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bioRxiv preprint doi: https://doi.org/10.1101/818658; this version posted October 25, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. Patterns, predictors, and consequences of dominance in hybrids Ken A. Thompson1 , Mackenzie Urquhart-Cronish2, Kenneth D. Whitney3, Loren H. Rieseberg2, and Dolph Schluter1 1Department of Zoology & Biodiversity Research Centre, University of British Columbia, Canada 2Department of Botany & Biodiversity Research Centre, University of British Columbia, Canada 3Department of Biology, University of New Mexico, USA Are first-generation (F1) hybrids typically intermediate for all of interest because such patterns can shed light on the mech- traits that differentiate their parents? Or are they similar to one anisms underlying selection against hybrids. For example, parent for most traits, or even mismatched for divergent traits? if hybrids resemble one parent they could thrive in that par- Although the phenotype of otherwise viable and fertile hybrids ent’s niche and readily back-cross (Mallet 1986). Alterna- determines their fate, little is known about the general patterns, tively, if hybrids are phenotypically intermediate for all traits, predictors, and consequences of phenotype expression in hy- or possess mismatched trait combinations due to dominance brids. To address this empirical gap, we compiled data from in opposing directions, they might be unable to survive and nearly 200 studies where traits were measured in a common en- reproduce in the available niche space (Arnegard et al. 2014; vironment for two parent populations and F1 hybrids. We find that individual traits are typically halfway between the parental Cooper et al. 2018; Hatfield and Schluter 1999; Matsubayashi midpoint and one parental value (i.e., hybrid trait values are et al. 2010). Currently, little is known about general patterns typically 0.25 or 0.75 if parents’ values are 0 & 1). When con- of trait expression in hybrids. sidering pairs of traits together, a hybrid’s multivariate pheno- Previous synthetic studies investigating hybrid pheno- type tends to resemble one parent (pairwise parent-bias) about types have mixed conclusions. Some authors suggest that 50 % more than the other while also exhibiting a similar mag- nitude of trait mismatch due to different traits having domi- hybrid intermediacy is the rule (Hubbs 1940) whereas others nance in conflicting directions. We detect no phylogenetic sig- find that hybrids are better described as mosaics of parental nal nor an effect of parental genetic distance on dominance or and intermediate characters (Rieseberg and Ellstrand 1993). mismatch. Using data from an experimental field planting of re- Such previous studies typically lacked a quantitative frame- combinant hybrid sunflowers—where there is among-individual work and/or focused on a single taxon (e.g., fish or plants), variation in dominance and mismatch due to segregation of limiting our ability to arrive at general conclusions. In ad- divergent alleles—we illustrate that pairwise parent-bias im- dition, previous studies of hybrid phenotype expression tend proves fitness while mismatch reduces fitness. Importantly, the to use mostly data from domesticated taxa, wherein domi- effect of mismatch on fitness was stronger than that of pairwise nance is expected to be elevated compared to natural popula- parent-bias. In sum, our study has three major conclusions. tions (Crnokrak and Roff 1995; Fisher 1931). Here, we use First, hybrids between ecologically divergent natural popula- a geometric approach to quantify patterns of hybrid pheno- tions are typically not phenotypically intermediate but rather exhibit substantial mismatch while also resembling one parent types in a way that is comparable across studies. By quan- more than the other. Second, dominance and mismatch are tifying the ‘parent-bias’ across each pair of traits we deter- likely determined by population-specific processesPRE-PRINT rather than mine the extent to which hybrids are intermediate or tend to general rules. Finally, selection against hybrids likely results resemble one parent more than the other. And by quantifying from both selection against somewhat intermediate phenotypes the ‘mismatch’ (also termed ‘opposing dominance’ [Matsub- and against mismatched trait combinations. ayashi et al. 2010; Nosil 2012]) we can determine the extent to which hybrids have mismatched combinations of divergent hybridization | speciation | phenotypic mismatch | opposing dominance Correspondence: [email protected] parental traits (i.e., resemble parent 1 for trait x but parent 2 for trait y). In this article, we systematically document patterns of Introduction phenotype expression in hybrids, investigate the possible pre- When divergent populations occur in sympatry, they might dictors of these patterns, and use experimental data to explore mate and form hybrids (Mallet 2005). If