Widespread misregulation of inter-species hybrid transcriptomes due to sex-specific and sex-chromosome regulatory evolution
Abstract
When gene regulatory networks diverge between species, their dysfunctional expression in inter-species hybrid individuals can create genetic incompatibilities that generate the developmental defects responsible for intrinsic post-zygotic reproductive isolation. Both cis- and trans-acting regulatory divergence can be hastened by directional selection through adaptation, sexual selection, and inter-sexual conflict, in addition to cryptic evolution under stabilizing selection. Dysfunctional sex-biased gene expression, in particular, may provide an important source of sexually-dimorphic genetic incompatibilities. Here, we characterize and compare male and female/hermaphrodite transcriptome profiles for sibling nematode species Caenorhabditis briggsae and C. nigoni, along with allele-specific expression in their F1 hybrids, to deconvolve features of expression divergence and regulatory dysfunction. Despite evidence of widespread stabilizing selection on gene expression, misexpression of sex-biased genes pervades F1 hybrids of both sexes. This finding implicates greater fragility of male genetic networks to produce dysfunctional organismal phenotypes. Spermatogenesis genes are especially prone to high divergence in both expression and coding sequences, consistent with a “faster male” model for Haldane’s rule and elevated sterility of hybrid males. Moreover, underdominant expression pervades male-biased genes compared to female-biased and sex-neutral genes and an excess of cis-trans compensatory regulatory divergence for X-linked genes underscores a “large-X effect” for hybrid male expressionmore »
- Authors:
-
[1];
[2];
[1]
- Univ. of Toronto, ON (Canada). Dept. of Ecologyand Evolutionary Biology
- Univ. of Toronto, ON (Canada). Dept. of Ecologyand Evolutionary Biology; Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
- Publication Date:
- Sponsoring Org.:
- USDOE National Nuclear Security Administration (NNSA); Natural Science and Engineering Research Council of Canada; University of Toronto
- OSTI Identifier:
- 1815800
- Grant/Contract Number:
- 89233218CNA000001
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PLoS Genetics
- Additional Journal Information:
- Journal Volume: 17; Journal Issue: 3; Journal ID: ISSN 1553-7404
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; gene expression; gene regulation; X chromosomes; evolutionary genetics; x-linked traits; autosomes; genomics; spermatogensis
Citation Formats
Sánchez-Ramírez, Santiago, Weiss, Jörg G., Thomas, Cristel G., and Cutter, Asher D. Widespread misregulation of inter-species hybrid transcriptomes due to sex-specific and sex-chromosome regulatory evolution. United States: N. p., 2021.
Web. doi:10.1371/journal.pgen.1009409.
Sánchez-Ramírez, Santiago, Weiss, Jörg G., Thomas, Cristel G., & Cutter, Asher D. Widespread misregulation of inter-species hybrid transcriptomes due to sex-specific and sex-chromosome regulatory evolution. United States. https://doi.org/10.1371/journal.pgen.1009409
Sánchez-Ramírez, Santiago, Weiss, Jörg G., Thomas, Cristel G., and Cutter, Asher D. Fri .
"Widespread misregulation of inter-species hybrid transcriptomes due to sex-specific and sex-chromosome regulatory evolution". United States. https://doi.org/10.1371/journal.pgen.1009409. https://www.osti.gov/servlets/purl/1815800.
