The evolution of hybrid fitness during speciation

Dagilis, Andrius J.; Kirkpatrick, Mark; Bolnick, Daniel I.

doi:10.1371/journal.pgen.1008125

Cited by 64 publications

(98 citation statements)

References 72 publications

(79 reference statements)

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“…Second, despite the widely documented, asymmetric risk of hybrid breakdown in the heterogametic sex, i.e., Haldane's rule (Haldane, 1922;Coyne and Orr, 1997;Delph and Demuth, 2016), our model considers sexual selection with only a single sex of mating type. Third, both empirical results from yeast (Bernardes et al, 2017) and from theoretical, populationgenetic models (Dagilis et al, 2019) point towards the importance of increased hybrid fitness, i.e., heterosis, even if only temporary, during speciation (Gavrilets, 2003). Forth, there are studies that clearly demonstrate the importance of divergent selection in the process of speciation (e.g., Nosil et al, 2002;Allender et al, 2003;Gow et al, 2007).…”

Section: Discussionmentioning

confidence: 99%

Reproductive barriers as a byproduct of gene network evolution

Yang

Scarpino

2020

Preprint

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Molecular analyses of closely related taxa have increasingly revealed the importance of 10 higher-order genetic interactions in explaining the observed pattern of reproductive isolation 11 between populations. Indeed, both empirical and theoretical studies have linked the process of 12 speciation to complex genetic interactions. Gene Regulatory Networks (GRNs) capture the 13 inter-dependencies of gene expression and encode information about an individual's phenotype 14 and development at the molecular level. As a result, GRNs can-in principle-evolve via natural 15 selection and play a role in non-selective, evolutionary forces. Here, we develop a network-based 16 model, termed the pathway framework, that considers GRNs as a functional representation of 17 coding sequences. We then simulated the dynamics of GRNs using a simple model that included 18 natural selection, genetic drift, and sexual reproduction and found that reproductive barriers can 19 develop rapidly between allopatric populations experiencing identical selection pressure. Further, 20 we show that alleles involved in reproductive isolation can predate the allopatric separation of 21 populations and that the number of interacting loci involved in genetic incompatibilities, i.e., the 22 order, is often high simply as a by-product of the networked structure of GRNs. Finally, we discuss 23 how results from the pathway framework are consistent with observed empirical patterns for 24 genes putatively involved in post-zygotic isolation. Taken together, this study adds support for the 25 central role of gene networks in speciation and in evolution more broadly. 26 27 31Through this work, it is widely accepted that divergent selection on de novo mutations in geo-32 graphically isolated populations can facilitate speciation, as originally theorized by (Bateson, 1909; 33 Dobzhansky, 1936; Muller, 1942). Despite well-established examples from Drosophila (Brideau34 et al., 2006), Xiphophorus (Wittbrodt et al., 1989; Powell et al., 2020), Oryza (Yamamoto et al., 35 2010), Arabidopsis (Bikard et al., 2009), and Mus (Davies et al., 2016), the genetics and evolutionary 36 history of incompatibilities are typically far more complex and/or less well understood than what 37 is suggested by classical models (Noor and Feder, 2006; Lowry et al., 2008; Presgraves, 2010; Wolf 38 et al., 2010; Nosil and Schluter, 2011; Seehausen et al., 2014; Marques et al., 2019; Dagilis and 39Matute, 2020). 40 Post-zygotic, genetic isolation is thought to occur due to epistatic interaction between loci, where 41 alleles arise and fix in allopatry prior to secondary contact, e.g., the Bateson-Dobzhansky-Muller 42 1 of 26 Manuscript submitted to eLife (BDM) model (Bateson, 1909; Dobzhansky, 1936; Muller, 1942). However, many incompatibilities 43 uncovered using high-throughput molecular analyses (Castillo and Barbash, 2017; Kuzmin et al., 44 2018; Vaid and Laitinen, 2019) and quantitative trait locus (QTL) mapping (Moyle and Nakazato, 45 2008; Turner et al., 2014; Ch...

