Abstract
Stalk-eyed flies (family Diopsidae) are a model system for studying sexual selection due to the elongated and sexually dimorphic eye-stalks found in many species. These flies are of additional interest because their X chromosome is derived largely from an autosomal arm in other flies. To identify candidate genes required for development of dimorphic eyestalks and investigate how sex-biased expression arose on the novel X, we compared gene expression between males and females using oligonucleotide microarrays and RNA from developing eyestalk tissue or adult heads in the dimorphic diopsid, Teleopsis dalmanni. Microarray analysis revealed sex-biased expression for 26% of 3,748 genes expressed in eye-antennal imaginal discs and concordant sex-biased expression for 86 genes in adult heads. Overall, 415 female-biased and 482 male-biased genes were associated with dimorphic eyestalk development but not differential expression in the adult head. Functional analysis revealed that male-biased genes are disproportionately associated with growth and mitochondrial function while female-biased genes are associated with cell differentiation and patterning or are novel transcripts. With regard to chromosomal effects, dosage compensation occurs by elevated expression of X-linked genes in males. Genes with female-biased expression were more common on the X and less common on autosomes than expected, while male-biased genes exhibited no chromosomal pattern. Rates of protein evolution were lower for female-biased genes but higher for genes that moved on or off the novel X chromosome. These findings cannot be due to meiotic sex chromosome inactivation or by constraints associated with dosage compensation. Instead, they could be consistent with sexual conflict in which female-biased genes on the novel X act primarily to reduce eyespan in females while other genes increase eyespan in both sexes. Additional information on sex-biased gene expression in other tissues and related sexually monomorphic species could confirm this interpretation.
Highlights
The evolution of sexual dimorphism requires differential selection such that a trait advantageous in one sex is deleterious in the opposite sex [1]
Fly stocks Adult and larval flies were reared in the lab from large outbred populations of Teleopsis dalmanni that were originally collected near the village of Ulu Gombak in peninsular Malaysia in 1999
Sex-biased expression in larval and adult heads Examination of hybridization patterns for eye-antennal imaginal disc and adult head tissue samples indicated that most of the 3,748 genes on the array were expressed in both tissues
Summary
The evolution of sexual dimorphism requires differential selection such that a trait advantageous in one sex is deleterious in the opposite sex [1]. When trait expression has a genetic basis, development of sexual dimorphism requires differential gene expression between the sexes at some point during development This can arise either by sex-biased expression or by genes relocating to a sex chromosome or both. Selection for femalebeneficial alleles should be stronger for X-linked than autosomal genes because genes on the X chromosome are exposed to selection in males half as often as in females, assuming an equal sex ratio. These predictions change, if dominance varies [4] or is context dependent [5]. Genes that affect expression of a sexually selected trait in males are generally expected to increase in frequency more rapidly when on an autosome or on the Y than on the X [6], X chromosome segregation distortion can lead to the opposite prediction [7]
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