Genetic analysis of inbreeding depression caused by chlorophyll-deficient lethals in Mimulus guttatus

Willis, John H.

doi:10.1038/hdy.1992.172

Cited by 57 publications

(54 citation statements)

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“…The ability of selection to remove weakly deleterious mutations is reduced when effective population sizes are small, which is typical for selfing species. Correspondingly, the dominance hypothesis has generally received the most empirical support from studies of inbreeding depression (73)(74)(75)(76). If heterosis is the reverse of inbreeding depression, then the degree of heterosis should positively correlate with the genetic distance between parents, and causal alleles should be rare with small phenotypic effects (8,(51)(52)(53)73).…”

Section: Arabidopsis Thaliana In the Context Of Traditional Heterosismentioning

confidence: 99%

Genetic architecture of nonadditive inheritance inArabidopsis thalianahybrids

Seymour

Chae

Grimm

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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The ubiquity of nonparental hybrid phenotypes, such as hybrid vigor and hybrid inferiority, has interested biologists for over a century and is of considerable agricultural importance. Although examples of both phenomena have been subject to intense investigation, no general model for the molecular basis of nonadditive genetic variance has emerged, and prediction of hybrid phenotypes from parental information continues to be a challenge. Here we explore the genetics of hybrid phenotype in 435 Arabidopsis thaliana individuals derived from intercrosses of 30 parents in a half diallel mating scheme. We find that nonadditive genetic effects are a major component of genetic variation in this population and that the genetic basis of hybrid phenotype can be mapped using genome-wide association (GWA) techniques. Significant loci together can explain as much as 20% of phenotypic variation in the surveyed population and include examples that have both classical dominant and overdominant effects. One candidate region inherited dominantly in the half diallel contains the gene for the MADS-box transcription factor AGAMOUS-LIKE 50 (AGL50), which we show directly to alter flowering time in the predicted manner. Our study not only illustrates the promise of GWA approaches to dissect the genetic architecture underpinning hybrid performance but also demonstrates the contribution of classical dominance to genetic variance.T he often observed phenotypic superiority of progeny relative to their parents, or heterosis, is a universal phenomenon and of great importance to plant agriculture. The earliest description of heterosis (also known as hybrid vigor or superiority) dates to Darwin's studies of cross-fertilization in plants. He noticed that intercrossing distantly related individuals gave rise to larger, more vigorous progeny (1). Four decades later, George Shull coined the term "heterosis" (2) for this phenomenon, which he and Edward East had independently described for hybrids of inbred maize in 1908 (3, 4). Heterosis has long been of interest to evolutionary biologists as a potential explanation for the ubiquity of cross-fertilization in plants and animals, but it is also a central component of agricultural breeding programs. The combination of hybrid seed technology and inbred line improvement has driven an unprecedented improvement in maize yield over the past century (5). Despite the economic importance of heterosis and its intensive investigation in a wide spectrum of species, prediction of hybrid performance from parental information remains a major challenge (6).In the terms of quantitative genetics, hybrid vigor (and its opposite, inferiority) describes a deviation of progeny from the phenotypic mean of the parents. This means that heterosis cannot be explained by the addition of the effects of contributing alleles (7). Nonadditive genetic variance can result from a nonlinear phenotypic effect of alleles at one locus, as in the case of dominant/recessive allele pairs in classical genetics, or from epistatic interactions ...

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Section: Arabidopsis Thaliana In the Context Of Traditional Heterosismentioning

confidence: 99%

Genetic architecture of nonadditive inheritance inArabidopsis thalianahybrids

Seymour

Chae

Grimm

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…These populations practice a moderate amount of selffertilization: the estimated outcrossing rates in 1989 were 0.91 ± 0.07 for the Iron Mountain population and 1.03 ± 0.06 for the Cone Peak population, and in 1990 the rates were 0.76 ± 0.11 and 0.66 ± 0.10 for the Iron Mountain and Cone Peak populations, respectively (Willis 1993b). Both populations also exhibit substantial inbreeding depression for major components of fitness (Willis 1992(Willis , 1993a.…”

Section: Outcrossedmentioning

confidence: 99%

Measures of Phenotypic Selection Are Biased by Partial Inbreeding

Willis

1996

Evolution

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Abstract,-When populations are partially inbred due to the population structure or to a mixed mating system like partial self-fertilization, some individuals will be more inbred than others. This heterogeneity among individuals in the history of inbreeding can greatly complicate the interpretation of measures of quantitative genetic variability when the traits studied exhibit inbreeding depression. Partial inbreeding can also bias measures of phenotypic selection toward the detection of strong directional and stabilizing selection. In this paper, data are presented from several inbreeding experiments conducted on two partially selfing, annual populations of the monkeyflower Mimulus guttatus that show that the means of many of the morphological and phenological traits measured were affected by inbreeding. These findings imply that estimates of heritabilities and additive genetic covariances would not reflect the potential for these populations to respond to selection, Phenotypic selection analyses conducted on naturally occurring plants, involving linear regressions of relative seed production on the traits, revealed significant directional selection on many of the same quantitative traits measured in the inbreeding studies. However, when the same selection analyses were performed on plants with known histories of inbreeding, part of the statistical relationship between relative seed number and the traits was found to be due to the mating system: inbred individuals had both lower seed production and different mean values for the traits than outcrossed individuals. It is also shown, with a hypothetical example, that partial inbreeding can bias measures of stabilizing selection toward the detection of strong stabilizing selection. Partial inbreeding therefore tends to make directional and stabilizing selection appear stronger than it is, and it may be that natural selection in the wild is actually weaker than many studies of partially inbred species suggest.Key words.-Inbreeding, inbreeding depression, Mimulus, natural selection, quantitative genetics, self-fertilization.Received August 7, 1995. Accepted August 24, 1995 Many studies of quantitative genetics and of phenotypic selection in natural populations of plants and animals have resulted from the realization that the evolution of quantitative traits by natural selection can be understood by independent analysis of selection and inheritance. These diverse empirical studies, prompted in large part by theoretical results in quantitative genetics and selection analysis (e.g.,