@article{osti_1815800,
title = {Widespread misregulation of inter-species hybrid transcriptomes due to sex-specific and sex-chromosome regulatory evolution},
author = {Sánchez-Ramírez, Santiago and Weiss, Jörg G. and Thomas, Cristel G. and Cutter, Asher D.},
abstractNote = {When gene regulatory networks diverge between species, their dysfunctional expression in inter-species hybrid individuals can create genetic incompatibilities that generate the developmental defects responsible for intrinsic post-zygotic reproductive isolation. Both cis- and trans-acting regulatory divergence can be hastened by directional selection through adaptation, sexual selection, and inter-sexual conflict, in addition to cryptic evolution under stabilizing selection. Dysfunctional sex-biased gene expression, in particular, may provide an important source of sexually-dimorphic genetic incompatibilities. Here, we characterize and compare male and female/hermaphrodite transcriptome profiles for sibling nematode species Caenorhabditis briggsae and C. nigoni, along with allele-specific expression in their F1 hybrids, to deconvolve features of expression divergence and regulatory dysfunction. Despite evidence of widespread stabilizing selection on gene expression, misexpression of sex-biased genes pervades F1 hybrids of both sexes. This finding implicates greater fragility of male genetic networks to produce dysfunctional organismal phenotypes. Spermatogenesis genes are especially prone to high divergence in both expression and coding sequences, consistent with a “faster male” model for Haldane’s rule and elevated sterility of hybrid males. Moreover, underdominant expression pervades male-biased genes compared to female-biased and sex-neutral genes and an excess of cis-trans compensatory regulatory divergence for X-linked genes underscores a “large-X effect” for hybrid male expression dysfunction. Extensive regulatory divergence in sex determination pathway genes likely contributes to demasculinization of XX hybrids. The evolution of genetic incompatibilities due to regulatory versus coding sequence divergence, however, are expected to arise in an uncorrelated fashion. This study identifies important differences between the sexes in how regulatory networks diverge to contribute to sex-biases in how genetic incompatibilities manifest during the speciation process.},
doi = {10.1371/journal.pgen.1009409},
journal = {PLoS Genetics},
number = 3,
volume = 17,
place = {United States},
year = {Fri Mar 05 00:00:00 EST 2021},
month = {Fri Mar 05 00:00:00 EST 2021}
}
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Works referenced in this record:
Misregulation of Gene Expression and Sterility in Interspecies Hybrids: Causal Links and Alternative Hypotheses
journal, March 2016
- Civetta, Alberto
- Journal of Molecular Evolution, Vol. 82, Issue 4-5
RNA-Seq Analysis of Allele-Specific Expression, Hybrid Effects, and Regulatory Divergence in Hybrids Compared with Their Parents from Natural Populations
journal, May 2013
- Bell, Graeme D. M.; Kane, Nolan C.; Rieseberg, Loren H.
- Genome Biology and Evolution, Vol. 5, Issue 7
Reproductive transitions in plants and animals: selfing syndrome, sexual selection and speciation
journal, June 2019
- Cutter, Asher D.
- New Phytologist, Vol. 224, Issue 3
Genome-wide germline-enriched and sex-biased expression profiles in Caenorhabditis elegans
journal, January 2004
- Reinke, Valerie; Gil, Inigo San; Ward, Samuel
- Development, Vol. 131, Issue 2
Genetic Variation for Postzygotic Reproductive Isolation Between Caenorhabditis Briggsae and Caenorhabditis sp. 9: Genetic Variation for Postzygotic Reproductive Isolation
journal, December 2011
- Kozlowska, Joanna L.; Ahmad, Abeer R.; Jahesh, Elnaz
- Evolution, Vol. 66, Issue 4
Insights Into Species Divergence and the Evolution of Hermaphroditism From Fertile Interspecies Hybrids of Caenorhabditis Nematodes
journal, November 2010
- Woodruff, Gavin C.; Eke, Onyinyechi; Baird, Scott E.
- Genetics, Vol. 186, Issue 3
WormBase ParaSite − a comprehensive resource for helminth genomics
journal, July 2017
- Howe, Kevin L.; Bolt, Bruce J.; Shafie, Myriam
- Molecular and Biochemical Parasitology, Vol. 215
Divergence Times in Caenorhabditis and Drosophila Inferred from Direct Estimates of the Neutral Mutation Rate
journal, February 2008
- Cutter, A. D.
- Molecular Biology and Evolution, Vol. 25, Issue 4
Differential expression analysis for sequence count data
journal, October 2010
- Anders, Simon; Huber, Wolfgang
- Genome Biology, Vol. 11, Issue 10
Additivity and trans-acting Effects on Gene Expression in Male Drosophila simulans
journal, November 2004
- Wayne, M. L.; Pan, Y-J; Nuzhdin, S. V.
- Genetics, Vol. 168, Issue 3
Sources of bias in measures of allele-specific expression derived from RNA-seq data aligned to a single reference genome
journal, August 2013
- Stevenson, Kraig R.; Coolon, Joseph D.; Wittkopp, Patricia J.
