Institute of Biodiversity, Animal Health & Comparative Medicine Clare Marsden, Hanny Verberkmoes,...

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Institute of Biodiversity, Animal Health & Comparative Medicine Clare Marsden, Hanny Verberkmoes, Rob Thomas and Barbara Mable Pictus, Pedigrees and MHC: an integrated approach for genetic management of captive African wild dogs

Transcript of Institute of Biodiversity, Animal Health & Comparative Medicine Clare Marsden, Hanny Verberkmoes,...

Institute of Biodiversity, Animal Health & Comparative Medicine

Clare Marsden, Hanny Verberkmoes, Rob Thomas and Barbara Mable

Pictus, Pedigrees and MHC: an integrated approach for genetic management of captive 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

African Wild Dogs

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?

PhD Project: Clare MarsdenComparing variation at adaptive and neutral genes:

• 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

African Wild Dogs

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?

PhD Project: Clare MarsdenComparing variation at adaptive and neutral genes:

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 choiceo 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

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 populationo inbreeding; risk of disease; breeding success

African wild dog EEP

• 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 samplesx Couldn’t assess breeding success in relation to

immune gene variation

• No samples kept from diseased animalsx 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 solveClare and Hanny implemented management plan

across zoos based on genetic variation

Initial Challenges

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

Genetic questions

Pedigree analyses

What is the genetic status of the EEP?

Father Mother

Son Son Daughter Daughter

Father Mother

Son Daughter

Family 2Family 1

Son Daughter Son Daughter

Male

Female

Inbred

KEY

Generation 1

Generation 2

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3070

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913WILDPRET

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695WILD

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Born ~ April 2002. Guessed at parents

Born ~ June 2002. Guessed at parents

No information on parents

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EEP African wild dog pedigree

6009 T6004

3070

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T6001

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T6003

54455444 5442 54405443

30533054 3057

3036 3016

T6008 3124

1984WILDPRET

3083

T6049T6048T6046 T6026

T5927T5926T5925T5924T5923T5922T5921T5920

T6047

T6024

T6021 T6022

1983WILDPRET

913WILDPRET

T5976

T6005

3130WILDTRNS

T6035 T6034T6031

T5976

T6030 T6029T6032T6031 T6027 T6026T6033

3128WILDTRNS

5602

T6013

5454

T6011

1483

5323 5264

1574

896Wild

897WILD

695WILD

51515237

1289

813 812

694WILD

412 416

548

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291UNK

706

1741 1739

885

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984

5193

986

1509 1508

1847

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5606

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T598157045701 5703569956985696 5700

54645459545754565455 5458

1333

766WILD

1702

52835282 5281 52875284 5204 5249

5346 53455341 5342

520652095207

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T5891T5890T5892T5888T5887T5886 T5889

895WILD

1463Zoo

767WILD

5093 5092

1544

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1431

5523 55225520 5521

57265725 5727

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56625617 5663

543554365433 5438 54345432 5437

5117

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1029Wild

5474 56345602560156005599 5603

5215 5493521752185214

T5862

5213

559855975595559455935592550955035479547754765472 5596

1543

898WILD

5429

899WILD

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5104

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5395 5396

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53945393 5398

5107

5355 5353

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T5853

FRIGUNK

T1350 T1353T1352

T6052T6051

T1357

3952PRET

3733PRET

T5985T5984T5983T5982 T5986

UNKHOED

T6053

UNKHOED

UNKHOED

T5991

T6061T6060T6059T6058T6057T6054T6055T6056

T5990T5993T5988T5987T5989

5723 572457205719 5721

UNKHOED

Born ~ April 2002. Guessed at parents

Born ~ June 2002. Guessed at parents

No information on parents

UNK

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Visit www.smartdraw.com or call 1-800-768-3729.

Unequal founder contributions

EEP African wild dog pedigree

ONLY 18/80 wild founders have left descendents.

