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«ABSTRACT Title of Document: UNDERSTANDING THE REPRODUCTIVE BIOLOGY OF THE PRZEWALSKI’S HORSE (EQUUS FERUS PRZEWALSKII) Christina Wynne Collins, ...»

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ABSTRACT

Title of Document: UNDERSTANDING THE REPRODUCTIVE

BIOLOGY OF THE PRZEWALSKI’S HORSE

(EQUUS FERUS PRZEWALSKII)

Christina Wynne Collins, M.V.B., Ph.D., 2010

Directed By: Associate Professor, Carol L. Keefer, Department of

Animal and Avian Sciences

The Przewalski’s horse (Equus ferus przewalskii) once roamed the Eurasian Steppe but is now considered Critically Endangered with only 1872 individuals remaining in the world, representing progeny from only 14 founder animals (Lee and Boyd, 2008). Genetic diversity needs to be optimal for long term survival of this species. Unfortunately, increasing genetic diversity of the captive population in North America has been hindered by a decrease in fertility. Therefore, the main focus of this research was to characterize reproductive parameters in Przewalski’s horse, including estrus cycle in mares and seminal traits in stallions, and determining whether age or inbreeding had an impact on these traits. A secondary focus was to determine whether hormone manipulation of the estrous cycle in mares could be utilized for the long-term goal of using artificial insemination as a breeding management tool for this species. To facilitate these studies, a technique for palpation of Przewalski’s mares was developed; the first application of such a procedure in a wild equid.

Subsequently, we were able to describe follicular changes in relation to urinary hormone patterns. Fifty percent of the mares had either irregular or acyclic hormonal and follicular patterns. These patterns were directly correlated with inbreeding which is the first time such a correlation has been described in this species. Estrous manipulation was possible using an injectable biorelease form of the progestagen, altrenogest. In stallions, we developed a reliable method of semen collection for Przewalski’s stallions and, as a result, describe seminal traits from 98 semen collections from 14 stallions. Based on these collections, we were able to show that sub-fertility in this population could be due to the low percentage of normal spermatozoa. Based on variable analysis, seminal traits total concentration, volume and morphology showed variable changes through the year. Traits also varied on an individual stallion basis. Together, these studies demonstrated that inbreeding is detrimentally affecting the reproductive fitness of this species and that aggressive management is needed for long term sustainability of the captive population.

UNDERSTANDING THE REPRODUCTIVE BIOLOGY OF THE

PRZEWALSKI’S HORSE

(EQUUS FERUS PRZEWALSKII)

–  –  –

Advisory Committee:

Associate Professor Carol Keefer, Chair Associate Professor Amy Burk Professor Jim Dietz Dr. Steven Monfort Professor Tom Porter Dr. Nucharin Songsasen ” Copyright by Christina Wynne Collins DEDICATION This thesis is dedicated to my father, Del, who was my main support and source of inspiration throughout this long endeavor.

Also, to my husband, Jeff, who has been my best friend.

–  –  –

This research would not have been possible without the support, friendship and guidance of Dr. Nucharin Songsasen, who served as my main advisor at the National Zoological Park. I was also fortunate to work with Dr. Carol Keefer, my main advisor at University of Maryland, who was a great guide especially through the final stages of my dissertation.

Of course, I would not have had the opportunity to work on this project without the ideas and support that I received from Dr. Steven Monfort and Dr. David Wildt. I would

also like to thank the rest of my dissertation committee for their guidance and support:

Dr. Tom Porter, Dr. Amy Burk, and Dr. Jim Dietz.

I am also extremely grateful to the individuals and organizations which provided funding for the project including: Morris Animal Foundation, Undersecretary for Science, Smithsonian Institution, and Shirley Sichel. I would especially like to thank Christine and Austin Bach for not only providing funding for the project but also for being such great friends and support when times were tough.

There were many people that assisted with this project, without which, I would have been unable to complete it. Many people at SCBI including Nicole Presley, Dr. Mandi Vick, Dr. Janine Brown, Dr. Mitch Bush, Dr. Luis Padilla, Lisa Ware, Dr. Budhan Pukazhenthi, and Linwood Williamson, assisted me with data collection and lab work.

A special thanks to the hoofstock team for all the extra work that they conducted:

Ken Lang, Greg Peterson, Dolores Reed, Dave Shiflett, Shannon Hunter and Allyson O’Neill At the Wilds, I had unwavering support from Dr. Evan Blumer, Dr. Barb Wolfe, Dan Beetem, Dr. Rachael Weiss and the hoofstock staff. I was also fortunate to work with many great interns who helped me complete and interpret data, many of whom also provided me with great friendship and support.

I would like to thank my father for being an honorary committee member and keeping me focused on completion. Thanks to my stepmother, Patty, who had to suffer through discussions about science on the phone. Sincere thanks to my brother, Rob, and my sister, Lainey, for being able to commiserate with me as they complete their graduate degrees; my sister-in-laws: Laura, Jane and Sandy; and my nieces and nephews. Thanks to my mother for checking up on me and my in-laws for understanding when I could not visit.





Most of all, I would to thank my husband, Jeff, for sticking by me through the last few years and for helping me see the funny side of things. You complete me.

