Evolution of X‐Linked Male‐Biased Genes in Drosophila

Abstract

Sex chromosomes, particularly the X chromosome, play a unique role in evolution due to several distinct features. In Drosophila, the X chromosome has been proposed to constitute an undesirable environment for genes expressed at higher levels in males than in females (i.e. male‐biased genes) and, as a result, is partially demasculinized. However, male‐biased genes remaining on the X chromosome do not seem to be at a disadvantage relative to their autosomal counterparts. Population genetic models predict that under certain conditions X‐linked genes will experience more bouts of positive selection than autosomal genes, leading to faster‐X evolution, particularly for male‐biased genes. As theory posits, Drosophila X‐linked male‐biased genes show evidence of adaptive evolution at both protein and expression levels. This faster‐X evolution has broad implications. In speciation, it may contribute to explain why the X chromosome is a hotspot for the genetic factors underlying hybrid male sterility (i.e. the large X‐effect).

Key Concepts:

  • Underrepresentation of X‐linked male‐biased genes due to unfavorable features of the X chromosome.

  • Faster‐X evolution of male‐biased genes at both the protein and expression levels.

  • Consequences of faster‐X evolution include the disproportionally large effect of the X chromosome in hybrid male sterility.

Keywords: X chromosome; sexual antagonism; meiotic sex chromosome inactivation; dosage compensation; faster‐X; gene expression; large X‐effect; speciation; adaptive evolution; positive selection

Figure 1.

Percentage of genes with male‐, female‐ and nonsex‐biased expression on the X chromosome (X) and autosomes (A) in D. melanogaster and D. pseudoobscura (Sturgill et al., ).

Figure 2.

The ratio of the X chromosomal to autosomal rates of evolution for beneficial and mildly deleterious mutations in male‐specific (solid line) and nonsex‐biased (dashed line) genes. Selection is set to Ne×s =−10 and +10 for deleterious and beneficial mutations respectively, where Ne is the effective population size and s is the selection coefficient. The NeX to NeA ratio is set to 0.75.

Figure 3.

(a) Gene expression divergence between D. yakuba and D. santomea for all genes, male‐biased genes and nonsex‐biased genes on the X chromosome (X) and autosomes (A). The number of genes analysed in each class of genes is indicated. (b) Gene expression divergence between D. yakuba and D. santomea for all gene types divided into three equally sized categories of genes with broad, intermediate, and narrow expression (Yanai et al., ). Medians with 50% and 90% confidence intervals are shown (Llopart, ).

Figure 4.

Percentage of interspecies X‐linked and autosomal introgressions that result in fertile and sterile hybrid males of D. mauritiana and D. sechellia (Masly and Presgraves, ).

Figure 5.

Percentages of genes differentially expressed between D. melanogaster and D. sechellia, and D. yakuba and D. santomea due to changes in only cis‐, only trans‐, or both cis‐ and trans‐acting regulatory factors (Llopart, ; Mcmanus et al., ).

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How to Cite close
Herrig, Danielle K, and Llopart, Ana(Jul 2014) Evolution of X‐Linked Male‐Biased Genes in Drosophila. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0025537]