Patterns, predictors, and consequences of dominance in hybrids

Abstract

Are first-generation (F 1 ) hybrids typically intermediate for all traits that differentiate their parents? Or are they similar to one parent for most traits, or even mismatched for divergent traits? Although the phenotype of otherwise viable and fertile hybrids determines their fate, little is known about the general patterns, predictors, and consequences of phenotype expression in hybrids. To address this empirical gap, we compiled data from nearly 200 studies where traits were measured in a common environment for two parent populations and F 1 hybrids. We find that individual traits are typically halfway between the parental midpoint and one parental value (i.e., hybrid trait values are typically 0.25 or 0.75 if parents' values are 0 & 1). When considering pairs of traits together, a hybrid's multivariate phenotype tends to resemble one parent (pairwise parent-bias) about 50 % more than the other while also exhibiting a similar magnitude of trait mismatch due to different traits having dominance in conflicting directions. We detect no phylogenetic signal nor an effect of parental genetic distance on dominance or mismatch. Using data from an experimental field planting of recombinant hybrid sunflowers-where there is among-individual variation in dominance and mismatch due to segregation of divergent alleles-we illustrate that pairwise parent-bias improves fitness while mismatch reduces fitness. Importantly, the effect of mismatch on fitness was stronger than that of pairwise parent-bias. In sum, our study has three major conclusions. First, hybrids between ecologically divergent natural populations are typically not phenotypically intermediate but rather exhibit substantial mismatch while also resembling one parent more than the other. Second, dominance and mismatch are likely determined by population-specific processes rather than general rules. Finally, selection against hybrids likely results from both selection against somewhat intermediate phenotypes and against mismatched trait combinations. hybridization | speciation | phenotypic mismatch | opposing dominanceCorrespondence: ken.thompson@zoology.ubc.ca

Non-additive genetic effects induce novel phenotypic distributions in male mating traits of F1 hybrids

“…In contrast to phenotypic mean, average phenotypic variability of male F1 hybrids was similar to the average value of parents' variability ( Fig. 1b), which aligns with previous comparative study on non-male-mating traits across animals and plants 13 . A caveat is that hybrid phenotypic variability is either larger or smaller than that of both parents in most trait observations (74.9%, see Novel variability), resulting in large heterogeneity in parent-hybrid difference in phenotypic variability (total I 2 = 75.6%, partitioned into phylogeny I 2 = 19.5%, study I 2 = 11.4%, crossed lineage I 2 = ~0%, residual I 2 = 44.7%; Fig.…”

“…2a; P < 0.001). This pattern is consistent with non-male-mating traits across animals and plants 13 . Given that maternal inheritance is particularly profound for morphology, including body size 23 , mothers seem to directly influence male-mating morphological traits, and even sound traits that are partially determined by morphology and body size 24,25 .…”

“…3a), indicating that non-additive genetic interaction is a powerful source of phenotypic novelty in male mating traits. A recent comparative analysis, using non-male-mating traits, showed that F1 hybrids express novel phenotype only in 20% of species pairs across any plants and animal taxa 13 . Discordance with our result suggests that male-mating traits of animals more frequently express novel phenotype during hybridization, and / or using sex-aggregated data in the earlier study has led to underestimation of novel phenotype expression frequency.…”

Quantitative trait locus mapping reveals an independent genetic basis for joint divergence in leaf function, life-history, and floral traits between scarlet monkeyflower (Mimulus cardinalis) populations

“…Composite functional traits often exhibit transgressive means and low heritability in hybrids, suggesting independent genetic bases for the underlying components -Two patterns seen in our experimental hybrids data underline complexities in predicting the evolution of ecological-proxy composite leaf functional traits. First, due to independent assortment and dominance, F1 hybrids between isolated populations may be more extreme that either parental genotype (heterosis or underdominance, respectively) for the composite trait (Rieseberg et al, 2011;Thompson et al, 2019). In our cross, F1…”

“…hybrids have the low photosynthetic rates of the CE10 parent coupled with the low stomatal resistance of the WFM parent, resulting in transgressively low hybrid iWUE; stigma-anther separation is similarly underdominant (Table1). Such transgressive composite phenotypes may reduce the fitness of hybrids between divergent populations and slow adaptive introgression and evolutionary rescue under contemporary climate change (Thompson et al, 2019). Second, later-generation hybrids may exhibit low heritability or transgressive segregation because genes underlying component trait sort into novel combinations (Rieseberg et al, 1999), potentially with epistatic interactions (Muir and Moyle, 2009).…”