Intentional Genetic Modifications of Antelopes & Other Large Mammals

Home , African buffalo, Black wildebeest, Blue duiker, European fallow deer, Oribi, Red hartebeest

Conference Antelope Giraffe,Hippo 2017 February 19-25, 2017, Prague, Czech Republic

Intentional genetic modifications of antelopes & other large mammals

Philippe Chardonnet & David Mallon

IGF Foundation Antelope Specialist Group SSC/IUCN Historical perspective of Intentional Genetic Modifications (IGM)

IGM of wildlife:

born with the anthropocene© François Diaz First domestications >10,000 years ago Domestic animal Wild animal production production * about 20 sp. mammals * +4,500 sp. mammals * about 15 sp. birds * +10,000 sp. birds Ancient domestication >2,000 years ago China: pionner country in deer farming

FAO/Czech Government Workshop - Prague, Czech Republic, 11-15 September 2006 Modern domestication: last century

FAO/Czech Government Workshop - Prague, Czech Republic, 11-15 September 2006 hunting Nowadays: Surface Wildlife production required herding systems

ranching

farming

feedlot

Stocking rate

Animal Improvement Act No. 62 of 1998 National Gazette No. 40075, 17 June 2016, Vol 612, Pg. 3

A major step forward for the South African Wildlife Industry has come to light as the Department of Agriculture, Forestry and Fisheries (DAFF) recently added twelve wildlife species to the list of tame and domesticated animals, currently regulated under its Animal Improvement Act (No. 62 of 1998). This alteration will allow game ranchers to breed and manage their wildlife similar to livestock farmers, which obtain animals with specific characteristics for agricultural purposes. The description in the Animal Improvement Act states that listed animals may be used “for the breeding, identification and utilisation of genetically superior animals in order to improve the production and performance of animals in the interest of the Republic; and to provide for matters connected therewith”. The listing of these species together with domestic stock comes as a leap forward for the game industry, as numerous game ranchers today comes from a background of cattle farming and breeding with domestic animals, and has in recent years applied several management methods to the breeding and enhancing the number and quality of their wildlife animals. The species added to the list are Black Wildebeest, Blue Wildebeest, Blue Duiker, Bontebok, Gemsbok, Impala, Oribi, Red Hartebeest, Roan, Sable, Springbok, and Tsessebe whereas the only wild animal that was previously listed under the Animal Improvement Act, was the Ostrich. Adriaan Snyman, 22 July 2016 Now: …toward the legal gazetting/listing of IGM:

Animal Improvement Act No. 62 of 1998 National Gazette No. 40075, 17 June 2016, Vol 612, Pg. 3

… the integrity of

IGM of wildlife:

all over the world © François Diaz Asia Long standing & intensive selection of several species of Cervids for velvet production

(here: a « champion » Formosan sambar deer in Taiwan)

Taxonomic perspective of Intentional Genetic Modifications (IGM)

IGM of wildlife: many aquatic & terrestrial wildlife sp. © François Diaz Nairobi Declaration CONSERVATION OF AQUATIC BIODIVERSITY AND USE OF GENETICALLY IMPROVED AND ALIEN SPECIES FOR AQUACULTURE IN AFRICA NAIROBI, KENYA 20 -23 FEBRUARY 2002 Strawberry Leopard www.io9.com Photo by Deon de Villiers via National Geographic

White lion The Golden Times issue 1 2015 Golden Breeders - « Hunting for colours » Many IGM candidates in antelopes…

Bongo in Central African Republic:

Leucistic Regular Leucistic reedbuck

Leucistic Uganda kob Leucistic impala, Kruger NP

Leucistic impala, South Africa © H. Planton © M. Fischer Cameroon Ethiopia Albino red duiker, Isimangaliso Wetland Park

… and candidates in African buffalo

White buffalo, South Africa IGM methods & impacts

IGM of wildlife:

• Natural breeding: - Outbreeding = crossing distinct taxa - Inbreeding = selection within taxa • Artificial breeding: - AI, embryo transfer etc. - Cloning, Crispr-Cas9 etc. IGM methods & impacts

IGM of wildlife:

