Institute of Biodiversity, Animal Health & Comparative Medicine
Pictus, Pedigrees and MHC: an integrated
approach for genetic management
of captive African wild dogs
Clare Marsden, Hanny Verberkmoes,
Rob Thomas and Barbara Mable
African Wild Dogs
• Lycaon pictus: one of most endangered canids
• Threatened by: habitat loss, persecution, disease
• Last 100 years: 98% reduction in population size;
95% reduction in range
• Status: <5,000 individuals found in small,
fragmented populations
• Captive population in Zoos: 632 (312 in Europe) not
genetically managed
PhD Project: Clare Marsden
Comparing variation at adaptive and neutral genes:
a) Have past bottlenecks reduced genetic
diversity in the wild?
b) How much diversity is maintained in zoos
and can management be improved?
c) Can genetic markers be used to trace
extinction/recolonisation events?
African Wild Dogs
• Lycaon pictus: one of most endangered canids
• Threatened by: habitat loss, persecution, disease
• Last 100 years: 98% reduction in population size;
95% reduction in range
• Status: <5,000 individuals found in small,
fragmented populations
• Captive population in Zoos: 632 (312 in Europe) not
genetically managed
PhD Project: Clare Marsden
Comparing variation at adaptive and neutral genes:
a) Have past bottlenecks reduced genetic
diversity in the wild?
b) How much diversity is maintained in zoos
and can management be improved?
c) Can genetic markers be used to trace
extinction/recolonisation events?
How did this project come about?
Brainstorming Session:
• Sarah Cleaveland (wildlife veterinarian)
• Dan Haydon (theoretical ecologist/epidemiologist)
• Rob Thomas (Conservation and Research Manager,
Royal Zoological Society of Scotland-Edinburgh Zoo)
• me (Evolutionary Geneticist)
• Lorna Kennedy (canid immune gene expert)
Why study genetics of wild and captive populations?
•Severe bottlenecks could have meant reduction in genetic
diversity in wild but hadn’t been studied
•Unknown genetic variation in captive populations
•Viral diseases problematic in wild populations but genetics
unknown
•Social structure means that low success rate of sharing of
animals across zoos but unknown whether due to
relatedness of individuals
How did this project come about?
Brainstorming Session:
• Sarah Cleaveland (wildlife veterinarian)
• Dan Haydon (theoretical ecologist/epidemiologist)
• Rob Thomas (Conservation and Research Manager,
Royal Zoological Society of Scotland-Edinburgh Zoo)
• me (Evolutionary Geneticist)
• Lorna Kennedy (canid immune gene expert)
Innovation
•Most studies only consider variation at DNA markers that have
no effect on fitness (“neutral” markers)
•We also used immune genes (Major Histocompatibility
Complex, MHC) as proxy for adaptive variation
o Immune genes have been implicated in mate choice
o Immune genes might indicate whether wild of captive
populations at risk of disease due to low variation
Why did it work?
Outstanding student!!
Collaborative support from
Studbook keeper
Collaborations with field researchers
African wild dog EEP
EEP (European Endangered Species Programme):
~ 270 African wild dogs
~ 44 zoos holding groups of wild dogs
~ 10-12 successful breeding groups (max capacity)
Research aims:
• Determine the ancestry and level of genetic
diversity conserved in the EEP
• Assess how management could improve the
genetic status of the population
o inbreeding; risk of disease; breeding success
Initial Challenges
• No records on breeding success tied to
samples
• No samples kept from diseased animals
• No pedigree
• Lack of sample sharing between zoos
• Incomplete records of original source of
animals
Initial Challenges
• No records on breeding success tied to
samples
x Couldn’t assess breeding success in relation to
immune gene variation
• No samples kept from diseased animals
x Couldn’t assess risk of disease in relation to
immune gene variation
Initial Challenges
• No pedigree
 Clare and Hanny worked together to produce
pedigree based on studbook records
• Lack of sample sharing between zoos
 Clare and Hanny worked together to establish
system for collecting and sharing samples
• Incomplete records of original source of
animals
 Genetics combined with pedigree to solve
 Clare and Hanny implemented management plan
across zoos based on genetic variation
Genetic questions
1) What is the genetic status of the EEP?
o
Pedigree based on existing records
2) Where did the EEP founders come from?
o
Genetic analysis of neutral markers compared to wild
populations
3) How much genetic diversity is found in the
EEP?
o
Genetic analysis of neutral markers and immune
genes compared to wild populations
4) What impact will recent South African imports
have on the EEP?
o
Genetic analysis of source of new imports
What is the genetic status of
the EEP?
Pedigree analyses
Family 1
Father Mother
Family 2
Father Mother
Generation 1
KEY
Male
Female
Inbred
Generation 2
Son Daughter
Son
Son Daughter
Son Daughter Daughter
Son Daughter
EEP African wild dog pedigree
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EEP African wild dog pedigree
Very few
descendents
Many
descendents
ONLY 18/80
wild founders
have left
descendents.
Unequal founder contributions
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EEP African wild dog pedigree
Bred with 3
males
20 offspring
1 offspring
4 litters
from 1 pair
80% of EEP
wild dogs
never breed
Reproductive skew
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What is the genetic status of
the EEP?
A large amount of genetic variation has been lost:
• Only 18/80 WILD founders have left descendents
• 80% of EEP wild dogs die before breeding.