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“…Second, albino seedlings may not be noticed in a single late census of germination if they perish early in the experiment, as such seedlings quickly rot and disappear. This is the main reason that my previous studies (Willis 1992(Willis , 1993a(Willis ,b, 1999a analyzed mortality due to albinism in this way.…”

Section: Measurement Of Fitness For Outcrossed and Selfed Progeny Fromentioning

confidence: 99%

“…Plants maintained in the greenhouse also complete their life cycle rapidly and can be grown under ideal conditions from seed to seed in less than six weeks. The population is predominantly outcrossing, with selfing rates ranging near 0 to about 0.25 (Willis 1993a), and exhibits substantial inbreeding depression in the field and greenhouse for most components of fitness, as well as for morphological and phenological traits (Willis 1992(Willis , 1993a(Willis ,b, 1996(Willis , 1999a.…”

Section: Study Species and Populationmentioning

confidence: 99%

“…Any chlorophylldeficient seedlings were noted throughout these 14 days, but were discarded and scored as not having germinated, since this recessive phenotype is lethal within a few days of germination (Willis 1992). I treated mortality due to albinism in this way, rather than analyzing it as a part of a later component of fitness, for two reasons.…”

Section: Measurement Of Fitness For Outcrossed and Selfed Progeny Fromentioning

confidence: 99%

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THE ROLE OF GENES OF LARGE EFFECT ON INBREEDING DEPRESSION IN MIMULUS GUTTATUS

Willis

1999

Evolution

109

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Abstract.-Severe inbreeding depression is routinely observed in outcrossing species. If inbreeding load is due largely to deleterious alleles of large effect, such as recessive lethals or steriles, then most of it is expected to be purged during brief periods of inbreeding. In contrast, if inbreeding depression is due to the cumulative effects of many deleterious alleles of small effect, then it will be maintained in the face of periodic inbreeding. Whether or not inbreeding depression can be purged with inbreeding in the short term has important implications for the evolution of mating systems and the probability that a small population will go extinct. In this paper I evaluate the extent to which the tremendous inbreeding load in a primarily outcrossing population of the wildflower, MimuLus guttatus, is due to alleles of large effect. To do this, I first constructed a large outbred "ancestral" population by randomly mating plants collected as seeds from a natural population. From this population I formed 1200 lines that were maintained by self-fertilization and single seedling descent: after five generations of selfing, 335 lines had survived the inbreeding process. Selection during the line formation is expected to have largely purged alleles of large effect from the collection of highly inbred lines. Because alleles with minor effects on fitness should have been effectively neutral, the inbreeding depression due to this class of genes should have been unchanged. The inbred lines were intercrossed to form a large, outcrossed "purged" population. Finally, I estimated the fitness of outbred and selfed progeny from the ancestral and purged populations to determine the contribution of major deleterious alleles on inbreeding depression. I found that although the average fitness of the outcrossed progeny nearly doubled following purging, the limited decline in inbreeding depression and limited increase in inbred fitness indicates that alleles of large effect are not the principle cause of inbreeding depression in this population. In aggregate, the data suggest that lethals and steriles make a minority contribution to inbreeding depression and that the increased outbred fitness is due primarily to adaptation to greenhouse conditions. Key words.-Deleterious mutations, genetic load, inbreeding depression, Mimulus, outcrossing, self-fertilization.Received August 26, 1998. Inbreeding reduces fitness in most species of plants and animals, a phenomenon known as inbreeding depression (Darwin 1876;Wright 1977;Charlesworth and Charlesworth 1987). The effect of inbreeding depression on a population's evolution or its chances of extinction depends on its genetic basis. We now have substantial evidence from studies on diverse organisms that most inbreeding depression is due to deleterious, partially recessive alleles, and not to overdominant loci (Moll et al. 1964;Simmons and Crow 1977;Mather 1982;Crow and Simmons 1983;Jinks 1983;Sprague 1983;Charlesworth and Charlesworth 1987;Crow 1993;Charlesworth and Hughes 1999;Dudash an...

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Genetic analysis of inbreeding depression caused by chlorophyll-deficient lethals in Mimulus guttatus

Cited by 57 publications

References 56 publications

Genetic architecture of nonadditive inheritance inArabidopsis thalianahybrids

Genetic architecture of nonadditive inheritance inArabidopsis thalianahybrids

Measures of Phenotypic Selection Are Biased by Partial Inbreeding

THE ROLE OF GENES OF LARGE EFFECT ON INBREEDING DEPRESSION IN MIMULUS GUTTATUS

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