Immunocontraception of mammalian wildlife: ecological and immunogenetic issues

in Reproduction

Immunocontraception involves stimulating immune responses against gametes or reproductive hormones thus preventing conception. The method is being developed for the humane control of pest and overabundant populations of mammalian wildlife. This paper examines three fundamental issues associated with its use: (1) the difficulties of obtaining responses to self-antigens, (2) the likely evolution of genetically based non-response to immunocontraceptive agents, and (3) the possible changes in the array of pathogens possessed by the target species after generations of immunocontraception. Our review of the literature demonstrates that the barriers to an effective immunocontraceptive are at present very basic. Should they be overcome, the effects of immunocontraception on the immunogenetic constitution of wildlife populations through the selection for non-responders must be examined. We suggest that the attempt to use the animal’s own immune system to modulate reproduction may be incompatible with the basic biological function of protection against infectious disease. Research programs on mammalian immunocontraception should involve measurement of the heritability of non-response and an assessment of the likely change in the response of the contracepted population to possible pathogens.

Abstract

Immunocontraception involves stimulating immune responses against gametes or reproductive hormones thus preventing conception. The method is being developed for the humane control of pest and overabundant populations of mammalian wildlife. This paper examines three fundamental issues associated with its use: (1) the difficulties of obtaining responses to self-antigens, (2) the likely evolution of genetically based non-response to immunocontraceptive agents, and (3) the possible changes in the array of pathogens possessed by the target species after generations of immunocontraception. Our review of the literature demonstrates that the barriers to an effective immunocontraceptive are at present very basic. Should they be overcome, the effects of immunocontraception on the immunogenetic constitution of wildlife populations through the selection for non-responders must be examined. We suggest that the attempt to use the animal’s own immune system to modulate reproduction may be incompatible with the basic biological function of protection against infectious disease. Research programs on mammalian immunocontraception should involve measurement of the heritability of non-response and an assessment of the likely change in the response of the contracepted population to possible pathogens.

Introduction

The regulation of human and animal population numbers constitutes a difficult and largely unsolved contemporary problem. In the developed world, steroid contraceptives for humans are both widely used and efficacious. Elsewhere they are too costly. The development of less expensive methods is considered necessary (Aitken et al. 1993). One such method is immunocontraception, i.e. the vaccination against sperm, eggs, or reproductive hormones to prevent either fertilization or the production of gametes. Attempts to design human immunocontraception have a long history (Joshi 1973, Stevens 1975, Basten 1988, Gupta & Talwar 1994). The targets include sperm antigens, oocyte antigens, especially zona pellucida proteins (PZP), gonadotropin riboflavin carrier protein, gonadotropins and gonadotropin releasing hormones (Delves et al. 2002). The most advanced method involves immunization against human chorionic gonadotropin, in reality a method of very early pregnancy termination (Baird 2000). It now seems likely that problems associated with autoimmune disease and variability of response will prevent any widespread use of immunocontraception in humans in the foreseeable future (Rao 2001, Aitken 2002). Women’s health advocates have objected to all forms of immunocontraception because of perceived health risks and the potential for political abuse of the vaccine (Richter 1994). Human male immunocontraceptives have received much less attention and do not appear to be feasible in the near future (Delves et al. 2002).

Immunocontraceptives for wild animals have a different objective than those for humans. Their main aim is to check population growth rather than to contracept particular individuals. If some animals are irreversibly sterilized so much the better whereas such an effect in human medicine would be ethically most undesirable. Immunocontraceptives for animals are ostensibly humane and could potentially be used on the large scale required for wildlife population regulation. Research progress to date has been reviewed in Tyndale-Biscoe (1991, 1994), Barber & Fayrer-Hosken (2000), Barlow (2000), and Cooper & Herbert (2001). Three fundamental questions remain to be addressed: (1) Can sufficiently strong immune responses be provoked against the antigens (immunogens) of gametes or reproductive hormones to cause contraception in a proportion of animals large enough for effective population management? (2) How rapidly will variation in these responses lead to the evolution of failure to respond to the immunocontraceptive agent? (3) What will be the ecological consequences of the likely changes to the immunogenetic constitution of the population as a result of selection for non-responders? In particular, will the endemic pathogens of the species change? There is considerable information which allows us to answer at least in part the first two questions. The third is of fundamental importance but even a preliminary answer is not possible at present.

Target species

Population control of native and exotic mammals is generally justified by environmental degradation, competition with and predation on native wildlife, conflicts with humans over food production, potential spread of pathogenic infectious diseases and the possibility of population crashes of over-abundant fauna or of wildlife populations near urban areas. Although still in its infancy, immunocontraception is regarded as being more humane than the traditional methods of wildlife population control, such as shooting, trapping, poisoning, or pathogenic agents and its use has strong support from influential animal welfare agencies worldwide (Oogjes 1997, Grandy & Rutberg 2002). Table 1 lists mammalian species for which immunocontraception is being investigated and for which the method could be applied. In all these species, there are at present no completely efficacious, cost-effective, or socially acceptable methods for population regulation available.

Immune responses to self-antigens

Responses to self-antigens are unusual and mainly weak. This constitutes a major barrier to the development of an immunocontraceptive. Table 2 summarizes data on attempts to induce immunocontraception using a variety of antigens in 14 mammalian species. The data in Table 2 show that in most cases a significant proportion of the population is not contracepted by administration of the immunocontraceptive antigen. The reason for this could be either genetic or environmental. In either case it indicates that a fraction of the population will continue to breed despite the administration of the contraceptive. In most cases, there is likely to be at least in part genetic causes underlying lack of response. If so, the genes for lack of response will be selected for and in a comparatively small number of generations most of the population will be non-responsive. This implies that the immunocontraceptive can be useful for only a short period of time.

