Abstract
The importance of regulatory incompatibilities to the early stages of speciation remains unclear. Hybrid mammals often show extreme parent-of-origin growth effects that are thought to be a consequence of disrupted genetic imprinting (parent-specific epigenetic gene silencing) during early development. Here, we test the long-standing hypothesis that abnormal hybrid growth reflects disrupted gene expression due to loss of imprinting (LOI) in hybrid placentas, resulting in dosage imbalances between paternal growth factors and maternal growth repressors. We analyzed placental gene expression in reciprocal dwarf hamster hybrids that show extreme parent-of-origin growth effects relative to their parental species. In massively enlarged hybrid placentas, we observed both extensive transgressive expression of growth-related genes and biallelic expression of many genes that were paternally silenced in normal sized hybrids. However, the apparent widespread disruption of paternal silencing was coupled with reduced gene expression levels overall. These patterns are contrary to the predictions of the LOI model and indicate that hybrid misexpression of dosage-sensitive genes is caused by other regulatory mechanisms in this system. Collectively, our results support a central role for disrupted gene expression and imprinting in the evolution of mammalian hybrid inviability, but call into question the generality of the widely invoked LOI model.
| Original language | English |
|---|---|
| Pages (from-to) | 2690-2703 |
| Number of pages | 14 |
| Journal | Evolution |
| Volume | 70 |
| Issue number | 12 |
| DOIs | |
| State | Published - Dec 1 2016 |
Funding
We would like to thank Ryan Bracewell, Colin Callahan, Zak Clare-Salzler, Ted Cosart, Kris Crandell, Doug Emlen, Mafalda Ferreira, Lila Fishman, Matt Jones, Sara Keeble, Evgeny Kroll, Erica Larson, John McCutcheon, Colin Prather, Brice Sarver, Dan Vanderpool, Paul Vrana, and Catherine Wynne-Edwards for helpful discussions, Kelly Carrick, Jessica Wexler, and the LAR staff for assistance with animal care, and Lou Herritt for assistance with histological sample preparation. Matt Carling and four anonymous reviewers provided helpful comments that improved the manuscript. We thank Robert Johnston, Mary Timonin, and Ned Place for supplying founding stocks for our colonies. This research was supported by the Eunice Kennedy Shriver National Institute of Child Health and Human Development of the National Institutes of Health (R01HD073439 to J.M.G.); a Doctoral Dissertation Improvement grant from the National Science Foundation (DEB-1406754 to T.D.B.); the University of Montana; the Society for the Study of Evolution's Rosemary Grant Award (to T.D.B.); and the David Nicholas Memorial Fund (to T.D.B.). Genomic instrumentation at the University of Montana was supported by a grant from the M. J. Murdock Charitable Trust. The funders had no role in study design, data collection, and analysis, decision to publish, or preparation of the manuscript. Genomic data are archived under the GenBank BioProject PRJNA306772. The Transcriptome Shotgun Assembly project has been deposited at DDBJ/EMBL/GenBank under the accessions GEVA00000000 and GEVB00000000. The versions described in this paper are the first versions, GEVA01000000 and GEVB01000000. The raw sequencing reads are found under SRA accession numbers SRR3884838-SRR3884865 and SRR3884867-SRR3884878. Pseudotranscriptomes and associated files are deposited in Dryad under the DOI 10.5061/dryad.j0j5K.
| Funders | Funder number |
|---|---|
| GEVA00000000, GEVA01000000, GEVB00000000, GEVB01000000, SRR3884867-SRR3884878, SRR3884838-SRR3884865 | |
| DEB-1406754 | |
| R01HD073439 | |
| PRJNA306772 | |
| European Molecular Biology Laboratory |
Keywords
- Gene expression
- Phodopus
- hybrid inviability
- hybridization