On the Theoretical and Empirical Framework for Studying Genetic Interactions within and among Species

Demuth,; Wade,

doi:10.2307/3473384

Cited by 23 publications

(69 citation statements)

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“…9), can also be derived from a model of genetic incompatibilities, each involving a small number of loci. Such models stem from the classic work of Dobzhansky 1937 and have been important in the study of speciation genetics (Fraïsse et al 2014; Orr 1995; Turelli and Orr 2000; Gavrilets 2004; Welch 2004; Demuth and Wade 2005; Fraïsse et al. 2016b).…”

Section: Results With Haploid Geneticsmentioning

confidence: 99%

“…The tools of quantitative genetics have often been used to study hybridization (e.g., Melchinger 1987; Lynch 1991; Demuth and Wade 2005; Fitzpatrick 2008), but Fisher's model is fully additive at the level of phenotype, and the “traits” need not correspond in any simple way to standard quantitative traits (Rosas et al. 2010; Martin 2014; Schiffman and Ralph 2017).…”

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confidence: 99%

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Coadapted genomes and selection on hybrids: Fisher's geometric model explains a variety of empirical patterns

2018

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Natural selection plays a variety of roles in hybridization, speciation, and admixture. Most research has focused on two extreme cases: crosses between closely related inbred lines, where hybrids are fitter than their parents, or crosses between effectively isolated species, where hybrids suffer severe breakdown. But many natural populations must fall into intermediate regimes, with multiple types of gene interaction, and these are more difficult to study. Here, we develop a simple fitness landscape model, and show that it naturally interpolates between previous modeling approaches, which were designed for the extreme cases, and invoke either mildly deleterious recessives, or discrete hybrid incompatibilities. Our model yields several new predictions, which we test with genomic data from Mytilus mussels, and published data from plants (Zea, Populus, and Senecio) and animals (Mus, Teleogryllus, and Drosophila). The predictions are generally supported, and the model explains a number of surprising empirical patterns. Our approach enables novel and complementary uses of genome‐wide datasets, which do not depend on identifying outlier loci, or “speciation genes” with anomalous effects. Given its simplicity and flexibility, and its predictive successes with a wide range of data, the approach should be readily extendable to other outstanding questions in the study of hybridization.

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Section: Results With Haploid Geneticsmentioning

confidence: 99%

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confidence: 99%

Coadapted genomes and selection on hybrids: Fisher's geometric model explains a variety of empirical patterns

2018

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“…A second round of crossing (Supplementary Figure S1) was conducted to generate all seeds for the fitness assay and joint scaling analyses (Mather and Jinks, 1982;Lynch and Walsh, 1998;Demuth and Wade, 2005) at the same time, in the same maternal environment. Seeds of parental lines and F 1 were germinated and raised to flowering as above.…”

Section: Growing Conditions and Crossing Designmentioning

confidence: 99%

“…For each line pair, we decomposed the total phenotypic variance for multiplicative fitness and fitness components into additive and non-additive components by joint scaling analyses (Mather and Jinks, 1982;Lynch and Walsh, 1998;Demuth and Wade, 2005). As we detected significant variation in the effect of cross type between line pairs within-population set (Table 1), we performed separate joint scaling analyses for each of the four line pairs.…”

Section: Statistical Analysesmentioning

confidence: 99%

“…These approaches have been championed for their utility in exploring the genetic architecture underlying fitness differences in crosses between natural populations (Fenster et al, 1997;Demuth and Wade, 2005Demuth et al, 2014). The line cross approach utilizes a set of crosses (minimally F 1 and F 2 ) between two parental lines to decompose the differences in a trait of interest into additive and non-additive genetic effects.…”

Section: Introductionmentioning

confidence: 99%

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Heterosis and outbreeding depression in crosses between natural populations of Arabidopsis thaliana

2015

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Understanding the causes and architecture of genetic differentiation between natural populations is of central importance in evolutionary biology. Crosses between natural populations can result in heterosis if recessive or nearly recessive deleterious mutations have become fixed within populations because of genetic drift. Divergence between populations can also result in outbreeding depression because of genetic incompatibilities. The net fitness consequences of between-population crosses will be a balance between heterosis and outbreeding depression. We estimated the magnitude of heterosis and outbreeding depression in the highly selfing model plant Arabidopsis thaliana, by crossing replicate line pairs from two sets of natural populations (C ↔ R, B ↔ S) separated by similar geographic distances (Italy ↔ Sweden). We examined the contribution of different modes of gene action to overall differences in estimates of lifetime fitness and fitness components using joint scaling tests with parental, reciprocal F 1 and F 2 , and backcross lines. One of these population pairs (C ↔ R) was previously demonstrated to be locally adapted, but locally maladaptive quantitative trait loci were also found, suggesting a role for genetic drift in shaping adaptive variation. We found markedly different genetic architectures for fitness and fitness components in the two sets of populations. In one (C ↔ R), there were consistently positive effects of dominance, indicating the masking of recessive or nearly recessive deleterious mutations that had become fixed by genetic drift. The other set (B ↔ S) exhibited outbreeding depression because of negative dominance effects. Additional studies are needed to explore the molecular genetic basis of heterosis and outbreeding depression, and how their magnitudes vary across environments.

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Loss of ecologically important genetic variation in late generation hybrids reveals links between adaptation and speciation

et al. 2020

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Adaptation to contrasting environments occurs when advantageous alleles accumulate in each population, but it remains largely unknown whether these same advantageous alleles create genetic incompatibilities that can cause intrinsic reproductive isolation leading to speciation. Identifying alleles that underlie both adaptation and reproductive isolation is further complicated by factors such as dominance and genetic interactions among loci, which can affect both processes differently and obscure potential links between adaptation and speciation. Here, we use a combination of field and glasshouse experiments to explore the connection between adaptation and speciation while accounting for dominance and genetic interactions. We created a hybrid population with equal contributions from four contrasting ecotypes of Senecio lautus (Asteraceae), which produced hybrid genomes both before (F1 hybrid generation) and after (F4 hybrid generation) recombination among the parental ecotypes. In the glasshouse, plants in the second generation (F2 hybrid generation) showed reduced fitness as a loss of fertility. However, fertility was recovered in subsequent generations, suggesting that genetic variation underlying the fitness reduction was lost in subsequent generations. To quantify the effects of losing genetic variation at the F2 generation on the fitness of later generation hybrids, we used a reciprocal transplant to test for fitness differences between parental ecotypes, and F1 and F4 hybrids in all four parental habitats. Compared to the parental ecotypes and F1 hybrids, variance in F4 hybrid fitness was lower, and lowest in habitats that showed stronger native-ecotype advantage, suggesting that stronger natural selection for the native ecotype reduced fitness variation in the F4 hybrids. Fitness trade-offs that were present in the parental ecotypes and F1 hybrids were absent in the F4 hybrid. Together, these results suggest that the genetic variation lost after the F2 generation was likely associated with both adaptation and intrinsic reproductive isolation among ecotypes from contrasting habitats.

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On the Theoretical and Empirical Framework for Studying Genetic Interactions within and among Species

Cited by 23 publications

References 0 publications

Coadapted genomes and selection on hybrids: Fisher's geometric model explains a variety of empirical patterns

Coadapted genomes and selection on hybrids: Fisher's geometric model explains a variety of empirical patterns

Heterosis and outbreeding depression in crosses between natural populations of Arabidopsis thaliana

Loss of ecologically important genetic variation in late generation hybrids reveals links between adaptation and speciation

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