All studies summarized in Table 2 involve the use of some kind of adjuvant, i.e. a substance or array of substances designed to enhance the immune response. There are no reports of successful immunocontraception without some form of adjuvant. Moreover, most immunizations were boosted at least once (see Table 2). The need for multiple injections and the dependence upon adjuvant to achieve the necessary level of response renders the whole approach impractical at present. The most commonly used adjuvant, Freund’s Adjuvant, also induces a range of undesirable side effects and its use is being challenged on animal welfare grounds (Leenaars et al. 1994, 1998). There is at present no feasible or acceptable method of promoting responses to self-antigens sufficient to cause immunocontraception.

Jackson et al.(2001) attempted to overcome the problem of lack of immune response to self-antigens in the absence of adjuvant by inserting the cytokine interleukin-4 into mousepox virus with the intention of increasing the humoral response. The virus was then inserted into the mice with the unwelcome outcome that the mice all died very quickly. This work caused alarm because of the possibility that this technology could lead to a method for simple conversion of relatively innocuous viruses into lethal ones, which could be used in biological warfare (Finkel 2001).

Another possible problem with virus-vectored immunocontraception is the potential for the horizontal transfer of the immunocontraceptive gene into viruses affecting other species (Becker 2000). While it may be possible to create genetically modified organisms without adverse effects on the target animals, the effects they might have on related species they come in contact with make any use of this approach questionable.

Variation in response and genetic change

Variation in response to biocontrol agents is a widespread phenomenon. This variation has frequently led to evolution of a degree of resistance so that the agent is no longer useful. The evolution of resistance to insecticides has been reviewed by McKenzie (1996). He draws a distinction between biocontrol agents with responses within the phenotypic range and those with responses outside the phenotypic range of the target species. An agent which initially kills all members of the target species is acting outside the normal phenotypical range, while one which kills onlya fraction of the population is acting within the normal phenotypical range. He points out that when resistance appears in the former case it is frequently monogenic, while in the latter case a number of different genetic regions are involved, i.e. it is probably multi-factorial. The basic genetic parameter to be estimated in either case is heritability, i.e. the extent to which genetic variation is controlled by genetic as opposed to environmental factors. The relative fertility of the immunocontracepted animals in Table 2 is >10% in 27 out of the 32 data sets. A proportion of non-responders is characteristic of most species. Only three species (Tammar wallaby, Fallow deer and Norway rat) out of 14 had no non-responders (Table 2). Following McKenzie’s (1996) argument, this implies that non-response is likely to be multi-factorial in genetic terms. There are no data which will allow estimates of the heritability of non-response to immunocontraception in any of the species in Table 2. We are unable to predict the rate at which this characteristic will increase in any one of these populations under the selective influence of immunocontraception. However, some idea of the likely change per generation given the initial frequency of non-responders can be found using Falconer’s (1965) model for threshold characters (Table 3). Reproduction is a good example of a threshold character; it is an all-or-none attribute which can be affected by a variety of underlying genetic and environmental factors. If heritabilities are high, rapid selection occurs. This is shown by the high percentage of non-responders that occur within one generation (Table 3).

A limited place for immunocontraception in wildlife management could be in species with long generation times. Genetic changes in them, if they occur, will take decades. Claims have been made for the potential efficacy of immunocontraception for African elephants (Fayrer-Hosken et al. 2000, Delsink et al. 2002), although this view has been challenged on demographic grounds (Pimm & van Aarde 2001). Long-term studies on immunocontraception in wild horses report 78–94.2% contraceptive efficacy (Kirkpatrick et al. 1995, Turner et al. 1997, 2002, Turner & Kirkpatrick 2002).

Zoo animals are convenient for immunocontraception studies of wild species, because of their long-term accessibility, although the small numbers usually available make controls hard to find. This is illustrated by an investigation involving 27 females from 10 felid species. Immunization with PZP and Freund’s Complete Adjuvant gave several kinds of adverse reaction but no convincing evidence of an effect upon fertility (Harrenstien et al. 2004).

Delves & Roitt (2005) review attempts to immunocontracept mammals and conclude that GnRH is the most promising target, because of its evolutionary conserved sequence.

Immunogenetic issues

Infectious diseases are assumed to be one of the main classes of selective forces which act upon genes controlling immune responses (Klein et al. 1993). Immunocontraceptive agents also have the potential to influence the genetic constitution of a population with respect to the ability to mount immune responses. The two are similar in that pathogens which cause plagues and immunocontraceptive agents are both capable of exerting very strong selective pressure with the potential for rapid genetic change. However, they differ in two important respects. First, most pathogens are cellular and antigenically more complex than most immunocontraceptive agents, which consist of one or a few proteins and in some cases associated carbohydrate. Second, they have opposite directions of selection; resistance to a pathogen involves a positive response, whereas resistance to an immunocontraceptive involves non-response. The consequences of this kind of selection imposed by an immunocontraceptive agent require study. It seems likely that it will alter the immunogenetic constitution of the target species. The existence of genes governing response to pathogens is well documented in humans for malaria (Hill 2001), tuberculosis (Blackwell 1998, Bellamy 2003), and HIV (McNicholl & Cuenco 1999, Carrington & O’Brien 2003). Relevant examples are found in New Zealand Red Deer in which susceptibility to tuberculosis has high heritability (Mackintosh et al. 2000) and in the NRAMP1 association with the human response to leishmaniasis (Bucheton et al. 2003). The complexities of the co-evolution of pathogens and hosts and its biomedical significance are beginning to be unraveled (Woolhouse et al. 2002). Both experimental (Lively & Dybdahl 2000) and theoretical analyses (e.g. Nowak & May 1994) point to the inherent difficulties of prediction of the course of these interactions. Prediction and detection of the ecopathological consequences of the use of immunocontraception of wild animals will also be made difficult by the spread of emerging infectious diseases as a result of human activity (Daszak et al. 2000).

