Disproportionate Roles for the X Chromosome and Proteins in Adaptive Evolution

Abstract

A daptation requires genetic variation. A complete understanding of this key evolutionary process includes identification of the mutations that confer adaptive change. High-resolution genetic dissection of particular adaptive phenotypes can pinpoint these mutations, but this is a challenging task and the resulting conclusions are restricted to the traits under consideration.An alternative approach is to examine characteristics of adaptive mutations through the powerful lens of population genetics. By measuring intraspecific polymorphism and interspecific divergence across genomes, evolutionary properties of those mutations targeted by natural selection can be discovered. Under this framework as well, generalities are widely sought and difficult to identify. A useful way to make progress is to compare patterns of adaptive evolution among different categories of loci. Two contrasts are based on the genomic location of mutations: X linked vs. autosomal and protein coding vs. cis-regulatory (i.e., noncoding sequences that affect local gene expression). These contrasts have generated substantial interest because they are tied directly to basic questions about adaptive evolution.The fate of a beneficial mutation should depend on its mode of inheritance. This idea motivates comparisons between rates of adaptive evolution on the X chromosome and the autosomes. Recent, low-frequency recessive mutations are immediately exposed to selection in males when X-linked and are mostly hidden from selection (in heterozygotes) when autosomal. If beneficial mutations are at least partially recessive on average, they will fix faster on the X chromosome (Avery 1984), elevating the rate of evolution relative to autosomal loci. In an influential theoretical article, Charlesworth et al. (1987) quantified this connection between dominance and "faster X" evolution and identified the biological conditions under which it applies. With several assumptions, the relative rates of molecular evolution at X-linked and autosomal loci can even be used to estimate the average dominance of new advantageous mutations, an important quantity in evolutionary biology.The study of faster X evolution is also motivated by a desire to explain the outsized role of the X chromosome in speciation. In a wide variety of species pairs, the sterility and/or inviability of hybrids created by interspecific crosses maps differentially to the X chromosome (Coyne and Orr 2004). This bias seems to reflect a higher density of hybrid incompatibilities involving the X chromosome (Masly and Presgraves 2007).The prediction of faster X evolution has been tested repeatedly by comparing between-species divergence at X-linked and autosomal genes (Meisel and Connallon 2013). The most popular approach calculates the relative rate of substitution at nonsynonymous and synonymous sites, reasoning that nonsynonymous changes will often be targeted by selection. A flurry of studies featuring Drosophila revealed a range of support for faster X evolution (Betancourt et al. 2002;Thornton and ...

Sex chromosomes and speciation in birds and other ZW systems

“…Such a pattern was not observed (Mank, Nam, et al., ; Mank, Vicoso, et al., ; Wright et al., ), casting doubt on the idea that the faster‐Z effect is driven primarily by adaptation via recessive mutations in female‐expression‐biased genes. However, the relative ratio of dominance and recessivity in beneficial mutations is not well established (Payseur, ), and dominant mutations might be under more effective selection when male‐biased and Z‐linked (as Z‐linked genes are in males 2/3 of the time, whereas autosomal genes are in males only ½ of the time). The net effect of the two types of beneficial mutations (recessive female‐biased ones accumulating faster on the Z than autosomes; dominant male‐biased ones accumulating faster on the Z than autosomes) might result in the observed no net difference in the faster‐Z effect between male‐biased and female‐biased genes.…”

“…Such a pattern was not observed (Mank, Nam, et al, 2010;Mank, Vicoso, et al, 2010;Wright et al, 2015), casting doubt on the idea that the faster-Z effect is driven primarily by adaptation via recessive mutations in female-expression-biased genes. However, the relative ratio of dominance and recessivity in beneficial mutations is not well established (Payseur, 2014) alleles, such that we might expect a faster rate of Z evolution in male-biased genes (see also Ellegren, 2011b regarding the tendency of genes with male-biased expression to move to the Z, whereas those with female-biased expression tend to move away from the Z onto autosomes).…”

Faster‐X evolution of gene expression is driven by recessive adaptive cis‐regulatory variation in Drosophila

“…The analysis of estimates of individual α that capture local changes in effective population size across the genome reveals higher rates of adaptive evolution on the X chromosome than on autosomes. The differential behaviour of X‐linked and autosomal 5′ noncoding regions suggests that selection is very efficient on the X chromosome (Garrigan, Kingan, Geneva, Vedanayagam, & Presgraves, ; Parsch et al., ; Payseur, ). One possible explanation would be that the N e X / N e A is greater than 1 for these species.…”

Studies on the causes and consequences of sex determination in turtles

“…Could regulatory sequences be under greater adaptive evolution than coding sequences, as observed in rodents (Halligan et al 2013)? Importantly, hybrid sterility in inter--specific mice crosses maps disproportionately to sex--linked genes, implicating them as players in speciation events (Payseur 2014;White et al 2012). Studies like ours that thus provide new avenues in the form of reptilian evidences of differential rate of evolution of sex--linked--and TSD-specific sequences to study reptilian speciation and other consequences of independent sex chromosome incipience in reptiles.…”

“…This differentiation of sex chromosomes from autosomes was proposed over a century ago (Muller 1914) has generated many important debates. Some of the recalcitrant questions delve into whether or not there exists a differential mutation rate and a bias to accumulate genes bestowing sex--specific fitness between sex chromosomes and autosomes (Vicoso and Charlesworth 2006), the extent of global dosage compensation prevalence in sex chromosomes as postulated by Ohno (Ohno 1967), and the extent to which sex chromosomes affect the early stages of speciation (Payseur 2014). Indeed, certain sex-linked genes in mice have been disproportionately associated with hybrid sterility in interspecific crosses (White et al 2012).…”