- BMC Genomics, Vol. 14, Issue 1
Genome-wide misexpression of X-linked versus autosomal genes associated with hybrid male sterility
journal, May 2010
- Lu, X.; Shapiro, J. A.; Ting, C. -T.
- Genome Research, Vol. 20, Issue 8
Trimmomatic: a flexible trimmer for Illumina sequence data
journal, April 2014
- Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern
- Bioinformatics, Vol. 30, Issue 15
Turning Clustering Loops: Sex Determination in Caenorhabditis elegans
journal, February 2002
- Goodwin, Elizabeth B.; Ellis, Ronald E.
- Current Biology, Vol. 12, Issue 3
The ‘effective number of codons’ used in a gene
journal, March 1990
- Wright, Frank
- Gene, Vol. 87, Issue 1
featureCounts: an efficient general purpose program for assigning sequence reads to genomic features
journal, November 2013
- Liao, Y.; Smyth, G. K.; Shi, W.
- Bioinformatics, Vol. 30, Issue 7
Compensatory cis-trans Evolution and the Dysregulation of Gene Expression in Interspecific Hybrids of Drosophila
journal, September 2005
- Landry, Christian R.; Wittkopp, Patricia J.; Taubes, Clifford H.
- Genetics, Vol. 171, Issue 4
Effect of read-mapping biases on detecting allele-specific expression from RNA-sequencing data
journal, October 2009
- Degner, Jacob F.; Marioni, John C.; Pai, Athma A.
- Bioinformatics, Vol. 25, Issue 24
Simplification and Desexualization of Gene Expression in Self-Fertile Nematodes
journal, November 2012
- Thomas, Cristel G.; Li, Renhua; Smith, Harold E.
- Current Biology, Vol. 22, Issue 22
Polyester : simulating RNA-seq datasets with differential transcript expression
journal, April 2015
- Frazee, Alyssa C.; Jaffe, Andrew E.; Langmead, Ben
- Bioinformatics, Vol. 31, Issue 17
Getting Started in Gene Orthology and Functional Analysis
journal, March 2010
- Fang, Gang; Bhardwaj, Nitin; Robilotto, Rebecca
- PLoS Computational Biology, Vol. 6, Issue 3
Evolution of New cis-Regulatory Motifs Required for Cell-Specific Gene Expression in Caenorhabditis
journal, September 2016
- Barkoulas, Michalis; Vargas Velazquez, Amhed M.; Peluffo, Alexandre E.
- PLOS Genetics, Vol. 12, Issue 9
Sex-specific Trans-regulatory Variation on the Drosophila melanogaster X Chromosome
journal, February 2015
- Stocks, Michael; Dean, Rebecca; Rogell, Björn
- PLOS Genetics, Vol. 11, Issue 2
Anomalies in the Expression Profile of Interspecific Hybrids of Drosophila melanogaster and Drosophila simulans
journal, March 2004
- Ranz, J. M.
- Genome Research, Vol. 14, Issue 3
What the X Has to Do with It: Differences in Regulatory Variability between the Sexes in Drosophila simulans
journal, April 2014
- Graze, Rita M.; McIntyre, Lauren M.; Morse, Alison M.
- Genome Biology and Evolution, Vol. 6, Issue 4
Genomic Networks of Hybrid Sterility
journal, February 2014
- Turner, Leslie M.; White, Michael A.; Tautz, Diethard
- PLoS Genetics, Vol. 10, Issue 2
Genomic basis of recombination suppression in the hybrid between Caenorhabditis briggsae and C. nigoni
journal, January 2018
- Ren, Xiaoliang; Li, Runsheng; Wei, Xiaolin
- Nucleic Acids Research, Vol. 46, Issue 3
Genetics of postzygotic isolation and Haldane's rule in haplodiploids
journal, June 2008
- Koevoets, T.; Beukeboom, L. W.
- Heredity, Vol. 102, Issue 1
Regulatory divergence in Drosophila revealed by mRNA-seq
journal, March 2010
- McManus, C. J.; Coolon, J. D.; Duff, M. O.