The effect of immunocontraception upon genetic diversity could be significant. There is the possibility that restriction of breeding to a small group of animals which are closely related will result in localized inbreeding. This will be especially likely if their capacity to resist the immunocontraceptive is the result of shared uncommon genotype. Acevedo-Whitehouse et al.(2003) have shown that in California sea lions, inbreeding is associated with a wide range of diseases. They suggest that inbred individuals could act disproportionally as reservoirs of infectious agents.

Selection based upon immune responses could be on one of two parts of the genome: the MHC (major histocompatability complex) region which governs responses to specific immunogens, or other genes, e.g. NRAMP which govern the functioning of the immune system in general (Bellamy 1999). The tightly linked MHC genes and the resultant linkage disequilibrium mean that selection on one gene will result in changes in gene frequencies at other loci. This could either raise or lower susceptibility to other pathogens. Understanding of the non-MHC genetic component of variability of the immune response is much less advanced than for the MHC component. This understanding is needed to attempt any predictions concerning immunocontraception-based selection.

Experimental approaches to this question have until now been very difficult. The existence of genetic maps of some wild animals (e.g. Tammar wallaby (Zenger et al. 2002)) may now allow a genomic approach, in which whole genome DNA typing may allow the identification of changes in gene frequency which accompany the application of immunocontraception or a pathogen, through comparing treated and control populations. A concomitant survey of pathogens in the two groups may identify susceptibility regions, whose existence could be further tested in lab-based investigation. The genome would thus be assayed for these genes, and test the extent to which the same genes are involved in responses to different pathogens and to immunocontraception.

A good model system to address these questions is wildlife tuberculosis which is of economic significance in several countries, e.g. Britain (Delahay et al. 2002), New Zealand (Buddle et al. 2002), and the United States (Palmer et al. 2002). Considerable information on the genetic control of response to mycobacterial antigens is available (North & Medina 1998, Kramnik et al. 2000, Bellamy 2003). The possibility of obtaining results relevant to human mycobacterial susceptibility may also encourage use of this system.

We conclude that attempting to use the immunological system to modulate reproduction could be incompatible with the basic biological function of resisting pathogens. We have not discussed some of the practical issues. For example, all fertility control methods have the problem of delivery of the control agent. Highly valued animals must be treated without harming them. When this is the case, fertility control methods with fewer concomitant problems, such as surgical sterilization or the use of steroids or gonadotropin-based hormones, would be competitive with immunocontraception (Cooper & Herbert 2001).

Table 1

Immunocontraception: target species and justification for fertility control.

SpeciesLocationManagement issuesPopulation control needsReferences
K-selected species
    KoalaAustralia; local overpopulationsHabitat degradation; likely destruction of own habitat; highly regarded speciesControl methods with public acceptanceMartin & Handasyde (1999)
    African elephantSouthern AfricaHabitat degradation; public safety and health concerns; highly regarded speciesControl methods with public acceptanceHanks (2001)
    Wild horseUSA, AustraliaHabitat degradation; conflicts with livestock, timber and mining industry interests (USA); highly regarded speciesControl methods with public acceptanceBerger (1986), Dobbie et al.(1993), Furbish & Albano (1994)
    White-tailed deerUSAHabitat degradation; public safety and health concerns; high frequencies of deer-vehicle collisions; crop and garden damageControl methods with public acceptanceMcShea et al.(1997), Warren (1997)
    Feral donkey/BurroUSA, Australia, AfricaHabitat degradation; public safety and health concerns; highly regarded speciesBroad-scale control over large, remote and inaccessible areas (Australia)McCool (1981), Berger (1986), Freeland & Choquenot (1990)
    Brushtail possumNew Zealand; major introduced pest speciesHabitat degradation (New Zealand); public, livestock and wildlife health concerns; reservoir for bovine tuberculosisBroad-scale control over large, often inaccessible, areas (New Zealand). Alternative to poison baits (1080)Montague (2000)
    MacropodsAustraliaPublic, livestock and wildlife health concerns; high frequencies of kangaroo-vehicle collisions; highly regarded speciesControl methods with public acceptanceDawson (1995), Pople & Grigg (1999)
    European red foxAustralia; major introduced pest speciesPredation on native wildlife (Australia); public, livestock and wildlife health concernsControl over continental area (Australia). Alternative to poison baits (1080)Saunders et al.(1995)
    PinnipedsWorldwidePossible contribution to the depletion of fish stocksContraception suggested as humane alternative to cullingButterworth et al.(1988), Brown et al.(1996), Mohn & Bowen (1996)
    Feral catWorldwide; major introduced pest species in AustraliaPredation on native wildlife (Australia); public and wildlife health concernsControl over continental area (Australia) Alternative to poison baits (1080)Newsome (1991),Bomford et al.(1996), Mahlow & Slater (1996)
    Feral dogWorldwidePublic and livestock safety and health concerns; predation on native wildlife (Australia)Control methods with public acceptanceFleming et al.(2001), Sabeta et al.(2003)
    Feral pigWorldwide; major introduced pest species in AustraliaHabitat degradation; damage to economic resources; public, live- stock and wildlife health concernsControl methods with public acceptanceChoquenot et al.(1996)
    BadgerUKPublic, livestock and wildlife health concerns; reservoir for bovine tuberculosisControl methods with public acceptanceKrebs et al.(1998), Donnelly et al.(2003)
    Grey squirrelUK; introduced speciesHabitat degradation; threat to the native Red squirrelControl methods with public acceptanceMoore et al.(1997)
r-selected species
    European rabbitWorldwide; major vertebrate pest species in AustraliaHabitat degradation; major cost to agriculture; public, livestock and wildlife health concernsBroad-scale control over large areasLawson (1995), Williamset al.(1995)
    RodentsWorldwideMajor damage to economic resources, incl. crops, pastures, stored grain, livestock, buildings and infrastructure; public, livestock and wildlife health concernsBroad-scale control over large areas. Species-specific alternatives to rodenticidesCaughley et al.(1998), Chambers et al.(1999), Seamark (2001)
Table 2

Relative fertility of immunocontracepted females in 14 mammalian species.

