Disruption of endosperm development is a major cause of hybrid seed inviability between <i>Mimulus guttatus</i> and <i>Mimulus nudatus</i>

Oneal, Elen; Willis, John H.; Franks, Robert G.

doi:10.1111/nph.13842

Cited by 74 publications

(98 citation statements)

References 80 publications

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“…Adding support to this idea, a similar hybrid inviability phenotype (i.e. shriveled, collapsed hybrid seeds) in a different Mimulus cross ( M. guttatus × M. nudatus ) was recently shown to be the result of disrupted endosperm development (Oneal et al ., ). To determine if our measure of seed viability is correlated with germination rate, we planted the seeds from a single fruit for crosses within parental lines ( n = 2 each) and for a subset of our F 2 × parental crosses ( n = 20; see Fig.…”

Section: Methodsmentioning

confidence: 97%

Genetic loci with parent‐of‐origin effects cause hybrid seed lethality in crosses between Mimulus species

et al. 2016

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SummaryIn flowering plants, F 1 hybrid seed lethality is a common outcome of crosses between closely related diploid species, but the genetic basis of this early-acting and potentially widespread form of postzygotic reproductive isolation is largely unknown.We intercrossed two closely related species of monkeyflower, Mimulus guttatus and Mimulus tilingii, to characterize the mechanisms and strength of postzygotic reproductive isolation. Then, using a reciprocal backcross design, we performed high-resolution genetic mapping to determine the genetic architecture of hybrid seed lethality and directly test for loci with parent-of-origin effects.We found that F 1 hybrid seed lethality is an exceptionally strong isolating barrier between Mimulus species, with reciprocal crosses producing < 1% viable seeds. This form of postzygotic reproductive isolation appears to be highly polygenic, indicating that multiple incompatibility loci have accumulated rapidly between these closely related Mimulus species. It is also primarily caused by genetic loci with parent-of-origin effects, suggesting a possible role for imprinted genes in the evolution of Mimulus hybrid seed lethality.Our findings suggest that divergence in loci with parent-of-origin effects, which is probably driven by genomic coevolution within lineages, might be an important source of hybrid incompatibilities between flowering plant species.

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Section: Methodsmentioning

confidence: 97%

Genetic loci with parent‐of‐origin effects cause hybrid seed lethality in crosses between Mimulus species

et al. 2016

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“…Inviable hybrid seeds are morphologically distinct from aborted ovules and can be readily distinguished by eye (Oneal et al. ). Lowry et al.…”

Section: Introductionmentioning

confidence: 99%

“…The Mimulus guttatus species complex (section Simiolus, Phrymaceae), a group of closely related riparian wildflower species, is a classic system for investigating the evolution and ecology of crossing barriers (Vickery 1978. F1 hybrid seed lethality is a major isolating barrier between the broadly sympatric species M. nudatus and M. guttatus (Gardner 1995, Gardner and MacNair 2000, Oneal et al 2016). Endosperm does not develop in hybrid seeds, which have a characteristic flat or shriveled shape and very rarely germinate (Gardner 1995, Oneal et al 2016.…”

Section: Introductionmentioning

confidence: 99%

“…F1 hybrid seed lethality is a major isolating barrier between the broadly sympatric species M. nudatus and M. guttatus (Gardner 1995, Gardner and MacNair 2000, Oneal et al 2016). Endosperm does not develop in hybrid seeds, which have a characteristic flat or shriveled shape and very rarely germinate (Gardner 1995, Oneal et al 2016. Inviable hybrid seeds are morphologically distinct from aborted ovules and can be readily distinguished by eye (Oneal et al 2016).…”

Section: Introductionmentioning

confidence: 99%

“…Endosperm does not develop in hybrid seeds, which have a characteristic flat or shriveled shape and very rarely germinate (Gardner 1995, Oneal et al 2016. Inviable hybrid seeds are morphologically distinct from aborted ovules and can be readily distinguished by eye (Oneal et al 2016). Lowry et al (2008) estimated the strength of this reproductive isolating barrier as 0.958.…”

