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X Chromosome Drive in Drosophila Testacea

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X Chromosome Drive in Drosophila Testacea X Chromosome Drive in Drosophila testacea by Graeme Keais B.Sc., University of Victoria, 2015 A Thesis Submitted in Partial Fulfillment of the Requirements for the Degree of MASTER OF SCIENCE in the Department of Biology ã Graeme Keais, 2018 University of Victoria All rights reserved. This thesis may not be reproduced in whole or in part, by photocopy or other means, without the permission of the author. ii Supervisory Committee X Chromosome Drive in Drosophila testacea by Graeme Keais B.Sc., University of Victoria, 2015 Supervisory Committee Dr. Steve J. Perlman, Department of Biology Supervisor Dr. Ben F. Koop, Department of Biology Departmental Member Dr. John S. Taylor, Department of Biology Departmental Member iii Abstract Supervisory Committee Dr. Steve J. Perlman, Department of Biology Supervisor Dr. Ben F. Koop, Department of Biology Departmental Member Dr. John S. Taylor, Department of Biology Departmental Member Selfish genes that bias their own transmission during gametogenesis can spread rapidly in populations, even if they contribute negatively to the fitness of their host. Driving X chromosomes provide a clear example of this type of selfish propagation. These chromosomes, which are found in a broad range of taxa including plants, mammals, and insects, can have important evolutionary and ecological consequences. In this thesis, I report a new case of X chromosome drive (X drive) in a widespread woodland fly, Drosophila testacea. I show that males carrying the driving X (SR males) sire 80-100% female offspring, and that the majority of sons produced by SR males are sterile and appear to lack a Y chromosome. This suggests that meiotic defects involving the Y chromosome may underlie X drive in this species. Abnormalities in sperm cysts of SR males reflect that some spermatids are failing to develop properly, confirming that drive is acting during gametogenesis. Further, I show that SR males possess a diagnostic X chromosome haplotype that is perfectly associated with the sex ratio distortion phenotype. Phylogenetic analysis of X-linked sequences from D. testacea and related species strongly suggests that the driving X arose prior to the split of D. testacea and its sister species, D. neotestacea and D. orientacea. Suppressed recombination between the XST and XSR due to inversions on the XSR likely explains their disparate evolutionary histories. By screening wild-caught flies using progeny sex ratios and a diagnostic X- linked marker, I demonstrate that the driving X is present in wild populations at a frequency of ~10% and that autosomal suppressors of drive are segregating in the same population. Both SR males and homozygous females for the driving X have reduced fertility, which helps to explain the persistence of the driving X over evolutionary timescales. The testacea species group appears to be a hotspot for X drive, and D. testacea is a promising model to compare driving X chromosomes in closely related species, some of which may even be younger than the chromosomes themselves. iv Table of Contents Supervisory Committee ...................................................................................................ii Abstract ......................................................................................................................... iii Table of Contents ........................................................................................................... iv List of Tables .................................................................................................................. v List of Figures ................................................................................................................ vi Acknowledgments ........................................................................................................viii Chapter 1 – X Chromosome Drive ................................................................................... 1 Meiotic Drive .............................................................................................................. 1 Sex Chromosome Drive ............................................................................................... 1 X Drive Mechanism .................................................................................................... 2 The Evolutionary Dynamics of X Drive ....................................................................... 4 Chapter 2 – X Chromosome Drive in a Widespread Palearctic Woodland Fly, Drosophila testacea ......................................................................................................................... 10 Introduction ............................................................................................................... 10 Materials and Methods .............................................................................................. 13 Results....................................................................................................................... 16 Discussion ................................................................................................................. 21 Chapter 2 Supplemental Information ......................................................................... 25 Chapter 3 – Maintenance of an ancient X drive polymorphism in Drosophila testacea .. 30 Introduction ............................................................................................................... 30 Materials and Methods .............................................................................................. 33 Results....................................................................................................................... 37 Discussion ................................................................................................................. 41 Chapter 3 Supplemental Information ......................................................................... 45 Chapter 4 – References .................................................................................................. 52 v List of Tables Table 1-1. Known cases of X drive in flies. ..................................................................... 3 Table 2-1. Fertility of 38 sons sired by seven different SR males. Sons were mated to four virgin laboratory females each to assess their fertility. DNA extractions were subsequently performed on these sons in order to screen for the Y-linked gene kl-2 using qPCR............................................................................................................................. 19 Table 3-1. Fecundity of XSRXST and XSRXSR females. ................................................... 41 Supplemental Table 2-1. Offspring sex ratio and skpA haplotype data from 23 Drosophila testacea males (mated to two laboratory females each). .............................. 25 Supplemental Table 2-2. Primers used in chapter 2. ..................................................... 25 Supplemental Table 2-3. Fertility data for 38 sons sired by seven different SR fathers, and 24 sons sired by an ST father. ................................................................................. 26 Supplemental Table 2-4. Offspring sex ratio and skpA haplotype data from wild caught male Drosophila testacea from St. Sulpice, Switzerland (mated to four laboratory females each). ............................................................................................................... 28 Supplemental Table 2-5. Offspring sex ratio and skpA haplotype data from F2 sons of wild-caught males carrying a suppressing element. F2 males are siblings produced by SR ST crossing X X females (F1 daughters of the wild-caught males S2 and S63) to laboratory XSTY males. ................................................................................................. 29 Supplemental Table 3-1. Offspring sex ratios (proportion female) of two representative males from the two Y replacement lines, Y2 and Y63. .................................................... 46 Supplemental Table 3-2. Primers used in chapter 3. ..................................................... 47 Supplemental Table 3-3. Individuals from the Drosophila testacea species group used for phylogenetic analysis of the autosomal gene gl. ....................................................... 48 Supplemental Table 3-4. Individuals from the Drosophila testacea species group used for phylogenetic analysis of the X-linked genes skpA and pgd. ...................................... 49 vi List of Figures Figure 2-1. Progeny sex ratios of male Drosophila testacea (SR or ST). Each male was mated to two virgin females. The number of offspring sired by each male is shown in brackets. Only males that produced >15 offspring are included. Progeny sex ratios that 2 significantly deviate from the expected 1:1 are shown as light bars (χ 1: P < 0.05). The dashed horizontal line denotes the expected proportion of female offspring (0.5). .......... 17 Figure 2-2. Crossing scheme used to determine the inheritance pattern of the SR trait in Drosophila testacea. Squares and circles denote males and females, respectively. Modified from James and Jaenike (1990). ..................................................................... 18 Figure 2-3. Electron micrographs of sperm cysts from 7-day old ST and SR males in cross section. (A) Cysts from ST males that have undergone individualization. Spermatids are tightly arranged, each with an orderly axoneme-Nebenkern pair. (B) Cysts from SR males are disorganized
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