• Natural breeding: - Outbreeding = crossing distinct taxa - Inbreeding = selection within taxa • Artificial breeding: - AI, embryo transfer etc. - Cloning, Crispr-Cas9 etc. Tentative typology Examples "Influencing" Introgression of giant sable by roan antelope (maybe human-induced) Hybridization natural Scimitar-horned oryx x addax hybridization Eland x greater kudu = mixing Blue wildebeest x black wildebeest Intentional species Blesbok x bontebok hybridization Lion x tiger Crossing Between In-country translocations with no consideration for regional specificities indigenous taxa taxa Crossing = Livingstone eland x Cape eland All provenances of roan antelope, of sable antelope mixing East African buffalo x Southern African buffalo Crossing exotic subspecies European fallow deer x Mesopotamian fallow deer taxa or strains Red deer x elk/wapiti Red deer x Père David deer Sika deer x red deer x elk/wapiti xxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxCloning Experimentation Several experiences, e.g. in gaurxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxx in USA, in various species in RSA xxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxBody size: red deer, sika deer,xxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxx fallow deer, elk, lion Morphology Trophy size and shape: African buffalo, red deer, elk, white-tailed deer xxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxx Extreme Coat colour: antelopes, red deer, lion Genetic manipulationsxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxWithin of wildlife xxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxx Behaviour Tameness: red deer, African buffalo, cane rat, ostrich xxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxinbreeding xxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxx taxa Reproduction Breeding performances: red deer, sika deer, sambar deer, cane rat, ostrich xxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxx Feeding Daily growth rate, nutritional efficiency: cervids, cane rat, ostrich, crocodile xxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxx Selective xxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxTrophy size Cervids, ovids xxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxx x harvesting Tentative typology Examples "Influencing" Introgression of giant sable by roan antelope (maybe human-induced) Hybridization natural Scimitar-horned oryx x addax hybridization Eland x greater kudu = mixing Blue wildebeest x black wildebeest Intentional species Blesbok x bontebok hybridization Lion x tiger Crossing Between In-country translocations with no consideration for regional specificities indigenous taxa taxa Crossing = Livingstone eland x Cape eland All provenances of roan antelope, of sable antelope mixing East African buffalo x Southern African buffalo Crossing exotic subspecies European fallow deer x Mesopotamian fallow deer taxa or strains Red deer x elk/wapiti Red deer x Père David deer Sika deer x red deer x elk/wapiti Cloning Experimentation Several experiences, e.g. in gaur in USA, in various species in RSA Body size: red deer, sika deer, fallow deer, elk, lion Morphology Trophy size and shape: African buffalo, red deer, elk, white-tailed deer Extreme Coat colour: antelopes, red deer, lion Genetic manipulationsWithin of wildlife inbreeding Behaviour Tameness: red deer, African buffalo, cane rat, ostrich taxa Reproduction Breeding performances: red deer, sika deer, sambar deer, cane rat, ostrich Feeding Daily growth rate, nutritional efficiency: cervids, cane rat, ostrich, crocodile Selective Trophy size Cervids, ovids harvesting IGM between taxa: outbreeding 1°) Between different taxa: mixing taxa IGM by outbreeding 1°) Between different taxa: mixing taxa 1.1. Hybridization = mixing species IGM by outbreeding 1°) Between different taxa: mixing taxa 1.1. Hybridization = mixing species 1.2. Crossing = mixing subspecies or strains Hybridization = mixing species Hybridization = mixing species

- natural - intentional « Natural » hybridization e.g. giant sable x roan antelope in Angola (thanks to Pedro Vaz Pinto, 2011 - Palanca Report July/August 2011)

e.g. translocating East African buffaloes to Southern Africa

► impact on importing countries

biological impact = genetic pollution of local buffaloes: loss of local taxa: no more ‘thoroughbreds’

►impact on exporting countries

economic impact = deprivation of specific assets:

loss of national heritage Impact of intentional “mixing” of taxa: o uncontrolled distortion of natural processes of evolution; o genetic pollution: loss of indigenous taxa; o homogenization of taxa at national level; o globalization of taxa at world’s level; o potential weakened resilience = reduced adaptability to any change: health hazard, ecosystem transformation, climate change etc. IGM within taxa: inbreeding 2°) Within a given taxon = selection of specific traits IGM by inbreeding 2°) Within a given taxon = selection of specific traits

