Sex-Biased Gene Expression during Head Development in a Sexually Dimorphic Stalk-Eyed Fly

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.

A general mechanism for conditional expression of exaggerated sexually‐selected traits

“…Within invertebrates, increased expression of InR, the target receptor for ILPs, is observed within the soon to be terminated horn primordia of hornless dung beetles ( Onthophagus nigriventris ) , and in the developing eye‐stalks of female stalk‐eyed flies, Teleopsis dalmanni (Fig. ), which do not grow exaggerated eye‐stalks . These results are consistent with inactivation of the ILS pathway within these tissues, as would be seen when exaggerated traits were not being grown, resulting in the upregulation of InR by feedback from the downstream target FOXO (Fig.…”

Sexual dimorphism and heightened conditional expression in a sexually selected weapon in the Asian rhinoceros beetle

“…However, these studies − like all those focused on candidate genes − are limited and necessarily biased in scope due to their reliance on prior knowledge of gene function from related taxa. Several recent studies have leveraged high‐throughput sequencing (e.g., RNAseq) to provide transcriptome‐wide screens for differential gene expression associated with extreme trait growth (Gotoh et al., ; Kijimoto et al., ; Ledón‐Rettig & Moczek, ; Ledón‐Rettig, Zattara, & Moczek, ; Ozawa et al., ; Pointer, Harrison, Wright, & Mank, ; Wilkinson, Johns, Metheny, & Baker, ), providing unbiased glimpses into the genetic architecture of sexually selected traits.…”

“…In many ways, exaggerated sexually selected structures are ideal for transcriptome‐wide, differential expression approaches (Pointer et al., ; Stuglik, Babik, Prokop, & Radwan, ; Wilkinson et al., , ). Not only are these traits often sexually dimorphic, such that similar starting tissues undergo dramatically different amounts of growth in males and females, but these traits also differ from each other in the extent of their nutritional plasticity (Moczek, 2006; Moczek & Nagy, 2005).…”

The locus of sexual selection: moving sexual selection studies into the post‐genomics era

“…Although sexual selection is clearly an important source of sex‐specific selection, without additional functional genetic analysis it is not possible to determine whether the genes that show significant sex‐biased expression also encode or influence identifiable sexually selected phenotypes. Functional genetic analysis can be complicated because gene expression differences between females and males vary substantially throughout development (Mank et al ., ; Wilkinson et al ., ; Perry et al ., ) as well as across tissues (Yang et al ., ; Baker et al ., ); therefore, ontogenetic trajectories of sexually selected phenotypes must be determined to identify when and where differential gene expression triggers the development of sexually selected traits. Nevertheless, studies of gene expression in species with intrasexual variation in male phenotypes indicate that sexual selection does contribute substantially to sex‐biased gene expression patterns.…”