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

Leanna M Birge,Marie L Pitts,Richard H Baker,Gerald S Wilkinson

doi:10.1186/1471-2148-10-227

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.

Highlights

Polymorphisms of single amino acid repeats (SARPs) are a potential source of genetic variation for rapidly evolving morphological traits
We designed the study to address four questions: 1) Are any single amino acid repeat polymorphisms (SARPs) unequally represented among amino acids in genes expressed during eyestalk development? 2) Are any SARPs preferentially located in transcription factors? 3) Are SARPs gained or lost frequently across species? 4) Do SARPs occur in genes that influence eyestalk length? To increase the likelihood of finding genes with adaptive phenotypic effects, we focus the study on repeats with nine or more consecutive codons because long repeats typically disrupt function and should, only persist if they provide some selective advantage [17,18,19,24,25,26,27]
Distribution of codon repeat loci To determine if any repeats containing nine or more codons occur out of proportion to codon abundance, we compared repeat frequencies to corresponding amino acid frequencies for genes in the T. dalmanni expressed sequence tag (EST) library and their homologs in D. melanogaster (Fig. 1)

Summary

Introduction

Polymorphisms of single amino acid repeats (SARPs) are a potential source of genetic variation for rapidly evolving morphological traits. 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. One class of repetitive sequences, known as single amino acid or codon repeats, is an exception to this pattern and has long been known to be associated with diseases of the nervous system [2,3]. Variation in the length of single amino acid tracts, often referred to as single amino acid repeat polymorphisms (SARPs), have been implicated in a variety of neuropathologies [2,3,4,5], such as Fragile-X [6], Kennedy’s disease [7]. Larger glutamine repeat tracts are associated with earlier onset and accelerated progression of the disease [16]

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Discussion

Conclusion