–  –  –

Dedication………………………………………………………………....... ii Acknowledgements…………………………………………………………. iii Table of Contents…………………………………………………………… iv List of Tables………………………………………………………………… vi List of Figures……………………………………………………………….. vii Abbreviations…………………………………………………………………ix Chapter1: Literature Review….................…………………………………... 1 The Asian Wild Horse…………………………………………………. 1 Artificial Insemination in the Domestic Horse………………………… 4 The Application of Artificial Insemination in Wildlife……………….. 6 Reproduction in Przewalski’s Mares…………………………………... 7 Reproduction in the Domestic Mare…………………………………… 9 Steroidogenic Pathway………………………………………………… 17 Reproduction in the Domestic Stallion………………………………… 23 Assisted Reproduction in the Domestic Horse………………………… 27 Chapter 2: Abnormal Reproductive Cycles are Prevalent in Przewalski’s Mares…

Introduction……………………………………………………………. 38 Materials and Methods………………………………………………….45 Animals…………………………………………………………….. 45 Urine Collection………………………………………………….....45 Enzyme Immunoassay……………………………………………... 45 Training for Ultrasound Examination………………………………48 Ultrasound Examination…………………………………………… 49 Statistical Analysis………………………………………………….50 Results…………………………………………………

Discussion ……………………………………………………………... 61 Chapter 3: Manipulation of the Estrous Cycle in Przewalski’s Mares………. 68 Introduction……………………………………………………………. 68 Materials and Methods………………………………………………… 72 Animals…………………………………………………………….. 72 Urine Collection…………………………………………………….73 Enzyme Immunoassay……………………………………………... 73 Ultrasound Examination………………………………………….... 75 Study 1……………………………………………………………... 76 iv Study 2……………………………………………………………... 77 Statistical Analysis………………………………………………….78 Results…………………………………………………………………. 80 Discussion…………………………………………………………….... 91 Chapter 4: Characterization of Seminal Traits in the Przewalski’s Stallion….97 Introduction……………………………………………………………. 97 Materials and Methods………………………………………………….101 Animals…………………………………………………………….. 101 Semen Collection……………………………………………………101 Semen Evaluation………………………………………………….. 102 Morphological Assessment…………………………………………102 Testicular Examination…………………………………………….. 103 Statistical Analysis………………………………………………….103 Results…………………………………………………………………..105 Discussion……………………………………………………………… 119 Chapter 5: Overall Significance and Future Directions……………………... 131 Appendix…………………………………………………………………….. 135 Bibliography…………………………………………………………………. 143

–  –  –

2.1 Mares included in study 1: classified as normal, abnormal or acyclic………. 46

2.2 Normal reproductive cycle parameters for Przewalski’s mares (n = 7) based on urinary hormone metabolites………………………………………. 51

3.1 Mean urinary hormone concentrations during pre-, peri-, and posttreatment periods (Oral 14 day altrenogest therapy)……………………….... 87

3.2 Mean urinary hormone concentrations during pre-, peri-, and posttreatment periods (Oral 12 day and Injectable 12 day altrenogest therapy)………………………………………………………………………. 91

4.1 Seminal parameters for 14 Przewalski’s stallions collected over a 45-month period………………………………………………………………………… 114

4.2 Sperm morphology for Przewalski’s stallions (n = 56 samples)…………….. 115

4.3 Seminal traits in stallions in relation to statistical variables stallion and season…………………………………………………………………………111

4.4 Seminal traits of Przewalski’s stallions (n = 14) in relation to season and sin/ cosin analysis……………………………………………………….. 115

–  –  –

1.1 Demographics of Current SSP Population……………………………3

1.2 The Estrous Cycle of the Domestic Mare……………………………. 12

1.3 Follicular Wave Patterns of the Domestic Mare……………………...13

1.4 Hypothalamo-Pituitary Gonadal Axis in the Domestic Mare………...14

1.5 Cholesterol…………………………………………………………… 18

1.6 Steroidogenic Pathway………………………………………………. 20

1.7 Two-cell Two-gonadotrophin theory…………………………………21

1.8 Endocrine Control of Spermatogenesis……………………………… 25

2.1 Founder representation in the North American SSP population for the Przewalski’s horse…………………………………………….40

2.2 Reproductive fecundity based on age of Przewalski’s mares………... 42

2.3 Mean urinary hormone metabolites (estrogen and progestagen) of Przewalski’s mares (n = 7)……………………………………....... 54

2.4 Longitudinal urinary hormone profiles of Przewalski’s mares (n = 3) with abnormal cycles………………………………………………… 55

2.5 Representative longitudinal urinary hormone data for acyclic mare… 56

2.6 Bar chart showing mean ± SEM urinary hormones of mares with normal, abnormal, or acyclic endocrine profiles…………………….. 58

2.7 Changes in urinary estrogen and progestagen metabolites in relation to follicular size……………………………………………... 60

3.1 Schematic of hormone therapy for Study 1………………………….. 77

–  –  –

3.3 Days from treatment to ovulation in Przewalski’s mares (n = 5) treated with saline (n = 2); GnRH (n = 5) and reLH (n = 2)………….81

3.4 Mean urinary hormone levels during treated cycles (n = 9) of Przewalski’s mares with 14 days oral altrenogest…………………… 82

3.5 Longitudinal urinary hormone data for Przewalski’s mares (n = 7) treated with oral altrenogest for 14 days…………………….. 84

3.6 Comparison of longitudinal urinary hormone profiles for Przewalski’s mares treated with:1) Oral 14 day; 2) Oral 12 day;

and 3) Injectable 12 day……………………………………………....85

3.7 Days from detection of estrous follicle to ovulation in Przewalski’s mares (n = 10) between natural cycles and those that were treated with an ovulatory agent (GnRH)………………………..89

3.8 Comparison of Oral 12 day and Injectable 12 day therapy.

Data are depicted as Mean ± SEM and graphed as longitudinal urinary hormone profiles…………………………………………….. 91

4.1 Micrograph of two spermatozoa with folded acrosome...…………… 108

4.2 Ultrasound image of testicle during examination of a Przewalski’s stallion………………………………………………………………...109



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