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Section: Discussionmentioning

confidence: 99%

Reproductive barriers as a byproduct of gene network evolution

Yang

Scarpino

2020

Preprint

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“…Reproductive isolation is recognized as a powerful driving force for maintaining species identity (Ouyang et al, 2010;Dagilis et al, 2018). An important genetic factor maintaining reproductive isolation is transmission ratio distortion (TRD), which is defined as the allele inheritance in progenies of hybrids that show a statistically significant deviation from the expected Mendelian segregation ratios, also leading to deviations in genotype frequencies (Koide et al, 2012;Leppala et al, 2013;Li et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

Genetic Dissection and Validation of Chromosomal Regions for Transmission Ratio Distortion in Intersubspecific Crosses of Rice

Zhang

Wang

et al. 2020

Front. Plant Sci.

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Transmission ratio distortion (TRD) refers to a widespread phenomenon in which one allele is transmitted by heterozygotes more frequently to the progeny than the opposite allele. TRD is considered as a mark suggesting the presence of a reproductive barrier. However, the genetic and molecular mechanisms underlying TRD in rice remain largely unknown. In the present study, a population of backcross inbred lines (BILs) derived from the cross of a japonica cultivar Nipponbare (NIP) and an indica variety 9311 was utilized to study the genetic base of TRD. A total of 18 genomic regions were identified for TRD in the BILs. Among them, 12 and 6 regions showed indica (9311) and japonica (NIP) alleles with preferential transmission, respectively. A series of F 2 populations were used to confirm the TRD effects, including six genomic regions that were confirmed by chromosome segment substitution line (CSSL)-derived F 2 populations from intersubspecific allelic combinations. However, none of the regions was confirmed by the CSSL-derived populations from intrasubspecific allelic combination. Furthermore, significant epistatic interaction was found between TRD1.3 and TRD8.1 suggesting that TRD could positively contribute to breaking intersubspecific reproductive barriers. Our results have laid the foundation for identifying the TRD genes and provide an effective strategy to breakdown TRD for breeding wide-compatible lines, which will be further utilized in the intersubspecific hybrid breeding programs.

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“…Our focus on this study was to assess whether Drosophila hybrids suffer from reduced attractiveness. Hybrid fitness is a continuum that ranges from hybrid vigor to complete inviability (Guerrero et al 2017;Dagilis et al 2019). In some cases, hybrids might be more attractive to their parentals that their own conspecifics (Pfennig 2007).…”

Section: Discussionmentioning

confidence: 99%

Pure species discriminate against hybrids in theDrosophila melanogasterspecies subgroup

Serrato-Capuchina¹,

Schwochert²,

Zhang³

et al. 2020

Preprint

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Introgression, the exchange of alleles between species, is a common event in nature. This transfer of alleles between species must happen through fertile hybrids. Characterizing the traits that cause defects in hybrids illuminate how and when gene flow is expected to occur. Inviability and sterility are extreme examples of fitness reductions but are not the only type of defects in hybrids. Some traits specific to hybrids are more subtle but are important to determine their fitness. In this report, we study whether F1 hybrids between two species pairs of Drosophila are as attractive as the parental species. We find that in both species pairs, the sexual attractiveness of the F1 hybrids is reduced and that pure species discriminate strongly against them. We also find that the cuticular hydrocarbon (CHC) profile of the hybrids is intermediate between the parental species. Perfuming experiments show that modifying the CHC profile of the hybrids to resemble pure species improves their chances of mating. Our results show that behavioral discrimination against hybrids might be an important component of the persistence of species that can hybridize.

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The evolution of hybrid fitness during speciation

Cited by 64 publications

References 72 publications

Reproductive barriers as a byproduct of gene network evolution

Reproductive barriers as a byproduct of gene network evolution

Genetic Dissection and Validation of Chromosomal Regions for Transmission Ratio Distortion in Intersubspecific Crosses of Rice

Pure species discriminate against hybrids in theDrosophila melanogasterspecies subgroup

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