Pervasive Antagonistic Interactions Among Hybrid Incompatibility Loci

Abstract

Species barriers, expressed as hybrid inviability and sterility, are often due to epistatic interactions between divergent loci from two lineages. Theoretical models indicate that the strength, direction, and complexity of these genetic interactions can strongly affect the expression of interspecific reproductive isolation and the rates at which new species 5 evolve. Nonetheless, empirical analyses have not quantified the frequency with which loci are involved in interactions affecting hybrid fitness, and whether these loci predominantly interact synergistically or antagonistically, or preferentially involve loci that have strong individual effects on hybrid fitness. We systematically examined the prevalence of interactions between pairs of short chromosomal regions from one species 10 (Solanum habrochaites) co-introgressed into a heterospecific genetic background (Solanum lycopersicum). We used lines containing pairwise combinations of 15 chromosomal segments from S. habrochaites crossed into the background of S. lycopersicum (i.e., 95 double introgression lines). We compared the strength of hybrid incompatibility (either pollen sterility or seed sterility) expressed in each double 15 introgression line to the expected additive effect of its two component single introgressions. We found that: epistasis was common among co-introgressed regions; epistastic effects for hybrid dysfunction were overwhelmingly antagonistic (i.e., double hybrids were less unfit than expected from additive single introgression effects); and, epistasis was substantially more prevalent in pollen fertility compared to seed fertility 20 phenotypes. Together, these results indicate that higher-order interactions frequently contribute to postzygotic sterility barriers in these species. This pervasive epistasis leads to the decoupling of the patterns of accumulation of isolation loci and isolation phenotypes, and is expected to attenuate the rate of accumulation of hybrid infertility among lineages over time (i.e., giving diminishing returns as more reproductive isolation 25 loci accumulate). This decoupling effect might also explain observed differences between pollen and seed fertility in their fit to theoretical predictions of the accumulation of isolation loci, including the 'snowball' effect.. CC-BY-NC-ND 4.0 International license peer-reviewed) is the author/funder. It is made available under aThe copyright holder for this preprint (which was not . http://dx.doi.org/10.1101/090886 doi: bioRxiv preprint first posted online Dec. 1, 2016; AUTHOR SUMMARY 30A characteristic feature of new species is their inability to produce fertile or viable hybrids with other lineages. This post-zygotic reproductive isolation is caused by dysfunctional interactions between genes that have newly evolved changes in the diverging lineages. Whether these interactions occur between pairs of divergent alleles, or involve more complex networks of genes, can have strong effects on how rapidly 35 reproductive isolation-and therefore new species-evolve. The...

ΦX174 Attenuation by Whole Genome Codon Deoptimization

“…A number of studies have investigated epistasis among pairs or triple sets of deleterious mutations, but the findings are mixed (105)(106)(107) . Sometimes the combined effect is the sum of the individual effects (additive/no epistasis), sometimes it is less than predicted from the individual effects (antagonistic/positive epistasis) (108,109) , and sometimes it is more than predicted (synergistic/negative epistasis) (110) . Among these three scenarios, antagonistic epistasis seems to be most common (104,111) .…”

Spiraling Complexity: A Test of the Snowball Effect in a Computational Model of RNA Folding

“…What explains this mismatch between the RNA data and the Orr model? One possibility is that some inviable introgressions are caused by multiple DMIs (Guerrero et al 2016). For example, imagine two genotypes, 1 and 2, divergent at multiple loci…”

“…For example, the individual segments introgressed in Moyle and Nakazato (2010) included approximately 2-4% of the genome, and likely contained hundreds of genes. Second, individual alleles might participate in multiple DMIs, specially if complex DMIs are common (Guerrero et al 2016).…”

Support for the dominance theory inDrosophilatranscriptomes

“…Regardless of the evolutionary forces driving faster--X (Z) evolution (positive selection or relaxed negative selection), its implications for the genetic basis of hybrid dysfunction are clear: the X chromosome will disproportionally contribute to between--species Dobzhansky--Muller incompatibilities (DOBZHANSKY 1937;MULLER 1942;COYNE AND ORR 1989). Even a slightly elevated substitution rate on the X chromosome will be amplified in hybrids, as the number of incompatibilities increases exponentially with divergence time (ORR 1995;TURELLI AND ORR 2000;MATUTE et al 2010;MOYLE AND NAKAZATO 2010;GUERRERO et al 2017). Mapping studies in a 6 variety of species including mice, Lepidoptera, and Drosophila have shown that the factors having the largest effects on hybrid dysfunction, particularly hybrid male sterility, are X--linked (COYNE AND ORR 1989;COYNE et al 1991;COYNE 1992; COYNE AND ORR 2004).…”