Type of trait Trait e.g. in:

Body Size Red deer, lion

Size Many game species Morphology Trophy Shape Buffalo, lion, red deer

Color Wholebody or part of it Antelopes, lion

Behavior Temperament:tameness Red deer,buffalo

Fertility Many game species Breeding Fecundity Cane rat

Response to complementary feeding (vs. adaptation Many species Feeding to food shortage) Food transformation efficiency, daily growth rate Cane rat, red deer Selection for larger trophies to produce « mega-trophies » Buffalo named “Horizon” with huge wide horn span auctioned at US$11.1 Selection for coat colour variants to produce oustanding coloured animals Selection of recessive characters which are expressed & retained by extreme inbreeding Natural colour variants becoming new taxa: e.g. impala: - the black impala - the saddled impala - others Natural colour variants becoming new taxa: e.g. wildebeest: - the golden wildebeest … royal wildebeest & others

Natural Transformed habitat (converted) habitat

Extensive wildlife Intensive ranching wildlife ranching

Compartments: segregating IGMed wildlife from genuine “natural” wildlife

…however:

compartments are not 100% wildlife proof: risk of “leakage” © Philippe Chardonnet Genetic impact of fragmentation:

© Philippe Chardonnet Genetic impact of fragmentation: What happens? [e.g.: African buffalo in Protected Areas in Kenya & Uganda (Heller et al., 2010)] in small protected areas: - lower genetic diversity of the populations; - populations tend to diverge (genetic drift) further from other populations elsewhere. What risks? - lower breeding fitness & offspring fitness; - less adaptability to environmental changes, etc.; - reliance on active management to ensure exchange of genetic material. © Philippe Chardonnet Veterinary concerns in relation to intensive & selective wildlife systems Impact of intensive wildlife systems on health Density-dependant diseases

Tuberculosis in antelopes and cervids

Sarcoptic mange in deer

FAO/Czech Government Workshop - Prague, Czech Republic, 11-15 September 2006 Impact of intensive wildlife systems on health

Stress-dependant diseases

• intraspecific stress • extraspecific stress • nutritional stress • climate-induced stress • disease-induced stress • human-induced stress • etc

FAO/Czech Government Workshop - Prague, Czech Republic, 11-15 September 2006 Impact of intensive wildlife systems on health

Reliance of wildlife on humans i.e.: on close management, especially on veterinary care (prophylaxy & treatment):

• Disrupts natural evolutionary processes in pathogens & hosts (e.g. immunity response of hosts, defense reaction of pathogens); • Either weakens exposure of hosts to pathogens resulting in lower capacity of hosts to defend themselves; • Or suppresses exposure of hosts to pathogens resulting in hosts becoming naïve towards pathogens; • Lead the immunity system of hosts to be poorly challenged, resulting in hosts becoming weak in reacting to pathogens, including to emerging (new) pathogens; • Intensively bred wildlife becomes poor candidate for reintroduction purposes: of little value to conservation. Impact of selective wildlife systems on health

Extreme selection of wildlife for specific traits : • Narrows genetic heterogeneity of the species at both scale (i) population & (ii) individual; • Disrupts natural processes of coevolution of the species with its global environment including predation, diseases, multi-specific competition, habitat transformation, climate change etc.; • Thus, reduces its capacity of adaptation (adaptability) to new situations (expected or not): ecosystem transformation, climate change etc. • Thus, reduces its capacity of resistance and recovery (resilience) to all sorts of shocks: health hazards, weather accidents etc.; • Exposes the species to a degrading trend of its conservation status. Impact of selective & intensive wildlife systems on health

Entering into a vicious cycle?