- Genome Research, Vol. 20, Issue 6
Evolution of gene sequence and gene expression are not correlated in yeast
journal, March 2008
- Tirosh, Itay; Barkai, Naama
- Trends in Genetics, Vol. 24, Issue 3
Sexual Selection and Maintenance of Sex: Evidence from Comparisons of Rates of Genomic Accumulation of Mutations and Divergence of Sex-Related Genes in Sexual and Hermaphroditic Species of Caenorhabditis
journal, February 2008
- Artieri, C. G.; Haerty, W.; Gupta, B. P.
- Molecular Biology and Evolution, Vol. 25, Issue 5
The ‘effective number of codons’ revisited
journal, May 2004
- Fuglsang, Anders
- Biochemical and Biophysical Research Communications, Vol. 317, Issue 3
PHAST and RPHAST: phylogenetic analysis with space/time models
journal, December 2010
- Hubisz, M. J.; Pollard, K. S.; Siepel, A.
- Briefings in Bioinformatics, Vol. 12, Issue 1
Gene regulation and speciation in house mice
journal, February 2016
- Mack, Katya L.; Campbell, Polly; Nachman, Michael W.
- Genome Research, Vol. 26, Issue 4
Ecological speciation: Ecological speciation
journal, January 2005
- Rundle, Howard D.; Nosil, Patrik
- Ecology Letters, Vol. 8, Issue 3
Convergent evolution of sperm gigantism and the developmental origins of sperm size variability in Caenorhabditis nematodes: EVOLUTION AND DEVELOPMENT OF SPERM SIZE VARIATION
journal, September 2016
- Vielle, Anne; Callemeyn-Torre, Nicolas; Gimond, Clotilde
- Evolution, Vol. 70, Issue 11
The dominance theory of Haldane's rule.
journal, May 1995
- Turelli, M.; Orr, H. A.
- Genetics, Vol. 140, Issue 1
Hybrid male sterility and genome-wide misexpression of male reproductive proteases
journal, July 2015
- Gomes, Suzanne; Civetta, Alberto
- Scientific Reports, Vol. 5, Issue 1
Specific down-regulation of spermatogenesis genes targeted by 22G RNAs in hybrid sterile males associated with an X-Chromosome introgression
journal, May 2016
- Li, Runsheng; Ren, Xiaoliang; Bi, Yu
- Genome Research, Vol. 26, Issue 9
OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy
journal, August 2015
- Emms, David M.; Kelly, Steven
- Genome Biology, Vol. 16, Issue 1
The reduction in fixation probability caused by substitutions at linked loci
journal, December 1994
- Barton, N. H.
- Genetical Research, Vol. 64, Issue 3
Natural selection on gene expression
journal, August 2006
- Gilad, Yoav; Oshlack, Alicia; Rifkin, Scott A.
- Trends in Genetics, Vol. 22, Issue 8
Pervasive Divergence of Transcriptional Gene Regulation in Caenorhabditis Nematodes
journal, June 2014
- Barrière, Antoine; Ruvinsky, Ilya
- PLoS Genetics, Vol. 10, Issue 6
Sex Determination: TRA-1 Is a Non-binary Regulator of Sexual Identity
journal, September 2020
- Ellis, Ronald E.
- Current Biology, Vol. 30, Issue 18
The Rapid Evolution of X-linked Male-Biased Gene Expression and the Large-X Effect in Drosophila yakuba, D. santomea, and Their Hybrids
journal, July 2012
- Llopart, Ana
- Molecular Biology and Evolution, Vol. 29, Issue 12
A New Dataset of Spermatogenic vs. Oogenic Transcriptomes in the Nematode Caenorhabditis elegans
journal, September 2014
- Ortiz, Marco A.; Noble, Daniel; Sorokin, Elena P.
- G3 Genes|Genomes|Genetics, Vol. 4, Issue 9
Allelic Variation in Human Gene Expression
journal, August 2002
- Yan, Hai; Yuan, Weishi; Velculescu, Victor E.
- Science, Vol. 297, Issue 5584, p. 1143-1143
Gene Regulation and Speciation
journal, January 2017
- Mack, Katya L.; Nachman, Michael W.
