CoChat
Sign Up
Cited by 48Chromosomal and Genetic VariationsEvolution and Genetic DynamicsPlant Reproductive Biology

Pervasive antagonistic interactions among hybrid incompatibility loci

Open access
Guerrero, Rafael F., Muir, Christopher D., Josway, Sarah, Moyle, Leonie C.·2017·PLoS Genetics
DOI 10.1371/journal.pgen.1006817PMC PMC5484531

Published version of a preprint

Open this paper in CoChat — free accountOpen PDF

Abstract

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 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 ( 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 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 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 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. AUTHOR SUMMARY A 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 reproductive isolation—and therefore new species—evolve. The complexity of these interactions, however, is poorly understood in empirical systems. We examined the fertility of hybrids that carried one or two chromosomal regions from a close relative, finding that hybrids with two of these heterospecific regions were frequently less sterile than would be expected from the joint fitness of hybrids that have the same regions singly. This ‘less-than-additive’ effect on hybrid sterility was widespread (observed in 20% of pairwise combinations), and especially pronounced for male sterility. We infer that genes contributing to male sterility form a more tightly connected network than previously thought, implying that reproductive isolation is evolving by incremental dysfunction of complex interactions rather than by independent pairwise incompatibilities. We use simulations to illustrate these expected patterns of accumulation of reproductive isolation when it involves highly interconnected gene networks.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1371/journal.pgen.1006817

Cites

44 of 44 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • The faster-than-linear accumulation of hybrid incompatibilities with divergence time has been recovered in multiple taxa including Solanum, Drosophila, and Mus musculus.

    “this result has been recovered in multiple taxa: Including Solanum (Moyle and Nakazato 2010; Guerrero et al. 2017), Drosophila (Matute et al. 2010), or Mus musculus (Wang et al. 2015).”

    From Finding Hybrid Incompatibilities Using Genome Sequences from Hybrid Populations (2021) · cites this paper as Guerrero et al. 2017

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 1

  1. [36]Arnqvist G, Rowe L. Sexual conflict: Princeton University Press; 2013.

Cited by

Sorted by citations

Related

Authors
Guerrero, R. F., Muir, C. D., Josway, S., & Moyle, L. C.
Affiliations
  • Indiana University Bloomington (US)
  • University of British Columbia (CA)
  • Oregon Health & Science University (US)
Corresponding author
Moyle, Leonie C.
ORCID
Venue
PLoS Genetics
Publisher
Public Library of Science (PLoS)
Published
2017-06-12
Volume
13
Issue
6
Pages
e1006817
ISSN
  • 1553-7390 (ISSN-L)
  • 1553-7404
DOI
10.1371/journal.pgen.1006817
PMC
PMC5484531
OpenAlex
W2951381369
Cited by
48
References
44
Citations by year
2026: 3 · 2025: 4 · 2024: 1 · 2023: 4 · 2022: 5 · 2021: 6 · 2020: 10 · 2019: 4 · 2018: 8 · 2017: 2 · 2016: 1
FWCI
6.46
Type
journal article
Language
en
Update notices
new_version (2017-06-26)
Open access
Licence
Locations
  • PLoS Genetics (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
Funders
Division of Environmental Biology (DEB-0532097, DEB-0841957)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Plant Reproductive Biology
Keywords
hybrid incompatibility, epistasis, antagonism, hybrid sterility, hybrid inviability, pollen fertility, seed fertility, reproductive isolation, speciation, introgression, Solanum habrochaites, tomato, snowball effect
MeSH terms
Chromosome Mapping, Epistasis, Genetic, Fertility, Genotype, Hybridization, Genetic, Models, Genetic, Phenotype, Pollen, Seeds, Species Specificity, Solanum lycopersicum, Chromosomes, Plant, Quantitative Trait Loci, Plant Infertility, Reproductive Isolation

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review