When poorly managed, selective & intensive wildlife systems tend to:

• select resistance in pathogens (infectious agents and parasites); • weaken the immunity system of wildlife; • disconnect the evolutionnary processes of hosts and pathogens with unknonw consequences; • increase progressively (indefinitely?) the reliance of ranched wildlife on drugs and human care. Public health issues: « One Health » concerns

Wildlife offers a great opportunity for research in human medicine and livestock industry to investigate the resistance and/or tolerance of wildlife to a number of diseases affecting humans and/or livestock e.g.: trypanosomosis, tick-borne diseases, ASF, RVF, theileriosis, FMD

But:

- Intensive wildlife systems with their reliance on veterinary interference and artificial support might lead to lose this opportunity; - Disease-free buffalo expose the species to lose resistance and/or tolerance to diseases especially given the evolutionay processes of pathogens. Public health issues: « One Health » concerns

Recent findings:

- Spread of antibiotic resistance from human to animal populations; - Risk of antibiotic resistance diffusion between wildlife, livestock and human populations.

Communication presented at the 2nd International Symposium on African Buffalo, Windhoek, 12-15 September 2016:

Escherichia coli populations sharing and antibioresistance gradient at buffalo/cattle interface in Southern Africa by Mercat M, Ruppe E, Clermont O, de Garine-Wichatitsky M, Miguel E, Valls Fox H, Cornelis D, Andremont A, Denamur E, Caron A However…

…selection may be a potential tool for combatting some diseases

Selective Breeding: the Future of TB Management in African Buffalo?

N le Roex1, CM Berrington1, EG Hoal1, PD van Helden1

1Stellenbosch University, DST/NRF Centre of Excellence for Biomedical Tuberculosis Research/Medical Research Council (MRC) Centre for TB Research, Division of Molecular Biology and Human Genetics, Faculty of Medicine and Health Sciences, Tygerberg, South Africa. The way forward IUCN policies = golden standards:

• Policy on Translocation of Living Organisms: http://intranet.iucn.org/webfiles/doc/SSC/SSCwebsite/Policy_statements/I UCN_Position_Statement_on_Translocation_of_Living_Organisms.pdf

• Guidelines for Re-introductions: http://intranet.iucn.org/webfiles/doc/SSC/SSCwebsite/Policy_statements/R eintroduction_guidelines.pdf

• Prevention of Biodiversity Loss by Alien Invasive Species: http://intranet.iucn.org/webfiles/doc/SSC/SSCwebsite/Policy_statements/I UCN_Guidelines_for_the_Prevention_of_Biodiversity_Loss_caused_by_A lien_Invasive_Species.pdf IUCN policies = golden standards:

 Addis Ababa Principles and Guidelines of the Convention on Biological Diversity, 1992: https://www.cbd.int/sustainable/addis.shtml)

 Policy Statement on Sustainable Use of Wild Living Resources of IUCN, 2000: http://povertyandconservation.info/en/biblio/b1391

 Guiding Principles on Trophy Hunting as a Tool for Creating Conservation Incentives of IUCN SSC, 2012: http://cmsdata.iucn.org/downloads/iucn_ssc_guiding_principles _on_trophy_hunting_ver1_09aug2012.pdf Antelope Specialist Group Groupe de Spécialistes des Antilopes

IUCN SSC ASG Position Statement on the Intentional Genetic Manipulation of Antelopes Ver. 1.0 (15 April 2015) Motion n°16: Management and regulation of selective intensive breeding of large wild mammals for commercial purposes

RECOGNISING that responsible wildlife use is a component of sustainable socio-economic development, especially in dryland ecosystems in developing countries, and that responsible wildlife use and conservation are interdependent; OBSERVING that current uses of indigenous wildlife include intensive selective breeding, associated with deliberate manipulation of the breeding process to produce animals with specific traits, and that this may involve hybridisation across species, subspecies or other recognised evolutionary boundaries; FURTHER OBSERVING that selective breeding is taking place on a large scale in some areas and that some animals may escape or be released into the wild; FURTHER OBSERVING that this selective breeding and intensification of management may ultimately increase domestication of wildlife; CONCERNED that large-scale intensive and selective breeding may have direct and indirect detrimental consequences for biodiversity; FURTHER CONCERNED that these detrimental effects will reduce the ability of eco-tourism and hunting to contribute sustainably to the economy and human well-being; and RECALLING the IUCN Species Survival Commission (SSC) Antelope Specialist Group Position Statement on the Intentional Genetic Manipulation of Antelopes.