Section: Introductionmentioning

confidence: 99%

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Hybrid inviability and differential submergence tolerance drive habitat segregation between two congeneric monkeyflowers

Toll

Willis

2018

Ecology

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Closely related, ecologically similar species are often separated at small geographic scales while being broadly sympatric. Both adaptation to abiotic environmental conditions and a variety of biotic interactions may determine small‐scale allopatry. In Northern California's coast range, two monkeyflower species, Mimulus guttatus and Mimulus nudatus, can co‐occur within local sites but rarely overlap at fine spatial scales, even though they are often separated by less than 1 m. M. guttatus naturally grows in wetter areas and is often submerged for up to four months of the year, while M. nudatus naturally occupies drier sites. We used a combination of observational data, reciprocal transplant, and laboratory experiments to test a series of biotic and abiotic hypotheses for the observed distribution pattern. Although M. guttatus can tolerate dry hillside conditions like those in which M. nudatus occurs, M. nudatus is unable to survive submerged for more than a week, limiting its distribution from seasonal streams inundated for months and dominated by M. guttatus. While herbivores did not differentially damage species, transplants were more likely to be damaged in M. guttatus’ seep habitat and M. nudatus was less tolerant to herbivory. Individuals of each species transplanted into populations of heterospecific congeners produced large proportions (up to 80%) of inviable seeds resulting from increased hybridization rates in close sympatry. Mimulus nudatus’ inability to tolerate submergence and herbivory establishes some degree of habitat association, and then, hybrid seed inviability reduces the ability of the locally rarer species to persist within the congener's microhabitat and maintains habitat segregation. Together these data show that both environmental filtering and biotic interactions shape the fine‐scale distribution of close relatives.

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Pre‐pollination barriers between two sympatric Arisaema species in northern Shikoku Island, Japan

Matsumoto

Miyazaki

Sueyoshi

et al. 2019

American J of Botany

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The genus Arisaema (Araceae) has rapidly diversified in Japan, and multiple species often coexist in the field. Although Japanese Arisaema species hybridize from artificial crossing, hybrid individuals are rare in mixed populations; suggesting the presence of effective pre-pollination barriers. We examined the following reproductive barriers between A. sikokianum and A. tosaense: habitat, phenology, and pollinator isolations. METHODS:Habitat isolation was examined by interspecific comparisons of microhabitat conditions at a mixed site and of altitude at the sampling site of herbarium specimens. Phenological isolation was evaluated by comparing seasonal transition in apparent spathe condition and frequency of insect visitation. Pollinator isolation was examined by comparing floral visitor assemblages between the two Arisaema species. To avoid overestimation of pollinator isolation due to seasonal changes in insect assemblages, we also compared visitor assemblages between natural and late-flowering A. sikokianum, where the latter was experimentally introduced and blooming with a natural A. tosaense population. RESULTS:Microhabitat conditions and sampling elevations of herbarium specimens overlapped between the two Arisaema species. At the population level, A. sikokianum and A. tosaense flowered for 39 and 52 days, respectively, with 13 days overlap. Insect visitation in A. sikokianum decreased before the seasonal overlap. Floral visitor assemblages differed between the two Arisaema species, while the difference between natural and lateflowering A. sikokianum was less distinct. CONCLUSIONS:Phenological and pollinator isolation contribute to reproductive isolation between the two Arisaema species and should enable the two species to coexist in this area.

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Disruption of endosperm development is a major cause of hybrid seed inviability between Mimulus guttatus and Mimulus nudatus

Cited by 74 publications

References 80 publications

Genetic loci with parent‐of‐origin effects cause hybrid seed lethality in crosses between Mimulus species

Genetic loci with parent‐of‐origin effects cause hybrid seed lethality in crosses between Mimulus species

Hybrid inviability and differential submergence tolerance drive habitat segregation between two congeneric monkeyflowers

Pre‐pollination barriers between two sympatric Arisaema species in northern Shikoku Island, Japan

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