Over- and under-representation of founder lineages
Wild dog social structure increases genetic risks:
• Reproductive skew (Alpha pair monopolise breeding)
• Large litters
Where do the founders of the EEP
originate from in the wild?
Stud book
Namibia, South Africa, Unknown
Mitochondrial DNA
•Maternally inherited gene
•“Neutral” genetic marker
•Can be used to trace back
to dead founders
Sampling from zoos
Zoo sampling kits
1. Pre-labelled
sampling tubes
#5572 ♀
Date______
2. Sampling and
sedation instructions
3. UK import licence
4. Pre-labelled
envelopes
Sampling coordinated
through stud book keeper
Sampling from zoos
Zoo sampling kits
1. Pre-labelled
sampling tubes
#5572 ♀
Date______
2. Sampling and
75%
response
sedation instructions
rate
3. UK import licence
4. Pre-labelled
envelopes
Sampling coordinated
through stud book keeper
Where do the founders of the EEP
originate from in the wild?
Stud book
Namibia, South Africa, Unknown
Expect
Results
EU zoos
S. African zoos
1) Founders have a diverse origin
2) Wider than S. Africa & Namibia
3) EU zoos have a more diverse Namibia
origin than S. African zoos
4) Risk that some imports from wild
populations
South Africa
How much genetic diversity is found
in the EEP?
Genetics: Assessed level of variation at a set of
immunity genes involved with disease resistance
Major Histocompatibility Complex (MHC)
Variation at these genes is important because it
determines the range of diseases you can fight
How much genetic diversity is found
in the EEP?
Genetics: Assessed
level
of variation
at a set
Genetics:
Assessed
level
of variation
at aofset
immunity
genes
(Major
Histocompatibility
Complex)
of immunity
genes
(Major
Histocompatability Complex)
Southern African wild:
14 genetic variants (alleles)
EU zoos:
11/14 variants
+ 1 variant not found
in the wild
How much genetic diversity is found
in the EEP?
Genetics: Assessed
level
of variation
at a set
Genetics:
Assessed
level
of variation
at aofset
immunity
genes
(Major
Histocompatability
Complex)
of immunity
genes
(Major
Histocompatability Complex)
The EU zoos contain
Southern African wild:
a lot of the diversity
14 genetic variants (alleles)
found in the wild
EU zoos:
11/14 variants
+ 1 variant not found
in the wild
How much genetic diversity is found in the
EEP?
How much genetic diversity is found in the
EEP?
High diversity but concentration of alleles
in some parts of pedigree suggests
inbreeding and unequal reproduction
How much genetic diversity is found in the
EEP?
How much genetic diversity is found in the
EEP?
Bias in MHC alleles in some families could
suggest selection (diseases?) but sample
sizes small and no disease records
What impact will recent South African
imports have on the EEP?
EU zoos have imported ~ 20 African wild dogs from
South African captive facilities in the last 10 years
Positive impact:
Cautions:
• New genetic variation
•
o 3/11 variants introduced
by South African animals
• Reduce inbreeding
•
Unknown parentage/ancestry
o inbreeding?
o outbreeding depression?
Genetics suggest some
sampled from wild
o impacts on wild populations
o encourages poaching?
Genetic questions
1) What is the genetic status of the EEP?
o Loss of variation in the past. Current over and underrepresentation of some lineages
2) Where did the EEP founders come from?
o A range of countries in Southern Africa, not just Namibia
& S. Africa. EEP is more diverse than S. African zoos
3) How much genetic diversity is found in the EEP?
o A large proportion of the diversity found in wild
populations in Southern Africa but could be managed
better
4) What impact will recent South African imports
have on the EEP?
o Introduce new genetic variation but risks might outweigh
benefits
Management implications?
SMALL CHANGES => BIG IMPACT
• Try to limit reproduction to 2-3 litters/pair
and 2-3 siblings per family
• Form breeding groups with animals from
different lineages; bias under-represented
lineages
• Integrate S. African imports into the EEP
Lessons Learned
•
Value of coordinating samples, stud book records,
behavioural data and health records
Benefits of collaborative approach and networking
Value of genetics for “forensics” of imports
Genetics demonstrated more variation than expected
based on studbook records
5 years on, management plan resulted in births with more
genetic variation in the EEP
Interest in genetic management from other zoo networks
(USA, Australia)
•
•
•
•
•
Remaining Challenges
•
•
•
Continuity and implementation
Sample and data storage
Biology of species/quality of zoo facilities
Acknowledgments
Contributing zoos
Aalborg zoo
Amneville zoo
Artis zoo
Attica zoo
Basel zoo
Belfast zoo
Boras zoo
Colchester zoo
Dortmund zoo
Dublin zoo
Duisburg zoo
Dvurkralv zoo
Ebeltoft zoo
Edinburgh zoo
Eskilstun zoo
Friguia zoo
Hilvarenbeek zoo
Howletts wild park
Kerkrade zoo
Kolmarden zoo
La Palmyr zoo
Le Pal zoo
Lisieux zoo
London zoo
Lympne wild park
Munich zoo
Peaugres zoo
Pont-Scorff zoo
Ramat-Gan zoo
Roma zoo
Rostock zoo
West Midlands
PhD supervisors
Barbara Mable
Dan Haydon
Lorna Kennedy
Chief collaborators
Hanny Verberkmoes
Rosie Woodroffe
Greg Rasmussen
Sarah Cleaveland
Rob Thomas
PhD funding
Natural Environment
Research Council
Royal Zoological
Society of Scotland