SpeciesImmunogenAdjuvantNo. of immunizationsReproductive performance (control, treated)Statistical significanceaReduction in relative fertility (%)bReference
Investigations have been conducted on approximately 70 species. This table includes only true experiments, i.e. studies with an immunized group compared with a control group.
aThe P values are those given in the references cited.
bRelative fertility is defined as the mean no. of offspring for females in the vaccinated group divided by the same figure for the control group (i.e. unimmunized females).
BaboonLDH-C4+ promiscuous epitopeCGP11637 emulsified w. Squalene:Arlacel - (4:1)3Offspring/females 10/13, 4/14P < 0.0262O’Hern et al.(1997)
Brushtail possumWhole spermFreund’s complete (FCA), Freund’s incomplete (FIA) in boosters3Offspring/females 12/16, 2/16P < 0.00183Duckworth et al.(1998)
Tammar wallabyPorcine ZPFCA, FIA in boosters5Offspring/females 4/6, 0/6P < 0.05 (n = 6)100Kitchener et al.(2002)
African elephant
    First schedulePorcine ZPAdjuvant used, type not given3Offspring/females 16/18, 8/18P = 0.00550Fayrer-Hosken et al.(2000)
    Second schedulePorcine ZPAdjuvant not mentioned2Offspring/females 2/10 (no true control)P = 0.00177Fayrer-Hosken et al.(2000)
Wild horsePorcine ZPFCA, FIA in boosters3–4Pregnancy rate 3/6, 1/14Not stated85Kirkpatrick et al.(1991)
White-tailed deer
    First schedulePorcine ZPFCA, FIA in booster2Fawns/doe years 30/16, 4/16P < 0.000187Miller et al. (2000a)
    Second scheduleRC55FCA, FIA in booster2Fawns/doe years 30/16, 19/14P < 0.0528Miller et al. (2000a)
    Third scheduleRC75aFCA, FIA in booster2Fawns/doe years 30/16, 11/8P < 0.0127Miller et al. (2000a)
    Fourth scheduleCombined antigensFCA, FIA in booster2Fawns/doe years 30/16, 16/8P>0.050Miller et al. (2000a)
White-tailed deerKLH-GnRHFCA, FIA in boosters2–4Fawns/doe years 35/19, 5/24P < 0.0189Miller et al. (2000b)
White-tailed deerPorcine ZPFCA, FIA in boosters2–3Fawns/doe years 35/19, 25/57P < 0.0176Miller et al. (2000c)
White-tailed deer
    First scheduleGnRHFCA, FIA in boosters3Fawns/doe years 110/90, 36/118P < 0.000575Curtis et al.(2002)
    Second schedulePorcine ZPFCA, FIA in boosters3Fawns/doe years 72/56, 10/60P < 0.000587Curtis et al.(2002)
Fallow deerSpayVacFCA1Pregnancy rate 322/334, 0/22P < 0.0001100Fraker et al.(2002)
BurroPorcine ZPFCA, FIA in boosters2–3Offspring/females 6/11, 1/16P < 0.0588Turner et al.(1996)
Grey sealSIZP (SpayVac)FCA1Pups/female 2.76, 0.22P < 0.00192Brown et al.(1996, 1997)
Tule elkPorcine ZPFCA, FIA in boosters3–4Calves/cow years 53/91, 5/104Not stated91Shideler et al.(2002)
CatPorcine ZPFCA, FIA in boosters5Pregnancy rate 2/2, 1/5Not stated50Ivanova et al.(1995)
Cat
    First scheduleSpayVacFCA1Mean litter size 5.2, 4.5P = 0.885913Gorman et al.(2002)
    Second scheduleSpayVacAlum1Mean litter size 5.2, 4.4P = 0.885915Gorman et al.(2002)
European rabbitMyxoma vectored ZPBFCA, FIA in boosters3Mean litter size 7.4, 7.0Not stated5Kerr et al.(1999)
Norway rat
    First scheduleMZPP/KLHFCA, FIA in boosters3Pregnancy rate 7/8, 4/8P>0.0540Miller et al.(1997)
    Second scheduleGnRH/KLHFCA, FIA in boosters3Pregnancy rate 7/8, 0/8P < 0.004100Miller et al.(1997)
Wild mouseKLH-mZP3FCA, FIA in boosters5Pregnancy rate 8/15, 7/30P = 0.04656Hardy et al. (2002b)
BALB/c mouse
    First schedule (71–81 days)Murine rFA-1FCA, FIA in boosters4Mean litter size 8.9, 3.2P < 0.000164Naz & Zhu (1998)
    Second schedule (283 days)Murine rFA-1FCA, FIA in boosters4Mean litter size 8.6, 9P>0.050Naz & Zhu (1998)
BALB/c mouse
    First schedulesp56FLAGFCA, FIA in boosters6Offspring/females 55/14, 12/5P = 001739Hardy & Mobbs (1999)
    Second schedulesp56FLAGFCA, FIA in boosters4Offspring/females 55/14, 19/5Not stated3Hardy & Mobbs (1999)
BALB/c mouse
    First scheduleMBP-polyepitope AFCA, FIA in boosters4Mean litter size 5.2, 3.3Not stated37Hardy et al. (2002a)
    Second scheduleMBP-polyepitope BFCA, FIA in boosters4Mean litter size 5.2, 2.1P < 0.0560Hardy et al. (2002a)
    Third schedule6XHis-polyepitope AFCA, FIA in boosters4Mean litter size 6.5, 6.3Not stated3Hardy et al. (2002a)
Table 3

Predicted proportion of non-responder daughters after one generation of selection by immunocontraception of mothers given various heritabilities (after Falconer 1965).

