Genome-wide patterns of regulatory divergence revealed by introgression lines

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 bi-allelic 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.

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“…; Guerrero et al. ). The vast majority of these transgressive differences were restricted to large S×C hybrids (Fig.…”

Section: Resultsmentioning

confidence: 96%

Genomic imprinting, disrupted placental expression, and speciation

2016

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“…In these cases, inferences about the gene expression changes associated with species barriers can only be drawn at the most general level, especially in the absence of a priori candidate loci (Guerrero et al . ).…”

Section: Discussionmentioning

confidence: 97%

Molecular mechanisms of postmating prezygotic reproductive isolation uncovered by transcriptome analysis

et al. 2016

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Little is known about the physiological responses and genetic mutations associated with reproductive isolation between species, especially for postmating prezygotic isolating barriers. Here, we examine changes in gene expression that accompany the expression of 'unilateral incompatibility' (UI)-a postmating prezygotic barrier in which fertilization is prevented by gamete rejection in the reproductive tract [in this case of pollen tubes (male gametophytes)] in one direction of a species cross, but is successful in the reciprocal crossing direction. We use whole-transcriptome sequencing of multiple developmental stages of male and female tissues in two Solanum species that exhibit UI to: (i) identify transcript differences between UI-competent and UI noncompetent tissues; (ii) characterize transcriptional changes specifically associated with the phenotypic expression of UI; and (iii) using these comparisons, evaluate the behaviour of a priori candidate loci for UI and identify new candidates for future manipulative work. In addition to describing transcriptome-wide changes in gene expression that accompany this isolating barrier, we identify at least five strong candidates for involvement in postmating prezygotic incompatibility between species. These include three novel candidates and two candidates that are strongly supported by prior developmental, functional, and quantitative trait locus mapping studies. These latter genes are known molecular players in the intraspecific expression of mate choice via genetic self-incompatibility, and our study supports prior evidence that these inter-and intraspecific postmating prezygotic reproductive behaviours share specific genetic and molecular mechanisms.

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“…For faster-X expression divergence, this would require that differences in transcript abundances are due to divergence in cis-regulatory elements and/or X-linked trans-regulatory elements (Kayserili et al 2012;Meisel et al 2012a;Meisel and Connallon 2013). Several studies suggest that divergence in transcript abundances is largely determined by evolution in cis (Wittkopp et al 2004;Landry et al 2005;Wittkopp et al 2008;Graze et al 2009;Goncalves et al 2012;Shi et al 2012;Shen et al 2014;Mack et al 2016), while other research indicates that trans-regulatory divergence is more common (Emerson et al 2010;McManus et al 2010;Schaefke et al 2013;Coolon et al 2014;Meiklejohn et al 2014;Combes et al 2015) or that the inferred mode of regulatory divergence is dependent on taxon and experimental design (Coolon and Wittkopp 2013;Guerrero et al 2016). The mechanisms underlying the evolution of DNA methylation are even more poorly understood, but levels of DNA methylation within a given genomic region appear strongly Faster-X sequence evolution also assumes that beneficial mutations are on average at least partially recessive (Charlesworth et al 1987), while theory (Gibson and Weir 2005) and several empirical studies (Lemos et al 2008;McManus et al 2010;Schaefke et al 2013) suggest that cis-regulatory elements should on average act additively.…”

Section: Regulatory Evolution and Spermatogenesismentioning

confidence: 99%

Contrasting Levels of Molecular Evolution on the Mouse X Chromosome

et al. 2016

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The mammalian X chromosome has unusual evolutionary dynamics compared to autosomes. Faster-X evolution of spermatogenic protein-coding genes is known to be most pronounced for genes expressed late in spermatogenesis, but it is unclear if these patterns extend to other forms of molecular divergence. We tested for faster-X evolution in mice spanning three different forms of molecular evolution-divergence in protein sequence, gene expression, and DNA methylation-across different developmental stages of spermatogenesis. We used FACS to isolate individual cell populations and then generated cell-specific transcriptome profiles across different stages of spermatogenesis in two subspecies of house mice (Mus musculus), thereby overcoming a fundamental limitation of previous studies on whole tissues. We found faster-X protein evolution at all stages of spermatogenesis and faster-late protein evolution for both X-linked and autosomal genes. In contrast, there was less expression divergence late in spermatogenesis (slower late) on the X chromosome and for autosomal genes expressed primarily in testis (testis-biased). We argue that slower-late expression divergence reflects strong regulatory constraints imposed during this critical stage of sperm development and that these constraints are particularly acute on the tightly regulated sex chromosomes. We also found slower-X DNA methylation divergence based on genome-wide bisulfite sequencing of sperm from two species of mice (M. musculus and M. spretus), although it is unclear whether slower-X DNA methylation reflects development constraints in sperm or other X-linked phenomena. Our study clarifies key differences in patterns of regulatory and protein evolution across spermatogenesis that are likely to have important consequences for mammalian sex chromosome evolution, male fertility, and speciation.KEYWORDS faster X evolution; gene expression; DNA methylation; fluorescence-activated cell sorting; postmeiotic sex chromosome repression (PSCR) T HE X chromosome plays a disproportionately large role in adaptation and speciation (Bachtrog et al. 2011;Ellegren 2011;Charlesworth 2013), but the underlying molecular and evolutionary drivers of these patterns remain unclear. On one hand, the X chromosome often shows strong signatures of evolutionary constraint. For example, the evolution of dosage compensation via epigenetic X-chromosome inactivation (XCI) in females (Lyon 1961(Lyon , 1962 imposes regulatory constraints that select for strong conservation of X-linked gene content in placental mammals (Ohno 1967;Kohn et al. 2004). On the other hand, these inherent constraints are punctuated by strong specialization in X-linked gene content (Emerson et al. 2004;Mueller et al. 2008Mueller et al. , 2013Potrzebowski et al. 2008;Zhang et al. 2010;Sin et al. 2012) and numerous examples of rapid X-linked evolution Singh 2003, 2006;Baines and Harr 2007;Kousathanas et al. 2014;Nam et al. 2015).The X chromosome is predicted to evolve faster than the autosomes if beneficial mutations...

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Genome-wide patterns of regulatory divergence revealed by introgression lines

Cited by 10 publications

References 48 publications

Genomic imprinting, disrupted placental expression, and speciation

Genomic imprinting, disrupted placental expression, and speciation

Molecular mechanisms of postmating prezygotic reproductive isolation uncovered by transcriptome analysis

Contrasting Levels of Molecular Evolution on the Mouse X Chromosome

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