus species complex that are largely reproductively isolated by hybrid seed inviability (HSI). HSI between M. guttatus and M. decorus is common and strong, but populations of M. decorus vary in the magnitude and directionality of HSI with M. guttatus. Patterns of HSI between M. guttatus and M. decorus, as well as within M. decorus conform to the predictions of parental conflict: (1) reciprocal F1s exhibit size differences and parent-of-origin specific endosperm defects, (2) the extent of asymmetry between reciprocal F1 seed size is correlated with asymmetry in HSI, and (3) inferred differences in the extent of conflict predict the extent of HSI between populations. We also find that HSI is rapidly evolving, as populations that exhibit the most HSI are each others’ closest relative. Lastly, while all populations are largely outcrossing, we find that the differences in the inferred strength of conflict scale positively with π, suggesting that demographic or life history factors other than mating system may also influence the rate of parental conflict driven evolution. Overall, these patterns suggest the rapid evolution of parent-of-origin specific resource allocation alleles coincident with HSI within and between M. guttatus and M. decorus. Parental conflict may therefore be an important evolutionary driver of reproductive isolation.


2000 ◽  
Vol 12 (12) ◽  
pp. 2367-2381 ◽  
Author(s):  
Ramin Yadegari ◽  
Tetsu Kinoshita ◽  
Ofra Lotan ◽  
Gal Cohen ◽  
Anat Katz ◽  
...  

2016 ◽  
Vol 211 (1) ◽  
pp. 319-331 ◽  
Author(s):  
Austin G. Garner ◽  
Amanda M. Kenney ◽  
Lila Fishman ◽  
Andrea L. Sweigart

PLoS ONE ◽  
2008 ◽  
Vol 3 (9) ◽  
pp. e3131 ◽  
Author(s):  
Yanchun Li ◽  
Cintia M. Coelho ◽  
Tian Liu ◽  
Song Wu ◽  
Jiasheng Wu ◽  
...  

Development ◽  
2000 ◽  
Vol 127 (11) ◽  
pp. 2493-2502 ◽  
Author(s):  
S. Adams ◽  
R. Vinkenoog ◽  
M. Spielman ◽  
H.G. Dickinson ◽  
R.J. Scott

Some genes in mammals and flowering plants are subject to parental imprinting, a process by which differential epigenetic marks are imposed on male and female gametes so that one set of alleles is silenced on chromosomes contributed by the mother while another is silenced on paternal chromosomes. Therefore, each genome contributes a different set of active alleles to the offspring, which develop abnormally if the parental genome balance is disturbed. In Arabidopsis, seeds inheriting extra maternal genomes show distinctive phenotypes such as low weight and inhibition of mitosis in the endosperm, while extra paternal genomes result in reciprocal phenotypes such as high weight and endosperm overproliferation. DNA methylation is known to be an essential component of the parental imprinting mechanism in mammals, but there is less evidence for this in plants. For the present study, seed development was examined in crosses using a transgenic Arabidopsis line with reduced DNA methylation. Crosses between hypomethylated and wild-type diploid plants produced similar seed phenotypes to crosses between plants with normal methylation but different ploidies. This is consistent with a model in which hypomethylation of one parental genome prevents silencing of alleles that would normally be active only when inherited from the other parent - thus phenocopying the effects of extra genomes. These results suggest an important role for methylation in parent-of-origin effects, and by inference parental imprinting, in plants. The phenotype of biparentally hypomethylated seeds is less extreme than the reciprocal phenotypes of uniparentally hypomethylated seeds. The observation that development is less severely affected if gametes of both sexes (rather than just one) are ‘neutralized’ with respect to parent-of-origin effects supports the hypothesis that parental imprinting is not necessary to regulate development.


2015 ◽  
Author(s):  
Austin G Garner ◽  
Amanda M Kenney ◽  
Lila Fishman ◽  
Andrea L Sweigart

The classic finding in both flowering plants and mammals that hybrid lethality often depends on parent of origin effects suggests that divergence in the underlying loci might be an important source of hybrid incompatibilities between species. In flowering plants, there is now good evidence from diverse taxa that seed lethality arising from interploidy crosses is often caused by endosperm defects associated with deregulated imprinted genes. A similar seed lethality phenotype occurs in many crosses between closely related diploid species, but the genetic basis of this form of early-acting F1 postzygotic reproductive isolation is largely unknown. Here, we show that F1 hybrid seed lethality is an exceptionally strong isolating barrier between two closely related Mimulus species, M. guttatus and M. tilingii, with reciprocal crosses producing less than 1% viable seeds. Using a powerful crossing design and high-resolution genetic mapping, we identify both maternally- and paternally-derived loci that contribute to hybrid seed incompatibility. Strikingly, these two sets of loci are largely non-overlapping, providing strong evidence that genes with parent of origin effects are the primary driver of F1 hybrid seed lethality between M. guttatus and M. tilingii. We find a highly polygenic basis for both parental components of hybrid seed lethality suggesting that multiple incompatibility loci have accumulated to cause strong postzygotic isolation between these closely related species. Our genetic mapping experiment also reveals hybrid transmission ratio distortion and chromosomal differentiation, two additional correlates of functional and genomic divergence between species.


2000 ◽  
Vol 12 (12) ◽  
pp. 2367
Author(s):  
Ramin Yadegari ◽  
Tetsu Kinoshita ◽  
Ofra Lotan ◽  
Gal Cohen ◽  
Anat Katz ◽  
...  

Author(s):  
Jean-Philippe Vielle-Calzada ◽  
Ueli Grossniklaus ◽  
Charles Spillane

2021 ◽  
Author(s):  
Jenn M Coughlan

Hybrid Seed Inviability (HSI) is a common barrier in angiosperms. Recent work suggests that the rapid evolution of HSI may, in part, be due to conflict between maternal and paternal optima for resource allocation to developing offspring (i.e. parental conflict). However, parental conflict requires that paternally-derived resource acquiring alleles impose a maternal cost. I test this requirement using three closely related species in the Mimulus guttatus species complex that exhibit significant HSI and differ in their inferred histories of parental conflict. I show that the presence of hybrid seeds significantly affects conspecific seed size for almost all crosses, such that conspecific seeds are smaller after developing with hybrids from fathers with a stronger history of conflict, and larger after developing with hybrids from fathers with a weaker history of conflict. This work demonstrates a cost of paternally-derived alleles, and also has implications for species fitness in secondary contact.


2014 ◽  
Vol 9 (S 01) ◽  
Author(s):  
X Liu ◽  
M Scholz ◽  
A Tönjes ◽  
M Stumvoll ◽  
PF Stadler ◽  
...  

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