Heritability (%)
Non-responder mothers (%)100806050
The prediction has been arrived at by entering the table in Falconer (1965) which relates heritability for a threshold trait to incidences in parent and offspring. The response to selection (predicted percentage of non-responders) obtained has been halved because selection is being carried out on one sex.
51511108
1023191615

Received 21 May 2006
 First decision 22 June 2006
 Revised manuscript received 30 July 2006
 Accepted 10 October 2006

We acknowledge helpful comments from John Aitken, Tony Basten, Kathy Belov, David Briscoe, Bryce Buddle, Margaret Carrington, Charles Daugherty, Dick Frankham, Cathy Herbert, John McKenzie, Bill Sherwin, Jim Shields, Roger Short, and Kyall Zenger. Our research on population control in koalas and kangaroos is supported by the Australian Research Council grant LPO560344. The authors declare that there is no conflict of interest that would prejudice the impartiality of this scientific work.

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  • Gupta SK & Talwar GP1994 Contraceptive vaccines. Advances in Contraceptive Delivery Systems10255–265.

  • Hanks J2001 Conservation strategies for Africa’s large mammals. Reproduction Fertility and Development13459–468.

  • Hardy CM & Mobbs KJ1999 Expression of recombinant mouse sperm protein sp56 and assessment of its potential for use as an antigen in an immunocontraceptive vaccine. Molecular Reproduction and Development52216–224.

  • Hardy CM Pekin J & ten Have JF2002a Mouse-specific immunocontraceptive polyepitope vaccines. Reproduction (Cambridge England) Supplement6019–30.

  • Hardy CM ten Have JF Mobbs KJ & Hinds LA2002b Assessment of the immunocontraceptive effect of a zona pellucida 3 peptide antigen in wild mice. Reproduction Fertility and Development14151–155.

  • Harrenstien LA Munson L Chassy LM Liu IK & Kirkpatrick JF2004 Effects of porcine zona pellucida immunocontraceptives in zoo felids. Journal of Zoo and Wildlife Medicine35271–279.

  • Hill AV2001 The genomics and genetics of human infectious disease susceptibility. Annual Review of Genomics and Human Genetics2373–400.

  • Ivanova M Petrov M Klissourska D & Mollova M1995 Contraceptive potential of procine zona pellucida in cats. Theriogenology43969–981.

  • Jackson RJ Ramsay AJ Christensen CD Beaton S Hall DF & Ramshaw IA2001 Expression of mouse interleukin-4 by a recombinant ectromelia virus suppresses cytolytic lymphocyte responses and overcomes genetic resistance to mousepox. Journal of Virology751205–1210.

  • Joshi SH1973 An immunological approach to fertility control. American Journal of Pharmacy14522–26.

  • Kerr PJ Jackson RJ Robinson AJ Swan J Silvers L French N Clarke H Hall DF & Holland MK1999 Infertility in female rabbits (Oryctolagus cuniculus) alloimmunized with the rabbit zona pellucida protein ZPB either as a purified recombinant protein or expressed by recombinant myxoma virus. Biology of Reproduction61606–613.

  • Kirkpatrick JF Liu IKM Turner JW & Bernoco M1991 Antigen recognition in feral mares previously immunized with porcine zonae pellucidae. Journal of Reproduction and Fertility. Supplement44321–325.

  • Kirkpatrick JF Naugle R Liu IKM & Turner JW1995Effects of Seven Consecutive Years of Porcine Zonae Pellucidae Contraception on Ovarian Function in Feral MaresBiology of Reproduction Monograph Series. vol 1 pp 411–413 (Equine Reproduction VI).

  • Kitchener AL Edds LM Molinia FC & Kay DJ2002 Porcine zonae pellucidae immunization of tammar wallabies (Macropus eugenii): fertility and immune responses. Reproduction Fertility and Development14215–223.

  • Klein J Satta Y O’HUigin C & Takahata N1993 The molecular descent of the major histocompatibility complex. Annual Review of Immunology11269–295.

  • Kramnik I Dietrich WF Demant P & Bloom BR2000 Genetic control of resistance to experimental infection with virulent Mycobacterium tuberculosis. PNAS978560–8565.

  • Krebs JR Anderson RM Clutton-Brock T Donnelly CA Frost S Morrison WI Woodroffe R & Young D1998 Badgers and bovine TB: conflicts between conservation and health. Science279817–818.

  • Lawson M1995 Rabbit virus threatens ecology after leaping the fence. Nature378531.

  • Leenaars PP Hendriksen CF Angulo AF Koedam MA & Claassen E1994 Evaluation of several adjuvants as alternatives to the use of Freund’s adjuvant in rabbits. Veterinary Immunology and Immunopathology40225–241.

  • Leenaars PP Koedam MA Wester PW Baumans V Claassen E & Hendriksen CF1998 Assessment of side effects induced by injection of different adjuvant/antigen combinations in rabbits and mice. Laboratory Animals32387–406.

  • Lively CM & Dybdahl MF2000 Parasite adaptation to locally common host genotypes. Nature405679–681.

  • Mackintosh CG Qureshi T Waldrup K Labes RE Dodds KG & Griffin JF2000 Genetic resistance to experimental infection with Mycobacterium bovis in red deer (Cervus elaphus). Infection and Immunity681620–1625.

  • Mahlow JC & Slater MR1996 Current issues in the control of stray and feral cats. Journal of the American Veterinary Medical Association2092016–2020.