those hybrids are vi- the fitness consequences of trait interactions in the field. We able and fertile, whether they survive and reproduce depends first summarize the results of a systematic literature review of on their ability to persist under prevailing ecological con- nearly 200 studies that compared the phenotypes of hybrids ditions. Because selection against hybrids limits gene flow and parents in a common environment. We then ask whether between parents (Harrison 1993), understanding the mech- features of a cross—such as the genetic distance between, or anisms underlying hybrid performance under ecologically- taxon of, the parents—are associated with dominance. We relevant conditions is key to understanding post-zygotic iso- then use data from an experimental planting of recombinant lation (Barton and Hewitt 1985; Gompert et al. 2017). Quan- hybrid sunflowers to evaluate whether patterns of pairwise tifying general patterns of phenotype expression in hybrids is parent-bias and mismatch predict fitness in hypothesized di- Thompson et al. | bioRχiv | October 24, 2019 | 1–28page.28 bioRxiv preprint doi: https://doi.org/10.1101/818658; this version posted October 25, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. rections. Our results provide insight into the mechanisms that visualization of pairwise parent-bias might commonly underlie selection against hybrids in nature. and mismatch in 2D trait space 1.00 P Methods 2 In this section, we provide a brief summary of, and rationale { 0.75 −1 ∙ for, our methodology. A detailed explanation of all methods, k dmismatch including a summary of the data sources, is given in the sup- F1 plementary methods. ait 2 0.50 r t { Systematic review of dominance patterns in F hy- −1 ∙ 1 0.25 k dparent-bias brids. We conducted a systematic literature search and iden- tified 198 studies from which we could collect data of at least one phenotypic trait measured in two parent taxa and their 0.00 P1 F1 hybrids in a common environment. We included studies that conducted crosses between wild-collected parental pop- 0.00 0.25 0.50 0.75 1.00 ulations or laboratory populations with fewer than ten gen- trait 1 erations of captivity. Data from wild hybrids (i.e., not from controlled crosses) were only included if hybrids were geno- Fig. 1. Visual overview of how 2-dimensional dominance metrics were calcu- typed. We aimed to include only traits with environment- lated. When studies contained two or more divergent traits we calculated pairwise parent-bias (dparent-bias) and mismatch (dmismatch) of the hybrid (here F1 but could in dependent effects on fitness—traits plausibly under diver- principle be any hybrid generation) phenotype with respect to the line connecting gent, rather than directional, selection (sometimes called the two parent phenotypes (P1 &P2). This procedure was repeated for every pair ‘non-fitness’ traits [Merilä and Sheldon 1999] or ‘ordinary’ of traits. k is a scaling factor that renders the maximum value observed without transgression (i.e., dmismatch when F1 trait values are [0, 1]; or√ pairwise dparent-bias traits [Orr and Betancourt 2001]). For example, traits such when F1 trait values are [0, 0]) equal to 1. For two traits, k = 2. Values > 1 can as ‘embryo viability’ are almost certainly under directional result when traits are transgressive. selection and were not included in our database. We ex- cluded likely fitness components because developmental dif- traits in all studies on a common scale where one (arbitrarily ficulties resulting from hybrid incompatibilities, or heterosis determined) parent had a value of 0 for all traits and the other resulting from outbreeding, often affects such traits in hy- had a value of 1 (see Fig. 1). Because we do not make any brids (Coyne and Orr 2004). This choice to exclude fitness assumptions about which trait value is ancestral or derived, traits likely renders our analysis on dominance more conser- dominance and recessivity of traits is indistinguishable. For vative, since hybrid breakdown or heterosis would manifest example, a trait’s degree of dominance is the same whether as a transgressive phenotype. By contrast, traits such as ‘limb the hybrid trait value is 0.2 or 0.8. Under an expectation of length’ might have particular values best suited to some en- additivity, a hybrid would have a trait value of 0.5 for all vironments and genetic backgrounds—it is implausible that traits. Importantly, however, if a hybrid had two traits with such traits would always be selected to a maximum or mini- values [0.2, 0.8], the arithmetic mean phenotype is indeed 0.5 mum value. Data from back-cross (BC1 only) and F2 hybrids but the hybrid is not intermediate but rather mismatched. The were collected when available, but primarily used to address hybrid in this case resembles one parent for the first trait and a different question (see Thompson 2019).

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