Spermatogenesis Drives Rapid Gene Creation and Masculinization of the X Chromosome in Stalk-Eyed Flies (Diopsidae)

Abstract

Throughout their evolutionary history, genomes acquire new genetic material that facilitates phenotypic innovation and diversification. Developmental processes associated with reproduction are particularly likely to involve novel genes. Abundant gene creation impacts the evolution of chromosomal gene content and general regulatory mechanisms such as dosage compensation. Numerous studies in model organisms have found complex and, at times contradictory, relationships among these genomic attributes highlighting the need to examine these patterns in other systems characterized by abundant sexual selection. Therefore, we examined the association among novel gene creation, tissue-specific gene expression, and chromosomal gene content within stalk-eyed flies. Flies in this family are characterized by strong sexual selection and the presence of a newly evolved X chromosome. We generated RNA-seq transcriptome data from the testes for three species within the family and from seven additional tissues in the highly dimorphic species, Teleopsis dalmanni. Analysis of dipteran gene orthology reveals dramatic testes-specific gene creation in stalk-eyed flies, involving numerous gene families that are highly conserved in other insect groups. Identification of X-linked genes for the three species indicates that the X chromosome arose prior to the diversification of the family. The most striking feature of this X chromosome is that it is highly masculinized, containing nearly twice as many testes-specific genes as expected based on its size. All the major processes that may drive differential sex chromosome gene content—creation of genes with male-specific expression, development of male-specific expression from pre-existing genes, and movement of genes with male-specific expression—are elevated on the X chromosome of T. dalmanni. This masculinization occurs despite evidence that testes expressed genes do not achieve the same levels of gene expression on the X chromosome as they do on the autosomes.

The Size and Content of the Sex-Determining Region of the Y Chromosome in Dioecious <em>Mercurialis annua</em>, a Plant with Homomorphic Sex Chromosomes

“…As an interesting contrast to our finding of Y-linked genes with male-limited expression, Baker et al [42] found genes only expressed in males to be enriched on the X chromosome of stalk-eyed flies. Their result seems more surprising than ours, and runs counter to the feminization (or demasculization) of expression patterns of X-linked genes reported in other studies [43][44][45].…”

“…Nevertheless, it is unclear how often we ought to expect genes with male-limited expression to be on the Y chromosome. Note that the patterns of gene expression used in our study here were observed for genes expressed in nonreproductive tissues [31], whereas many of those reported by Baker et al [42] were gonadal.…”

Impacts of sex ratio meiotic drive on genome structure and defense in a stalk-eyed fly

“…Maelstrom and aubergine have also duplicated within diopsids. We previously (Baker et al 2016) identified five duplicates of maelstrom, and here found an additional near-identical copy. Four of these six copies, including the adaptively evolving Xlinked copy appear to be novel within the genus Teleopsis (Figure S8).…”

The Z chromosome is enriched for sperm proteins in two divergent species of Lepidoptera

“…However, intersecting these sperm proteome results with a nuanced dissection of gene expression indicates a possible dearth of X-linked sperm genes with testis-specific expression, depending on the gene-set analyzed (Meisel et al 2012). More recently, another species of fly, the stalk-eyed fly, was observed to have a masculinized X chromosome (Baker et al 2016). Thus, the pattern of sex-biased gene distribution is still far from clear; these sperm proteomic results from monarch and Carolina sphinx represent an important complement to similar analyses in XX/XY species by testing the same hypotheses in a set of independent sex chromosomes.…”