  • Martin R & Handasyde K1999The Koala: Natural History Conservation and Management Sydney: University of New South Wales Press Ltd.

  • McCool CJ1981Feral Donkeys in the Northern Territory: Report to the Feral Animals Committee of a Working Party on the Feral Donkey Problem Darwin: Department of Primary Production.

  • McKenzie JA1996Ecological and Evolutionary Aspects of Insecticide Resistance Texas USA: Academic Press/R.G. Landes.

  • McNicholl JM & Cuenco KT1999 Host genes and infectious diseases. HIV other pathogens and a public health perspective. American Journal of Preventive Medicine16141–154.

  • McShea WJ Underwood HB & Rappole JH1997The Science of Overabundance: Deer Ecology and Population Management Washington D.C.: Smithsonian Institution Press.

  • Miller LA Johns BE Elias DJ & Crane KA1997 Comparative efficacy of two immunocontraceptive vaccines. Vaccine151858–1862.

  • Miller LA Johns BE & Killian GJ2000a Immunocontraception of white-tailed deer using native and recombinant zona pellucida vaccines. Animal Reproduction Science63187–195.

  • Miller LA Johns BE & Killian GJ2000b Immunocontraception of white-tailed deer with GnRH vaccine. American Journal of Reproductive Immunology44266–274.

  • Miller LA Johns BE & Killian GJ2000c Long-term effects of PZP immunization on reproduction in white-tailed deer. Vaccine18568–574.

  • Mohn R & Bowen WD1996 Grey seal predation on the Eastern Scotian Shelf: modeling the impact on Atlantic cod. Canadian Journal of Fisheries and Aquatic Sciences532722–2738.

  • Montague TLe2000The Brushtail Possum: Biology Impact and Management of an Introduced Marsupial Lincoln NZ: Manaaki Whenua Press.

  • Moore HD Jenkins NM & Wong C1997 Immunocontraception in rodents: a review of the development of a sperm-based immuno-contraceptive vaccine for the grey squirrel (Sciurus carolinensis). Reproduction Fertility and Development9125–129.

  • Naz RK & Zhu X1998 Recombinant fertilization antigen-1 causes a contraceptive effect in actively immunized mice. Biology of Reproduction591095–1100.

  • Newsome AE1991 Feral cats: an overview. In The Impact of Cats on Native Wildlife Ed. C Potter. Canberra: Australian National Parks and Wildlife Service.

  • North RJ & Medina E1998 How important is Nramp1 in tuberculosis?. Trends in Microbiology6441–443.

  • Nowak MA & May RM1994 Superinfection and the evolution of parasite virulence. Proceedings of the Royal Society of London. Series B25581–89.

  • O’Hern PA Liang ZG Bambra CS & Goldberg E1997 Colinear synthesis of an antigen-specific B-cell epitope with a ‘promiscuous’ tetanus toxin T-cell epitope: a synthetic peptide immunocontraceptive. Vaccine151761–1766.

  • Oogjes G1997 Ethical aspects and dilemmas of fertility control of unwanted wildlife: an animal welfarist’s perspective. Reproduction Fertility and Development9163–167.

  • Palmer MV Waters WR & Whipple DL2002 Milk containing Mycobacterium bovis as a source of infection for white-tailed deer fawns (Odocoileus virginianus). Tuberculosis (Edinburgh Scotland)82161–165.

  • Pimm SL & van Aarde RJ2001 Population control: African elephants and contraception. Nature411766.

  • Pople T & Grigg G1999Commercial Harvesting of Kangaroos in Australia Canberra: Environment Australia.

  • Rao AJ2001 Is there a role for contraceptive vaccines in fertility control?. Journal of Biosciences26425–427.

  • Richter J1994 Anti-fertility ‘vaccines’: a plea for an open debate on the prospects of research. Newsletter (Women’s Global Network on Reproductive Rights)463–5.

  • Sabeta CT Bingham J & Nel LH2003 Molecular epidemiology of canid rabies in Zimbabwe and South Africa. Virus Research91203–211.

  • Saunders GR Coman B Kinnear J & Braysher M1995Managing Vertebrate Pests: Foxes Canberra: Bureau of Rural Science.

  • Seamark RF2001 Biotech prospects for the control of introduced mammals in Australia. Reproduction Fertility and Development13705–711.

  • Shideler SE Stoops MA Gee NA Howell JA & Lasley BL2002 Use of porcine zona pellucida (PZP) vaccine as a contraceptive agent in free-ranging tule elk (Cervus elaphus nannodes). Reproduction (Cambridge England) Supplement60169–176.

  • Stevens VC1975 Potential control of fertility in women by immunization with HCG. Research in Reproduction1–2.

  • Turner A & Kirkpatrick JF2002 Effects of immunocontraception on population longevity and body condition in wild mares (Equus caballus). Reproduction (Cambridge England) Supplement60187–195.

  • Turner JW Liu IKM & Kirkpatrick JF1996 Remotely delivered immunocontraception in free-roaming feral burros (Equus asinus). Journal of Reproduction and Fertility10731–35.

  • Turner JW Liu IKM Rutberg AT & Kirkpatrick JF1997 Immunocontraception limits foal production in free-roaming feral horses in Nevada. Journal of Wildlife Management10731–35.

  • Turner JW Liu IKM Flanagan DR Bynum KS & Rutberg AT2002 Porcine zona pellucida (PZP) immunocontraception of wild horses (Equus caballus) in Nevada: a 10 year study. Reproduction (Cambridge England) Supplement60177–186.

  • Tyndale-Biscoe CH1991 Fertility control in wildlife. Reproduction Fertility and Development3339–343.

  • Tyndale-Biscoe CH1994 Virus-vectored immunocontraception of feral mammals. Reproduction Fertility and Development6281–287.

  • Warren RJ1997 The challenge of deer overabundance in the 21st century. Wildlife Society Bulletin25213–214.

