Sex-differential selection and the evolution of X inactivation strategies.

Sex-differential selection and the evolution of X inactivation strategies.
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DOI:
10.1371/journal.pgen.1003440
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发表时间:
2013-04
期刊:
影响因子:
4.5
通讯作者:
Clark AG
Clark AG
中科院分区:
生物学2区
文献类型:
--
作者:
Connallon T;Clark AG

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X染色体失活-每个雌性体细胞一个X染色体拷贝的转录沉默-在兽目哺乳动物中是普遍的,但是选择哪个X染色体沉默在物种之间表现出相当大的差异。X失活策略的范围可以从严格的父系遗传X失活(PXI)到无偏的随机X失活(RXI),前者使所有母系遗传等位基因的雌性单倍体,后者使每个雌性组织中母系和父系遗传等位基因的表达相等。然而,潜在的进化过程,可能占这种观察到的多样性的X失活策略仍然不清楚。我们提出了一个理论群体遗传分析X失活进化,并特别考虑如何条件的优势,连锁,重组,性别差异选择每个影响X失活的进化轨迹。结果表明,等位基因显性和性别差异选择之间的一个单一的,关键的相互作用,可以选择一个广泛的和连续的X失活策略,包括不平等的失活率之间的母系和父系遗传的X染色体。只要对雌性适合度有害的等位基因是足够隐性的,RXI优于完全的PXI,并且当适合度变异是性拮抗的时,RXI进化的标准是相当多的限制性的(即,对雌性有害的等位基因对雄性有益)相对于对两性都有害的变异。从PXI到RXI的进化转变也普遍增加了平均相对女性健康,而牺牲了男性健康。这些结果提供了一个理论框架,用于预测和解释X连锁基因的染色体全表达的演变,并导致几个有用的预测,可以激励未来的等位基因特异性基因表达变异的研究。除了最原始的成员,哺乳动物物种的做法是X失活,其中每个X染色体对的一个副本在女性身体的每个细胞中沉默。然而,被沉默的X基因的特定拷贝在物种之间显示出相当大的变异性,这种变异性的进化原因仍然不清楚。在这里,我们表明,X失活策略很可能会演变的性别差异健身属性的X连锁遗传变异。对男性和女性适应性具有相似影响的遗传变异通常有利于随机X失活的进化,可能包括母系遗传X染色体的优先失活。在每种性别中具有相反适应性效应的变异(“性拮抗”变异,包括降低雌性适应性和增强雄性适应性的突变)选择优先或完全失活父系遗传的X。父系偏向的X染色体失活模式在自然界中普遍存在,这表明性拮抗遗传变异可能是X染色体失活进化的重要因素。该理论为理解X失活策略的演变提供了一个概念框架,并产生了几个新的预测,可能很快就会用现代基因组测序技术进行测试。
X inactivation—the transcriptional silencing of one X chromosome copy per female somatic cell—is universal among therian mammals, yet the choice of which X to silence exhibits considerable variation among species. X inactivation strategies can range from strict paternally inherited X inactivation (PXI), which renders females haploid for all maternally inherited alleles, to unbiased random X inactivation (RXI), which equalizes expression of maternally and paternally inherited alleles in each female tissue. However, the underlying evolutionary processes that might account for this observed diversity of X inactivation strategies remain unclear. We present a theoretical population genetic analysis of X inactivation evolution and specifically consider how conditions of dominance, linkage, recombination, and sex-differential selection each influence evolutionary trajectories of X inactivation. The results indicate that a single, critical interaction between allelic dominance and sex-differential selection can select for a broad and continuous range of X inactivation strategies, including unequal rates of inactivation between maternally and paternally inherited X chromosomes. RXI is favored over complete PXI as long as alleles deleterious to female fitness are sufficiently recessive, and the criteria for RXI evolution is considerably more restrictive when fitness variation is sexually antagonistic (i.e., alleles deleterious to females are beneficial to males) relative to variation that is deleterious to both sexes. Evolutionary transitions from PXI to RXI also generally increase mean relative female fitness at the expense of decreased male fitness. These results provide a theoretical framework for predicting and interpreting the evolution of chromosome-wide expression of X-linked genes and lead to several useful predictions that could motivate future studies of allele-specific gene expression variation. With the exception of its most primitive members, mammal species practice X inactivation, where one copy of each X chromosome pair is silenced in each cell of the female body. The particular copy of the X that is silenced nevertheless shows considerable variability among species, and the evolutionary causes for this variability remain unclear. Here, we show that X inactivation strategies are likely to evolve in response to the sex-differential fitness properties of X-linked genetic variation. Genetic variation with similar effects on male and female fitness will generally favor the evolution of random X inactivation, potentially including preferential inactivation of the maternally inherited X chromosome. Variation with opposing fitness effects in each sex (“sexually antagonistic” variation, which includes mutations that both decrease female fitness and enhance male fitness) selects for preferential or complete inactivation of the paternally inherited X. Paternally biased X inactivation patterns appear to be common in nature, which suggests that sexually antagonistic genetic variation might be an important factor underlying the evolution of X inactivation. The theory provides a conceptual framework for understanding the evolution of X inactivation strategies and generates several novel predictions that may soon be tested with modern genome sequencing technologies.
DOI: 10.1071/bi9760245
发表时间: 1976-01-01
期刊: AUSTRALIAN JOURNAL OF BIOLOGICAL SCIENCES
影响因子: --
作者:
COOPER, DW
通讯作者: COOPER, DW
DOI: 10.1111/j.1558-5646.2012.01584.x
发表时间: 2012-07-01
期刊: EVOLUTION
影响因子: 3.3
作者:
Arbuthnott, Devin;Rundle, Howard D.
通讯作者: Rundle, Howard D.
DOI: 10.1086/595841
发表时间: 2009-02-01
影响因子: 2.9
作者:
Cox, Robert M.;Calsbeek, Ryan
通讯作者: Calsbeek, Ryan
DOI: 10.1126/science.1185550
发表时间: 2010-04-02
期刊: SCIENCE
影响因子: 56.9
作者:
Cox, Robert M.;Calsbeek, Ryan
通讯作者: Calsbeek, Ryan
DOI: 10.1534/genetics.111.137117
发表时间: 2012-04-01
期刊: GENETICS
影响因子: 3.3
作者:
Connallon, Tim;Clark, Andrew G.
通讯作者: Clark, Andrew G.