The World Conservation Congress, at its session in Hawai‘i, United States of America, 1-10 September 2016: 1. INVITES governments where intensive and selective breeding of wildlife is, or may be, practiced to: a. adopt a risk-averse strategy in permitting establishment or expansion of this practice; b. prohibit intentional hybridisation of large wild mammals across species, subspecies or other recognised evolutionary boundaries; c. prohibit release of selectively bred animals into the wild until the risks are understood and can be managed; d. evaluate the need to develop domestic legal frameworks to regulate, monitor and mitigate impacts associated with these practices; e. require assessments of project-specific and cumulative impacts prior to considering the permitting of such activities; f. develop and implement norms and standards for husbandry practices of intensively bred species; g. strengthen capacity building for monitoring, educating and enforcing; h. establish monitoring systems to document the extent and impact of these activities, and support research to provide more information to anticipate and manage risks; and i. develop and implement certification systems for wildlife operations to ensure transparency so that end users know the origin of the animals they are using and/or buying; and

2. ENCOURAGES the wildlife ranching industry to: a. acknowledge the potential risks associated with these practices; and b. work with government and other stakeholders, as appropriate, to manage and minimise the risks associated with these activities. Nairobi Declaration CONSERVATION OF AQUATIC BIODIVERSITY AND USE OF GENETICALLY IMPROVED AND ALIEN SPECIES FOR AQUACULTURE IN AFRICA NAIROBI, KENYA 20 -23 FEBRUARY 2002 Selective intensive wildlife breeding:

…the conclusion is:

• not to be pro or con

• to adopt best practices

Foot-and-Mouth Disease Apthovirus Cattle and African buffalo Impala (Keet et al 1996; Vosloo, et al. 2009); saiga antelope (Kindyakov et al 1970), Mongolian gazelle (Bolortsetseg et al 2012).

Rinderpest Morbillivirus Cattle, wild ruminants biologically competent but Tragelaphine antelope (Kock, 2006) population insufficient.

PPR VIrus Morbillivirus Goats and sheep Only recorded in captive antelope (e.g. Furley et al. 1987)

Bluetongue Orbivirus Wild ruminants and cattle - mosquitos Disease recorded in pronghorn antelope Antilocapra americana (Thorne et al 1988), serological evidence of absence in saiga antelope in endemic zone (Lundervold et al. 2003)

Rift Valley Fever Phlebovirus Aedine mosquitoes Various antelope (Olive et al 2012; Evans et al 2008)

Rabies Lyssa virus Numerous wild canids, felids and viverids, Greater kudu (Hubschle 1988) spread by browse domestic dogs

Ebola virus Fruit bats (Hypsignathus monstrosus, Epomops Duikers (Rouquet 2005) franqueti, Myonyteris torquata)

Heartwater Rickettsia Certain wild ruminants (e.g. buffalo), chelonians Springbok (Fourie and Horak 1987; Peter et al 1998) and gallinaceous birds, ticks Cowdria ruminantium

Babesiosis Ruminants and ticks Rhipicephalus evertsi Sable antelope (Hove et al 1998)

Theileriosis Ruminants and ticks Rhipicephalus appendiculatus Various associated with translocation (Nijhof et al 2005)

Anthrax Bacillus anthracis Soil saprophyte Large die-offs recorded in impala, kudu, tiang (Grant et al 2002; Lindeque and Turnbull 1994; Gainer 1987

Bovine tuberculosis Mycobacterium Cattle, buffalo Lechwe Kafue (maintenance host), Uganda kob, Indian blackbuck, greater kudu and bushbuck Munyeme et al bovis 2011; Gupta and Singh 1987; Weber at al 1992; Renwick et al 2007; Zieger et al 1998

Pasteurellosis Ruminants latent carriers Saiga antelope (Bekenov 1998)

Corynebacterium pseudotuberculosis Environment Black wildebeest (Connochaetes gnou), Blesbok (Damaliscus dorcas phillipsi), wildebeest (C. taurinus), Red hartebeest (Alcelaphus buselaphus caama) Springbok (Antidorcas marsupialis) (Muller et al. 2011)

Major infectious diseases of antelope (Kock, Chardonnet & Risley, 2016)