Very few descendentsVery few descendents

Many descendentsMany descendents

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T6047

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T6021 T6022

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913WILDPRET

T5976

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3130WILDTRNS

T6035 T6034T6031

T5976

T6030 T6029T6032T6031 T6027 T6026T6033

3128WILDTRNS

5602

T6013

5454

T6011

1483

5323 5264

1574

896Wild

897WILD

695WILD

51515237

1289

813 812

694WILD

412 416

548

293UNK

291UNK

706

1741 1739

885

624Z00

984

5193

986

1509 1508

1847

15601753

5024 5180518351845028502750265025

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1565

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UNK

15111637

1304

502250235019 5021

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51435165

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5158

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5577

5452 53675375 53745373

56735672

56075605

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5606

5370536953665376 545354625461 54635460

T598157045701 5703569956985696 5700

54645459545754565455 5458

1333

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1702

52835282 5281 52875284 5204 5249

5346 53455341 5342

520652095207

T5959T5958T5957T5956T5955T5954T5953T5952T5951T5950

T5891T5890T5892T5888T5887T5886 T5889

895WILD

1463Zoo

767WILD

5093 5092

1544

T5960 T5961

1431

5523 55225520 5521

57265725 5727

56415640 563954515525 5450 558855865585 5524

56625617 5663

543554365433 5438 54345432 5437

5117

1046110460104591045810457104561045510454 T5937 T5939T5936T5935T5934T5933T5932T5931T5930T5929T5928 T5938

1029Wild

5474 56345602560156005599 5603

5215 5493521752185214

T5862

5213

559855975595559455935592550955035479547754765472 5596

1543

898WILD

5429

899WILD

T5829T5828T5827T5825T5824T5823T5822T5821T5820T581957095708

55165517 5514 55155512 55135467 5352546554685532 553655355534 5533553755315530552955275518

569556925691

T5830

56905689568856875686568555535552555155505549

57075705 5706

P20793P20791P20789 P20799P20790 P20796

5104

5575 55745572 5573

53285329532653255324 53275101

5395 5396

55795578 5580

53945393 5398

5107

5355 5353

FRIGUNK

T5853

FRIGUNK

T1350 T1353T1352

T6052T6051

T1357

3952PRET

3733PRET

T5985T5984T5983T5982 T5986

UNKHOED

T6053

UNKHOED

UNKHOED

T5991

T6061T6060T6059T6058T6057T6054T6055T6056

T5990T5993T5988T5987T5989

5723 572457205719 5721

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Born ~ April 2002. Guessed at parents

Born ~ June 2002. Guessed at parents

No information on parents

UNK

T6050

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T5839T5838T5837T5836T5835 T5840

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Visit www.smartdraw.com or call 1-800-768-3729.

4 litters from 1 pair4 litters from 1 pair

Bred with 3 malesBred with 3 males

20 offspring20 offspring

1 offspring1 offspring

EEP African wild dog pedigree

Reproductive skew

80% of EEP wild dogs never breed

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

What is the genetic status of the EEP?

Stud book

Namibia, South Africa, Unknown

Mitochondrial DNA•Maternally inherited gene•“Neutral” genetic marker•Can be used to trace back to dead founders

Where do the founders of the EEP originate from in the wild?

Sampling from zoosZoo sampling kits

1. Pre-labelled sampling tubes

2. Sampling and sedation instructions

3. UK import licence

4. Pre-labelled envelopes

Clare

Mar

sden

Gla

sgow

Uni

vers

ity

#5572 ♀Date______

Sampling coordinated through stud book keeper

Sampling from zoosZoo sampling kits

1. Pre-labelled sampling tubes

2. Sampling and sedation instructions

3. UK import licence

4. Pre-labelled envelopes

Clare

Mar

sden

Gla

sgow

Uni

vers

ity

#5572 ♀Date______

Sampling coordinated through stud book keeper

75% response rate

Stud book

Namibia, South Africa, Unknown

Where do the founders of the EEP originate from in the wild?

Namibia

South Africa

EU zoos S. African zoos

Results

1)Founders have a diverse origin

2)Wider than S. Africa & Namibia

3) EU zoos have a more diverse origin than S. African zoos

4) Risk that some imports from wild populations

Expect

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

Genetics: Assessed level of variation at a set 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 of immunity genes (Major Histocompatibility Complex)

Genetics: Assessed level of variation at a set 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?

The EU zoos contain a lot of the diversity found in the wild

Genetics: Assessed level of variation at a set of immunity genes (Major Histocompatability Complex)

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

Positive impact:•New genetic variationo3/11 variants introduced by South African animals•Reduce inbreeding

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

Cautions:•Unknown parentage/ancestryoinbreeding?ooutbreeding depression?•Genetics suggest some sampled from wild

o impacts on wild populationso encourages poaching?

1) What is the genetic status of the EEP?oLoss of variation in the past. Current over and under-representation of some lineages

2) Where did the EEP founders come from?oA 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?oA 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?oIntroduce new genetic variation but risks might outweigh benefits

Genetic questions

• 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

Management implications?

SMALL CHANGES => BIG IMPACT

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

Aalborg zooAmneville zooArtis zooAttica zooBasel zooBelfast zooBoras zooColchester zooDortmund zooDublin zooDuisburg zooDvurkralv zooEbeltoft zooEdinburgh zooEskilstun zooFriguia zoo

Hilvarenbeek zooHowletts wild parkKerkrade zooKolmarden zooLa Palmyr zooLe Pal zooLisieux zooLondon zooLympne wild parkMunich zooPeaugres zooPont-Scorff zooRamat-Gan zooRoma zooRostock zooWest Midlands

Contributing zoosPhD supervisorsBarbara MableDan HaydonLorna Kennedy

Chief collaboratorsHanny VerberkmoesRosie WoodroffeGreg RasmussenSarah CleavelandRob Thomas

PhD fundingNatural Environment Research CouncilRoyal Zoological Society of Scotland