  • Williams K Parer I Coman B Burley J & Braysher M1995Managing Vertebrate Pests: Rabbits Canberra: Bureau of Rural Science.

  • Woolhouse ME Webster JP Domingo E Charlesworth B & Levin BR2002 Biological and biomedical implications of the co-evolution of pathogens and their hosts. Nature Genetics32569–577.

  • Zenger KR McKenzie LM & Cooper DW2002 The first comprehensive genetic linkage map of a marsupial: the tammar wallaby (Macropus eugenii). Genetics162321–330.

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Gorman SF Levy JK Hampton AL Collante WR Harris AL & Brown RG2002 Evaluation of a porcine zona pellucida vaccine for the immunocontraception of domestic kittens (Felis catus). Theriogenology58135–149.

Grandy JW & Rutberg AT2002 An animal welfare view of wildlife contraception. Reproduction (Cambridge England) Supplement601–7.

Gupta SK & Talwar GP1994 Contraceptive vaccines. Advances in Contraceptive Delivery Systems10255–265.

Hanks J2001 Conservation strategies for Africa’s large mammals. Reproduction Fertility and Development13459–468.

Hardy CM & Mobbs KJ1999 Expression of recombinant mouse sperm protein sp56 and assessment of its potential for use as an antigen in an immunocontraceptive vaccine. Molecular Reproduction and Development52216–224.

Hardy CM Pekin J & ten Have JF2002a Mouse-specific immunocontraceptive polyepitope vaccines. Reproduction (Cambridge England) Supplement6019–30.

Hardy CM ten Have JF Mobbs KJ & Hinds LA2002b Assessment of the immunocontraceptive effect of a zona pellucida 3 peptide antigen in wild mice. Reproduction Fertility and Development14151–155.

Harrenstien LA Munson L Chassy LM Liu IK & Kirkpatrick JF2004 Effects of porcine zona pellucida immunocontraceptives in zoo felids. Journal of Zoo and Wildlife Medicine35271–279.

Hill AV2001 The genomics and genetics of human infectious disease susceptibility. Annual Review of Genomics and Human Genetics2373–400.

Ivanova M Petrov M Klissourska D & Mollova M1995 Contraceptive potential of procine zona pellucida in cats. Theriogenology43969–981.

Jackson RJ Ramsay AJ Christensen CD Beaton S Hall DF & Ramshaw IA2001 Expression of mouse interleukin-4 by a recombinant ectromelia virus suppresses cytolytic lymphocyte responses and overcomes genetic resistance to mousepox. Journal of Virology751205–1210.

Joshi SH1973 An immunological approach to fertility control. American Journal of Pharmacy14522–26.

Kerr PJ Jackson RJ Robinson AJ Swan J Silvers L French N Clarke H Hall DF & Holland MK1999 Infertility in female rabbits (Oryctolagus cuniculus) alloimmunized with the rabbit zona pellucida protein ZPB either as a purified recombinant protein or expressed by recombinant myxoma virus. Biology of Reproduction61606–613.

Kirkpatrick JF Liu IKM Turner JW & Bernoco M1991 Antigen recognition in feral mares previously immunized with porcine zonae pellucidae. Journal of Reproduction and Fertility. Supplement44321–325.

Kirkpatrick JF Naugle R Liu IKM & Turner JW1995Effects of Seven Consecutive Years of Porcine Zonae Pellucidae Contraception on Ovarian Function in Feral MaresBiology of Reproduction Monograph Series. vol 1 pp 411–413 (Equine Reproduction VI).

Kitchener AL Edds LM Molinia FC & Kay DJ2002 Porcine zonae pellucidae immunization of tammar wallabies (Macropus eugenii): fertility and immune responses. Reproduction Fertility and Development14215–223.

Klein J Satta Y O’HUigin C & Takahata N1993 The molecular descent of the major histocompatibility complex. Annual Review of Immunology11269–295.

Kramnik I Dietrich WF Demant P & Bloom BR2000 Genetic control of resistance to experimental infection with virulent Mycobacterium tuberculosis. PNAS978560–8565.

Krebs JR Anderson RM Clutton-Brock T Donnelly CA Frost S Morrison WI Woodroffe R & Young D1998 Badgers and bovine TB: conflicts between conservation and health. Science279817–818.

Lawson M1995 Rabbit virus threatens ecology after leaping the fence. Nature378531.

Leenaars PP Hendriksen CF Angulo AF Koedam MA & Claassen E1994 Evaluation of several adjuvants as alternatives to the use of Freund’s adjuvant in rabbits. Veterinary Immunology and Immunopathology40225–241.

Leenaars PP Koedam MA Wester PW Baumans V Claassen E & Hendriksen CF1998 Assessment of side effects induced by injection of different adjuvant/antigen combinations in rabbits and mice. Laboratory Animals32387–406.

Lively CM & Dybdahl MF2000 Parasite adaptation to locally common host genotypes. Nature405679–681.

Mackintosh CG Qureshi T Waldrup K Labes RE Dodds KG & Griffin JF2000 Genetic resistance to experimental infection with Mycobacterium bovis in red deer (Cervus elaphus). Infection and Immunity681620–1625.

Mahlow JC & Slater MR1996 Current issues in the control of stray and feral cats. Journal of the American Veterinary Medical Association2092016–2020.

Martin R & Handasyde K1999The Koala: Natural History Conservation and Management Sydney: University of New South Wales Press Ltd.

McCool CJ1981Feral Donkeys in the Northern Territory: Report to the Feral Animals Committee of a Working Party on the Feral Donkey Problem Darwin: Department of Primary Production.

McKenzie JA1996Ecological and Evolutionary Aspects of Insecticide Resistance Texas USA: Academic Press/R.G. Landes.

