Gene expression and sexual selection in sex role reversed flies

Overview

Empid flies (commonly known as dance flies) are exceptional in displaying elaborate sexually selected morphologies and behaviours in females. The normal Darwinian pattern in which males have elaborate ornaments and females tend to be choosier than males is reversed in many species of this group, probably because of male investment in nuptial gifts donated during copulation [1]. Both males and females exhibit a remarkable range of sexual signals to attract mating partners and sexual dimorphism shows extraordinary variation in the group. There have been numerous studies of the action of sexual and natural selection on these traits which have demonstrated the nature and extent of both honest and dishonest signalling [2,3,4]. These studies suggest complex and fluctuating selection across taxa that has contributed to the group’s unusual diversity, but the molecular genetic consequences of this rapid evolution of sexual characters remain unexplored.

This studentship will introduce a molecular, gene expression component to the study of trait variation in empids. We will collect adults, sequence genes and start new studies of gene expression in adult heads. We will take advantage of developing evo-devo work in Drosophila [e.g. 5] to examine the expression of candidate genes for eye and head shape variation. We will then relate sexually dimorphic gene expression to trait elaboration [6] to begin a novel contribution to the study of sexual selection on gene expression.

The elaborate traits of female empids are assessed visually by males, and recent unpublished work suggests correlated evolution between female ornament expression and dimorphism in eye shape and eye facet size. New work in Drosophila has identified genes that contribute to both eye shape divergence between sexes and species of Drosophila, and also developed methods to score the expression of rhodopsin and other visual pigments in adult fly heads and relate this to natural variation in eye shape [6]. To date, there have been no genetic studies of such genes in empids despite the obvious and dramatic elaborate selection on visual acuity and eye shape.

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Image Captions

Fig. 1 Scanning Electron Micrograph (SEM) of female Rhamphomyia longipes, illustrating ornamental pennate scales on the hind tibiae, which males lack (photo credit Axel Wiberg).
Fig. 2 SEM of the head of male Empis aestiva, illustrating dorsally enlarged eye facets (photo credit Claire Murray).

Methodology

We will exploit recent advances in the study of dance fly sexual selection and fly eye evolutionary genetics to
1. Develop methods to score rhodopsin variation in wild caught (newly eclosed) male and female heads of empid species which vary in the extent and direction of sexual dimorphism in eye shape. We predict that the extent of sexual dimorphism in Rh expression will depend on sex roles, and possibly reverse in species with sex role reversal.
2. Prepare transcriptomes from heads and quantify the overall levels of sexual dimorphism in gene expression. We predict sexual dimorphism in gene expression will scale with the intensity of sexual selection on female ornamentation.
3. We will examine gene sequence variation for genes being found to influence eye shape and size development in studies of Drosophila. Currently nothing is known of the evolution of such candidate genes in empids.
4. We will complement these genetic studies with field based behavioural experiments that formally quantify selection on male visual performance. We will use manipulations of artificial females in swarms [4] to examine if variation in expression related to visual performance is associated with specific forms of ornamentation and deception. If sexual conflict is responsible for antagonistic coevolution between males eyes and female ornaments, we expect to find that males with particularly exaggerated visual abilities are best able to discriminate between females with genuinely high reproductive value and their deceptive rivals.

The main methodologies utilised will be standard molecular genetic analyses, but applied to a novel system. Prof Alistair McGregor at Oxford Brookes will help advise based on his knowledge of eye shape genes in Drosophila. The student will complement this work with behavioural ecology experiments quantifying sexual selection on natural variation in morphology and gene expression. This work will involve a long-term collaborator, Prof. Darryl Gwynne from the University of Toronto.

The student will have two placements with our collaborators, one (OB) to receive training in the sequencing and analysis of candidate genes from Drosophila, and the other (UT) to receive training on selection analysis from field data. Field work will involve both Scottish and Canadian sites to include a wide range of species

Project Timeline

Year 1

Oct-Dec St. Andrews Candidate gene sequencing from existing samples
Jan-Mar Oxford Brookes Placement & sequence analysis
Apr-Jul Scotland First field season
Aug-Dec St. Andrews Transcriptome prep & sequencing

Year 2

Jan-Apr TBC Industrial placement
May-Jul Canada Second field season
Aug-Dec St. Andrews Selection analysis; transcriptome analysis

Year 3

Jan-May Scotland Genetic laboratory work
Apr-Jun Scotland Final field season
Jul-Aug St. Andrews Genetic processing of wild samples
Sep-Dec St. Andrews Comparative genomic analyses

Year 3.5

Dec-Mar St. Andrews Thesis and MS prep

Training
& Skills

Key skills learned will involve gene and transcriptome sequencing, bioinformatics, comparative genomics, behavioural ecology, selection analysis, morphological analysis and entomology. The student will eventually have a rare combination of skill sets including both modern molecular genetic and bioinformatic skills alongside behavioural ecology field expertise. The candidate will also receive advanced training in modern quantitative analyses of genomic and ecological data.

References & further reading

1. Herridge, E. J., Murray, R. L., Gwynne, D. T. & Bussière, L. F. Mating and Parental Sex Roles, Diversity in. Encyclopedia of Evolutionary Biology 453-458 (2016).
2. LeBas, N. R., Hockham, L. R. & Ritchie, M. G. Nonlinear and correlational sexual selection on ‘honest’ female ornamentation. Proc R Soc London B Biol Sci 270, 2159-2165 (2003).
3. LeBas, N. R., Hockham, L. R. & Ritchie, M. G. Sexual selection in the gift-giving dance fly, Rhamphomyia sulcata, favors small males carrying small gifts. Evolution (N Y) 58, 1763-1772 (2004).
4. Murray, R. L., Wheeler, J., Gwynne, D. T. & Bussière, L. F. Sexual selection on multiple female ornaments in dance flies. Proc R Soc B Biol Sci 285, 20181525 (2018).
5. lbrant, M., I. Almudi, D. J. Leite, L. Kuncheria, N. Posnien, M. D. S. Nunes and A. P. McGregor (2014). Sexual dimorphism and natural variation within and among species in the Drosophila retinal mosaic. Bmc Evolutionary Biology 14.
6. Veltsos, P., Y. Fang, A. R. Cossins, R. R. Snook and M. G. Ritchie (2017). Mating system manipulation and the evolution of sex-biased gene expression in Drosophila. Nature Communications 8: 2072.

Further Information

Prof. Michael Ritchie, mgr@st-andrews.ac.uk. 01334 463495

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