- Trends in Genetics, Vol. 33, Issue 1
STAR: ultrafast universal RNA-seq aligner
journal, October 2012
- Dobin, Alexander; Davis, Carrie A.; Schlesinger, Felix
- Bioinformatics, Vol. 29, Issue 1
Males, Outcrossing, and Sexual Selection in Caenorhabditis Nematodes
journal, September 2019
- Cutter, Asher D.; Morran, Levi T.; Phillips, Patrick C.
- Genetics, Vol. 213, Issue 1
3′ UTRs Are the Primary Regulators of Gene Expression in the C. elegans Germline
journal, October 2008
- Merritt, Christopher; Rasoloson, Dominique; Ko, Darae
- Current Biology, Vol. 18, Issue 19
The population genetics of speciation: the evolution of hybrid incompatibilities.
journal, April 1995
- Orr, H. A.
- Genetics, Vol. 139, Issue 4
The Relative Rates of Evolution of Sex Chromosomes and Autosomes
journal, July 1987
- Charlesworth, B.; Coyne, J. A.; Barton, N. H.
- The American Naturalist, Vol. 130, Issue 1
Comparative genomics of 10 new Caenorhabditis species
journal, April 2019
- Stevens, Lewis; Félix, Marie‐Anne; Beltran, Toni
- Evolution Letters, Vol. 3, Issue 2
The Evolution of Gene Expression in cis and trans
journal, July 2018
- Signor, Sarah A.; Nuzhdin, Sergey V.
- Trends in Genetics, Vol. 34, Issue 7
Transvection regulates the sex-biased expression of a fly X-linked gene
journal, January 2021
- Galouzis, Charalampos Chrysovalantis; Prud’homme, Benjamin
- Science, Vol. 371, Issue 6527
Coevolution within and between Regulatory Loci Can Preserve Promoter Function Despite Evolutionary Rate Acceleration
journal, September 2012
- Barrière, Antoine; Gordon, Kacy L.; Ruvinsky, Ilya
- PLoS Genetics, Vol. 8, Issue 9
The evolutionary significance of cis-regulatory mutations
journal, March 2007
- Wray, Gregory A.
- Nature Reviews Genetics, Vol. 8, Issue 3
Faster-X Evolution of Gene Expression in Drosophila
journal, October 2012
- Meisel, Richard P.; Malone, John H.; Clark, Andrew G.
- PLoS Genetics, Vol. 8, Issue 10
Comparative Genetics of Sex Determination: Masculinizing Mutations in Caenorhabditis briggsae
journal, March 2008
- Kelleher, Danielle F.; de Carvalho, Carlos Egydio; Doty, Alana V.
- Genetics, Vol. 178, Issue 3
Sex Chromosomes and the Evolution of Sexual Dimorphism
journal, July 1984
- Rice, William R.
- Evolution, Vol. 38, Issue 4
Trends, Stasis, and Drift in the Evolution of Nematode Vulva Development
journal, November 2007
- Kiontke, Karin; Barrière, Antoine; Kolotuev, Irina
- Current Biology, Vol. 17, Issue 22
A Yeast Hybrid Provides Insight into the Evolution of Gene Expression Regulation
journal, April 2009
- Tirosh, I.; Reikhav, S.; Levy, A. A.
- Science, Vol. 324, Issue 5927
Evolution of Postmating Reproductive Isolation: The Composite Nature of Haldane's Rule and Its Genetic Bases
journal, August 1993
- Davis, Andrew W.
- The American Naturalist, Vol. 142, Issue 2
cis-Regulatory and Protein Evolution in Orthologous and Duplicate Genes
journal, August 2004
- Castillo-Davis, C. I.
- Genome Research, Vol. 14, Issue 8
Natural selection on cis and trans regulation in yeasts
journal, May 2010
- Emerson, J. J.; Hsieh, L. -C.; Sung, H. -M.
- Genome Research, Vol. 20, Issue 6
The roles of cis- and trans-regulation in the evolution of regulatory incompatibilities and sexually dimorphic gene expression
journal, September 2013
- Meiklejohn, C. D.; Coolon, J. D.; Hartl, D. L.
