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Evolution of Reproductive Proteins in Deer Mice

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Evolution of Reproductive Proteins in Deer Mice UNIVERSITY OF CALIFORNIA, SAN DIEGO EVOLUTION OF REPRODUCTIVE PROTEINS IN DEER MICE (PEROMYSCUS) A dissertation submitted in partial satisfaction of the requirements for the degree Doctor of Philosophy in Biology by Leslie McCue Turner Committee in charge: Professor Joshua R. Kohn, Chair Professor Hopi E. Hoekstra, Co-Chair Professor Peter Andolfatto Professor Ronald S. Burton Professor Victor D. Vacquier 2007 Copyright Leslie McCue Turner, 2007 All rights reserved. The dissertation of Leslie McCue Turner is approved, and it is acceptable in quality and form for publication on microfilm: Co-Chair Chair University of California, San Diego 2007 iii TABLE OF CONTENTS Signature Page ..............................................................................................................iii Table of contents....................................................................................................... iv List of figures.......................................................................................................... viii List of tables ............................................................................................................. ix Acknowledgements.................................................................................................... x Curriculum vita........................................................................................................ xii Abstract of the dissertation...................................................................................... xiv Chapter 1: Adaptive evolution of fertilization proteins within a genus: Variation in ZP2 and ZP3 in deer mice (Peromyscus) .................................................................... 1 Abstract.................................................................................................................. 1 Introduction............................................................................................................ 2 Materials and methods............................................................................................ 6 Extraction, amplification, and sequencing........................................................... 6 Phylogenetic reconstruction................................................................................ 8 Detection of positive selection............................................................................ 9 Mapping of amino acid substitutions ................................................................ 12 Results ................................................................................................................. 14 Structure and sequence variation of egg proteins .............................................. 14 Phylogenetic reconstruction.............................................................................. 15 Intraspecific variation....................................................................................... 16 Amino acid sites under selection....................................................................... 16 iv Mapping of amino acid substitutions ................................................................ 18 Discussion............................................................................................................ 22 Conclusions.......................................................................................................... 27 Acknowledgements .............................................................................................. 29 Literature Cited .................................................................................................... 41 Chapter 2: Reproductive protein evolution within and between species: ZP3 sequence variation in Peromyscus truei and P. gratus ............................................................. 48 Abstract................................................................................................................ 48 Introduction.......................................................................................................... 49 Materials and methods.......................................................................................... 52 Extraction, amplification and sequencing.......................................................... 52 Sequence analysis............................................................................................. 54 Results ................................................................................................................. 56 Population structure.......................................................................................... 56 Tests of neutrality............................................................................................. 57 Polymorphism in Zp3 ....................................................................................... 58 Geographic distribution of allelic diversity in Zp3 ............................................ 60 Discussion............................................................................................................ 60 Zp3 shows no evidence of selective sweeps ...................................................... 61 ZP3 shows high levels of amino acid polymorphism......................................... 62 Levels of allelic diversity in ZP3 are similar between populations of P. truei.... 63 Conclusions.......................................................................................................... 64 v Acknowledgements .............................................................................................. 66 Literature cited..................................................................................................... 76 Chapter 3: Comparative analysis of testis protein evolution in rodents...................... 82 Abstract................................................................................................................ 82 Introduction.......................................................................................................... 83 Materials and methods.......................................................................................... 85 Peromyscus maniculatus testis cDNA library construction and EST sequencing85 Evolutionary EST analysis................................................................................ 85 Identification of protein domains in Peromyscus EST sequences ...................... 88 Additional sequencing in Peromyscus species .................................................. 89 Analysis of Peromyscus testis-expressed gene sequences.................................. 90 Results ................................................................................................................. 93 EST sequencing................................................................................................ 93 Evolutionary EST analysis................................................................................ 93 Evolutionary rates of testis-specific genes ........................................................ 96 Functions of rapidly evolving genes ................................................................. 98 Evolution of rapidly evolving genes in Peromyscus.........................................100 Positive selection within Peromyscus ..............................................................101 Length variation in testis genes within Peromyscus .........................................104 Evolution of testis genes in divergent mammals...............................................106 Discussion...........................................................................................................107 Functional roles of rapidly evolving genes.......................................................108 vi Targets of selection at various levels of divergence .........................................111 Success of EST screen.....................................................................................112 Length variation ..............................................................................................114 Implications for fertilization and reproductive isolation ...................................115 Conclusions.........................................................................................................116 Acknowledgements .............................................................................................117 Literature cited....................................................................................................127 vii LIST OF FIGURES Figure 1.1 Gene and protein structure....................................................................... 34 Figure 1.2 Maximum likelihood gene trees.............................................................. 35 Figure 1.3 Amino acid sequence alignments............................................................ 37 Figure 1.5 Patterns of nucleotide substitution ........................................................... 40 Figure 2.1 Geographic distribution of sequence variation ......................................... 71 Figure 2.2 Tables of polymorphism......................................................................... 73 Figure 3.1 Evolutionary rates of testis-expressed ESTs............................................124 Figure 3.2 Rapidly evolving testis genes in three rodent lineages............................125 Figure 3.3 Positively selected testis genes in Peromyscus........................................126 viii
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