Length polymorphism and head shape association among genes with polyglutamine repeats in the stalk-eyed fly, Teleopsis dalmanni

Abstract

BackgroundPolymorphisms of single amino acid repeats (SARPs) are a potential source of genetic variation for rapidly evolving morphological traits. Here, we characterize variation in and test for an association between SARPs and head shape, a trait under strong sexual selection, in the stalk-eyed fly, Teleopsis dalmanni. Using an annotated expressed sequence tag database developed from eye-antennal imaginal disc tissues in T. dalmanni we identified 98 genes containing nine or more consecutive copies of a single amino acid. We then quantify variation in length and allelic diversity for 32 codon and 15 noncodon repeat regions in a large outbred population. We also assessed the frequency with which amino acid repeats are either gained or lost by identifying sequence similarities between T. dalmanni SARP loci and their orthologs in Drosophila melanogaster. Finally, to identify SARP containing genes that may influence head development we conducted a two-generation association study after assortatively mating for extreme relative eyespan.ResultsWe found that glutamine repeats occur more often than expected by amino acid abundance among 3,400 head development genes in T. dalmanni and D. melanogaster. Furthermore, glutamine repeats occur disproportionately in transcription factors. Loci with glutamine repeats exhibit heterozygosities and allelic diversities that do not differ from noncoding dinucleotide microsatellites, including greater variation among X-linked than autosomal regions. In the majority of cases, repeat tracts did not overlap between T. dalmanni and D. melanogaster indicating that large glutamine repeats are gained or lost frequently during Dipteran evolution. Analysis of covariance reveals a significant effect of parental genotype on mean progeny eyespan, with body length as a covariate, at six SARP loci [CG33692, ptip, band4.1 inhibitor LRP interactor, corto, 3531953:1, and ecdysone-induced protein 75B (Eip75B)]. Mixed model analysis of covariance using the eyespan of siblings segregating for repeat length variation confirms that significant genotype-phenotype associations exist for at least one sex at five of these loci and for one gene, CG33692, longer repeats were associated with longer relative eyespan in both sexes.ConclusionAmong genes expressed during head development in stalk-eyed flies, long codon repeats typically contain glutamine, occur in transcription factors and exhibit high levels of heterozygosity. Furthermore, the presence of significant associations within families between repeat length and head shape indicates that six genes, or genes linked to them, contribute genetic variation to the development of this extremely sexually dimorphic trait.

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

“…Whether some X-linked genes also are responsible for increases in male eyespan is less clear, although this could occur if X-linked transcription factors influenced expression of autosomal genes. Considerable allelic variation in transcription factors that contain amino-acid repeats has been detected and at least one X-linked variant has been associated with eyestalk length in T. dalmanni [40]. Additional studies on how allelic variation at candidate genes influences sex-biased expression are likely to provide insight into the nature of genetic change required to produce the extraordinary morphology displayed by these flies.…”

“…Many species exhibit dramatic sexual dimorphism in head shape [37] with the outer-most distance between the eyes (eyespan) being two or more times the body length of males in some species. Sexual dimorphism in eyespan has evolved multiple times within the family [38] and is heritable [39], [40]. Sexual selection operates on male eyespan before mating in sexually dimorphic species by male-male competition [41] and female choice [42]–[44].…”

Selection pressure on human STR loci and its relevance in repeat expansion disease

“…Some of STRs located in regulatory regions have been known as "evolutionary tuning knobs" that quantitatively regulate gene expression depending on their number of repeats (Gebhardt et al 1999;King 2012;Trifonov 1989). Moreover, effects of STR variation on phenotypes are not restricted to quantitative fine tuning but also influence dynamic changes in development (Birge et al 2010;Fondon and Garner 2004;Galant and Carroll 2002) and behavior (Hammock and Young 2005) by alternation of mRNA splicing (Lorenz et al 2007) and amino acid translation (Chang et al 2001;Erwin et al 2006;Weiser et al 1989), which are called "evolutionary switches." These evolutionary switches bring about not only selection of individuals carrying advantageous alleles but also a shift to heterogeneous populations with various alleles that is advantageous for organisms in rapid adaptation to variable environments [e.g., counter strategy to host immune system in Haemophilus influenza, (Erwin et al 2006) and diversifying sexual selection in the stalk-eyed fly, Teleopsis dalmanni (Birge et al 2010;Cotton et al 2014)].…”

“…Moreover, effects of STR variation on phenotypes are not restricted to quantitative fine tuning but also influence dynamic changes in development (Birge et al 2010;Fondon and Garner 2004;Galant and Carroll 2002) and behavior (Hammock and Young 2005) by alternation of mRNA splicing (Lorenz et al 2007) and amino acid translation (Chang et al 2001;Erwin et al 2006;Weiser et al 1989), which are called "evolutionary switches." These evolutionary switches bring about not only selection of individuals carrying advantageous alleles but also a shift to heterogeneous populations with various alleles that is advantageous for organisms in rapid adaptation to variable environments [e.g., counter strategy to host immune system in Haemophilus influenza, (Erwin et al 2006) and diversifying sexual selection in the stalk-eyed fly, Teleopsis dalmanni (Birge et al 2010;Cotton et al 2014)]. Furthermore, according to the hypothesis focusing on rapid evolution of the human brain (social brain hypothesis) (Dunbar 1998), highly variable STRs leading to neurodegenerative disease may work as an evolutionary switch, by contributing to the increase of the diversities of populations in sensory, motor and cognitive abilities, which are a definitive feature of the human population with highly structured society (Fondon et al 2008;Nithianantharajah and Hannan 2007).…”

Haldane’s Rule Is Linked to Extraordinary Sex Ratios and Sperm Length in Stalk-Eyed Flies

“…Genotype data were generated using primers designed for T. dalmanni microsatellites (Wright et al 2004) or genes containing glutamine repeats (Birge et al 2010). Initially, parents were genotyped to identify loci that exhibited variation that could be associated with each parental population and spanned each chromosome.…”