- Genome Research, Vol. 24, Issue 1
Gene Expression Divergence and Hybrid Misexpression between Lake Whitefish Species Pairs (Coregonus spp. Salmonidae)
journal, January 2009
- Renaut, S.; Nolte, A. W.; Bernatchez, L.
- Molecular Biology and Evolution, Vol. 26, Issue 4
Tempo and Mode in Evolution of Transcriptional Regulation
journal, January 2012
- Gordon, Kacy L.; Ruvinsky, Ilya
- PLoS Genetics, Vol. 8, Issue 1
X exceptionalism in Caenorhabditis speciation
journal, December 2017
- Cutter, Asher D.
- Molecular Ecology, Vol. 27, Issue 19
The loci of Evolution: how Predictable is Genetic Evolution?
journal, September 2008
- Stern, David L.; Orgogozo, Virginie
- Evolution, Vol. 62, Issue 9
A mutation accumulation assay reveals a broad capacity for rapid evolution of gene expression
journal, November 2005
- Rifkin, Scott A.; Houle, David; Kim, Junhyong
- Nature, Vol. 438, Issue 7065
Evolutionary changes in cis and trans gene regulation
journal, July 2004
- Wittkopp, Patricia J.; Haerum, Belinda K.; Clark, Andrew G.
- Nature, Vol. 430, Issue 6995
A Streamlined System for Species Diagnosis in Caenorhabditis (Nematoda: Rhabditidae) with Name Designations for 15 Distinct Biological Species
journal, April 2014
- Félix, Marie-Anne; Braendle, Christian; Cutter, Asher D.
- PLoS ONE, Vol. 9, Issue 4
Regulatory changes underlying expression differences within and between Drosophila species
journal, February 2008
- Wittkopp, Patricia J.; Haerum, Belinda K.; Clark, Andrew G.
- Nature Genetics, Vol. 40, Issue 3
Full-genome evolutionary histories of selfing, splitting, and selection in Caenorhabditis
journal, March 2015
- Thomas, Cristel G.; Wang, Wei; Jovelin, Richard
- Genome Research, Vol. 25, Issue 5
The transcriptional consequences of mutation and natural selection in Caenorhabditis elegans
journal, April 2005
- Denver, Dee R.; Morris, Krystalynne; Streelman, J. Todd
- Nature Genetics, Vol. 37, Issue 5
Cis- and trans-regulatory divergence between progenitor species determines gene-expression novelty in Arabidopsis allopolyploids
journal, January 2012
- Shi, Xiaoli; Ng, Danny W-K.; Zhang, Changqing
- Nature Communications, Vol. 3, Issue 1
Specific Interactions Between Autosome and X Chromosomes Cause Hybrid Male Sterility in Caenorhabditis Species
journal, May 2019
- Bi, Yu; Ren, Xiaoliang; Li, Runsheng
- Genetics, Vol. 212, Issue 3
Dominance and the evolutionary accumulation of cis- and trans-effects on gene expression
journal, September 2008
- Lemos, B.; Araripe, L. O.; Fontanillas, P.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 38
BEDTools: a flexible suite of utilities for comparing genomic features
journal, January 2010
- Quinlan, Aaron R.; Hall, Ira M.
- Bioinformatics, Vol. 26, Issue 6
Evaluating genomic signatures of “the large X-effect” during complex speciation
journal, July 2018
- Presgraves, Daven C.
- Molecular Ecology, Vol. 27, Issue 19
Haldane’s Rule: Genetic Bases and Their Empirical Support
journal, May 2016
- Delph, Lynda F.; Demuth, Jeffery P.
- Journal of Heredity, Vol. 107, Issue 5
Dramatic evolution of body length due to postembryonic changes in cell size in a newly discovered close relative of Caenorhabditis elegans: BODY SIZE EVOLUTION IN CAENORHABDITIS
journal, July 2018
- Woodruff, Gavin C.; Willis, John H.; Phillips, Patrick C.
- Evolution Letters, Vol. 2, Issue 4
Reproductive Mode and the Evolution of Genome Size and Structure in Caenorhabditis Nematodes
journal, June 2015
- Fierst, Janna L.; Willis, John H.; Thomas, Cristel G.
