Evidence of Adaptive Evolution and Relaxed Constraints in Sex-Biased Genes of South American and West Indies Fruit Flies (Diptera: Tephritidae)

Abstract

Several studies have demonstrated that genes differentially expressed between sexes (sex-biased genes) tend to evolve faster than unbiased genes, particularly in males. The reason for this accelerated evolution is not clear, but several explanations have involved adaptive and nonadaptive mechanisms. Furthermore, the differences of sex-biased expression patterns of closely related species are also little explored out of Drosophila. To address the evolutionary processes involved with sex-biased expression in species with incipient differentiation, we analyzed male and female transcriptomes of Anastrepha fraterculus and Anastrepha obliqua, a pair of species that have diverged recently, likely in the presence of gene flow. Using these data, we inferred differentiation indexes and evolutionary rates and tested for signals of selection in thousands of genes expressed in head and reproductive transcriptomes from both species. Our results indicate that sex-biased and reproductive-biased genes evolve faster than unbiased genes in both species, which is due to both adaptive pressure and relaxed constraints. Furthermore, among male-biased genes evolving under positive selection, we identified some related to sexual functions such as courtship behavior and fertility. These findings suggest that sex-biased genes may have played important roles in the establishment of reproductive isolation between these species, due to a combination of selection and drift, and unveil a plethora of genetic markers useful for more studies in these species and their differentiation.

Evolutionary dynamics of sex-biased genes expressed in cricket brains and gonads

“…For example, the pattern in Gryllus (Fig. 3) is consistent with observations of rapid evolution of testis-biased and slow evolution of ovary-biased genes in Drosophila [7,11,14,61] (see also results in a related fly, [37] ). In addition, this pattern also matches our recent results from beetles (Tribolium castaneum) that showed rapid evolution of testis-biased genes [13], a taxon which like Drosophila species' is polyandrous, and has evidence of pre-and post-mating female choice mechanisms [84].…”

“…However, there is a striking paucity of data on the relationship between sex-biased expression in the brain and protein sequence evolution [22]. Moreover, the minimal research available from birds, humans and flies have suggested different types of male and female effects on rates of protein evolution, depending on the system [23,29,32] (see also some brain-related and composite-tissue analyses [36,37]), and the causes of those patterns remain poorly understood. It is therefore evident that additional study is needed of sex-biased brain expression and its relationship to molecular…”

Peer Review #1 of "Genomic signatures of globally enhanced gene duplicate accumulation in the megadiverse higher Diptera fueling intralocus sexual conflict resolution (v0.1)"

“…Consistent with our results for the higher Diptera, for instance, Katzourakis et al ( 2001) found evidence for a correlation between sexual selection and species richness in hoverflies. Similar conclusions have been drawn in a study of tephritid species (Congrains et al, 2018), which aligns taxonomically more closely with our findings of parallel sex biased gene…”

Genomic signatures of globally enhanced gene duplicate accumulation in the megadiverse higher Diptera fueling intralocus sexual conflict resolution

“…Consistent with our results for the higher Diptera, Katzourakis et al (2001) found evidence for a correlation between sexual selection and species richness in hoverflies. Similar conclusions have been drawn in a study of tephritid species (Congrains et al, 2018), which aligns taxonomically more closely with our findings of parallel sex biased gene duplications in schizophoran lineages outside the Drosophilidae. Based on artificial breeding experiments, however, sexual conflict was concluded to play no role in reproductive isolation in D. pseudoobscura (Bacigalupe et al, 2007).…”