McNicholl JM & Cuenco KT1999 Host genes and infectious diseases. HIV other pathogens and a public health perspective. American Journal of Preventive Medicine16141–154.

McShea WJ Underwood HB & Rappole JH1997The Science of Overabundance: Deer Ecology and Population Management Washington D.C.: Smithsonian Institution Press.

Miller LA Johns BE Elias DJ & Crane KA1997 Comparative efficacy of two immunocontraceptive vaccines. Vaccine151858–1862.

Miller LA Johns BE & Killian GJ2000a Immunocontraception of white-tailed deer using native and recombinant zona pellucida vaccines. Animal Reproduction Science63187–195.

Miller LA Johns BE & Killian GJ2000b Immunocontraception of white-tailed deer with GnRH vaccine. American Journal of Reproductive Immunology44266–274.

Miller LA Johns BE & Killian GJ2000c Long-term effects of PZP immunization on reproduction in white-tailed deer. Vaccine18568–574.

Mohn R & Bowen WD1996 Grey seal predation on the Eastern Scotian Shelf: modeling the impact on Atlantic cod. Canadian Journal of Fisheries and Aquatic Sciences532722–2738.

Montague TLe2000The Brushtail Possum: Biology Impact and Management of an Introduced Marsupial Lincoln NZ: Manaaki Whenua Press.

Moore HD Jenkins NM & Wong C1997 Immunocontraception in rodents: a review of the development of a sperm-based immuno-contraceptive vaccine for the grey squirrel (Sciurus carolinensis). Reproduction Fertility and Development9125–129.

Naz RK & Zhu X1998 Recombinant fertilization antigen-1 causes a contraceptive effect in actively immunized mice. Biology of Reproduction591095–1100.

Newsome AE1991 Feral cats: an overview. In The Impact of Cats on Native Wildlife Ed. C Potter. Canberra: Australian National Parks and Wildlife Service.

North RJ & Medina E1998 How important is Nramp1 in tuberculosis?. Trends in Microbiology6441–443.

Nowak MA & May RM1994 Superinfection and the evolution of parasite virulence. Proceedings of the Royal Society of London. Series B25581–89.

O’Hern PA Liang ZG Bambra CS & Goldberg E1997 Colinear synthesis of an antigen-specific B-cell epitope with a ‘promiscuous’ tetanus toxin T-cell epitope: a synthetic peptide immunocontraceptive. Vaccine151761–1766.

Oogjes G1997 Ethical aspects and dilemmas of fertility control of unwanted wildlife: an animal welfarist’s perspective. Reproduction Fertility and Development9163–167.

Palmer MV Waters WR & Whipple DL2002 Milk containing Mycobacterium bovis as a source of infection for white-tailed deer fawns (Odocoileus virginianus). Tuberculosis (Edinburgh Scotland)82161–165.

Pimm SL & van Aarde RJ2001 Population control: African elephants and contraception. Nature411766.

Pople T & Grigg G1999Commercial Harvesting of Kangaroos in Australia Canberra: Environment Australia.

Rao AJ2001 Is there a role for contraceptive vaccines in fertility control?. Journal of Biosciences26425–427.

Richter J1994 Anti-fertility ‘vaccines’: a plea for an open debate on the prospects of research. Newsletter (Women’s Global Network on Reproductive Rights)463–5.

Sabeta CT Bingham J & Nel LH2003 Molecular epidemiology of canid rabies in Zimbabwe and South Africa. Virus Research91203–211.

Saunders GR Coman B Kinnear J & Braysher M1995Managing Vertebrate Pests: Foxes Canberra: Bureau of Rural Science.

Seamark RF2001 Biotech prospects for the control of introduced mammals in Australia. Reproduction Fertility and Development13705–711.

Shideler SE Stoops MA Gee NA Howell JA & Lasley BL2002 Use of porcine zona pellucida (PZP) vaccine as a contraceptive agent in free-ranging tule elk (Cervus elaphus nannodes). Reproduction (Cambridge England) Supplement60169–176.

Stevens VC1975 Potential control of fertility in women by immunization with HCG. Research in Reproduction1–2.

Turner A & Kirkpatrick JF2002 Effects of immunocontraception on population longevity and body condition in wild mares (Equus caballus). Reproduction (Cambridge England) Supplement60187–195.

Turner JW Liu IKM & Kirkpatrick JF1996 Remotely delivered immunocontraception in free-roaming feral burros (Equus asinus). Journal of Reproduction and Fertility10731–35.

Turner JW Liu IKM Rutberg AT & Kirkpatrick JF1997 Immunocontraception limits foal production in free-roaming feral horses in Nevada. Journal of Wildlife Management10731–35.

Turner JW Liu IKM Flanagan DR Bynum KS & Rutberg AT2002 Porcine zona pellucida (PZP) immunocontraception of wild horses (Equus caballus) in Nevada: a 10 year study. Reproduction (Cambridge England) Supplement60177–186.

Tyndale-Biscoe CH1991 Fertility control in wildlife. Reproduction Fertility and Development3339–343.

Tyndale-Biscoe CH1994 Virus-vectored immunocontraception of feral mammals. Reproduction Fertility and Development6281–287.

Warren RJ1997 The challenge of deer overabundance in the 21st century. Wildlife Society Bulletin25213–214.

Williams K Parer I Coman B Burley J & Braysher M1995Managing Vertebrate Pests: Rabbits Canberra: Bureau of Rural Science.

Woolhouse ME Webster JP Domingo E Charlesworth B & Levin BR2002 Biological and biomedical implications of the co-evolution of pathogens and their hosts. Nature Genetics32569–577.

Zenger KR McKenzie LM & Cooper DW2002 The first comprehensive genetic linkage map of a marsupial: the tammar wallaby (Macropus eugenii). Genetics162321–330.

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