- PLOS Genetics, Vol. 11, Issue 6
Comparative RNAi Screens in C. elegans and C. briggsae Reveal the Impact of Developmental System Drift on Gene Function
journal, February 2014
- Verster, Adrian J.; Ramani, Arun K.; McKay, Sheldon J.
- PLoS Genetics, Vol. 10, Issue 2
Sexual and Temporal Dynamics of Molecular Evolution in C. elegans Development
journal, September 2004
- Cutter, Asher D.; Ward, Samuel
- Molecular Biology and Evolution, Vol. 22, Issue 1
Genomic sources of regulatory variation in cis and in trans
journal, June 2005
- Wittkopp, P. J.
- Cellular and Molecular Life Sciences, Vol. 62, Issue 16
The Genomics of Sexual Conflict
journal, August 2018
- Rowe, Locke; Chenoweth, Stephen F.; Agrawal, Aneil F.
- The American Naturalist, Vol. 192, Issue 2
Optimization of gene expression by natural selection
journal, January 2009
- Bedford, T.; Hartl, D. L.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 4
Rates of Divergence in gene Expression Profiles of Primates, Mice, and Flies: Stabilizing Selection and Variability Among Functional Categories
journal, January 2005
- Lemos, Bernardo; Meiklejohn, Colin D.; Cáceres, Mario
- Evolution, Vol. 59, Issue 1
Natural selection shapes nucleotide polymorphism across the genome of the nematode Caenorhabditis briggsae
journal, May 2010
- Cutter, A. D.; Choi, J. Y.
- Genome Research, Vol. 20, Issue 8
Developmental system drift and flexibility in evolutionary trajectories
journal, March 2001
- True, John R.; Haag, Eric S.
- Evolution and Development, Vol. 3, Issue 2
Genomic Signatures of Sexual Conflict
journal, September 2017
- Kasimatis, Katja R.; Nelson, Thomas C.; Phillips, Patrick C.
- Journal of Heredity, Vol. 108, Issue 7
Asymmetric Postmating Isolation: Darwin's Corollary to Haldane's Rule
journal, June 2007
- Turelli, Michael; Moyle, Leonie C.
- Genetics, Vol. 176, Issue 2
High-Resolution Genome-Wide Dissection of the Two Rules of Speciation in Drosophila
journal, September 2007
- Masly, John P.; Presgraves, Daven C.
- PLoS Biology, Vol. 5, Issue 9
MAFFT version 5: improvement in accuracy of multiple sequence alignment
journal, January 2005
- Katoh, K.
- Nucleic Acids Research, Vol. 33, Issue 2
Rapid genome shrinkage in a self-fertile nematode reveals sperm competition proteins
journal, January 2018
- Yin, Da; Schwarz, Erich M.; Thomas, Cristel G.
- Science, Vol. 359, Issue 6371
Gene expression divergence and the origin of hybrid dysfunctions
journal, October 2006
- Ortíz-Barrientos, Daniel; Counterman, Brian A.; Noor, Mohamed A. F.
- Genetica, Vol. 129, Issue 1
Gametic selection, developmental trajectories, and extrinsic heterogeneity in Haldane's rule: HETEROGENEITY IN HALDANE’S RULE
journal, July 2015
- Bundus, Joanna D.; Alaei, Ravin; Cutter, Asher D.
- Evolution, Vol. 69, Issue 8
The quantitative genetics of transcription
journal, November 2005
- Gibson, Greg; Weir, Bruce
- Trends in Genetics, Vol. 21, Issue 11
Developmental expression of FOG-1/CPEB protein and its control in theCaenorhabditis elegans hermaphrodite germ line
journal, January 2007
- Lamont, Liana B.; Kimble, Judith
- Developmental Dynamics, Vol. 236, Issue 3
A Genome-Wide Hybrid Incompatibility Landscape between Caenorhabditis briggsae and C. nigoni
journal, February 2015
- Bi, Yu; Ren, Xiaoliang; Yan, Cheung
- PLOS Genetics, Vol. 11, Issue 2