The genetic footprint of Alpine ibex reintroductions and implications

Institut für Evolutionsbiologie und Umweltwissenschaften
The genetic footprint
of Alpine ibex reintroductions
and implications for population management
WISO 2012, Christine Grossen
Iris Biebach
Lukas Keller
Alpine ibex ~1820
Gran Paradiso!
1906
Wildpark PP!
Wildpark IH!
Gran Paradiso!
reintroductions after 1911
Wildpark PP!
Brienzer
Rothorn!
Wildpark IH!
Piz
Albris!
Mont
Pleureur!
Gran Paradiso!
reintroductions after 1911
Wildpark PP!
Brienzer
Rothorn!
Wildpark IH!
Piz
Albris!
Mont
Pleureur!
Gran Paradiso!
Fast recovery of Alpine ibex populations
(Maudet et al. 2002, Molecular Ecology)
Fast recovery of Alpine ibex populations
Small populations:
Decrease of genetic diversity
Increase of inbreeding
(Maudet et al. 2002, Molecular Ecology)
Genetic drift: decrease of genetic diversity
Random change in frequency of gene variants (alleles) over
generations
Genetic drift: decrease of genetic diversity
Random change in frequency of gene variants (alleles) over
generations
Genetic drift is strongest
in small populations
Inbreeding = breeding between related individuals
Inbreeding: reduced survival and reproduction
(Keller et al. 1998, Evolution)
Inbreeding: reduced survival and reproduction
Inbreeding depression
(Keller et al. 1998, Evolution)
Effects of reintroductions on genetic
variability of Alpine ibex
Do we see genetic drift?
Are Alpine ibex populations inbred?
1262 samples
42 populations (N=17-61)
37 neutral microsatellites
5 MHC-linked microsatellites
Switzerland
Austria
Italy
Sampling
Blood from anesthetized animals
Tissue from hunted animals
Biopsy samples (darts) from
colonies with no or low hunting pressure
Sampling
Blood from anesthetized animals
Tissue from hunted animals
Biopsy samples (darts) from
colonies with no or low hunting pressure
Sampling
Blood from anesthetized animals
Molecular genotyping
Tissue from hunted animals
Biopsy samples (darts) from
colonies with no or low hunting pressure
AL
ALP1
P
G 2
R
PC S
SGG
G VBB
G P.O N
P
Ad .Va rco
ul lsa
a. v
Vi
a
Al Alb l
et ris
Al .Bi
ps et
Bi A tein
re r
Br .O olla
.R es
ot ch
C
C a hor
ap la n
eM nd
C oi a
a n
C tog e
C hu ne
ra r
D p.Ffirst
D ent lem
ue s.
ss Mi
.T di
Fe Fa oed
rg lkn
e. is
S
Fe eet
Fl rr
ue et
Fl bri
Fo ue g
os ela
t
G
G a ock
or st
G ne ern
r.H rg
G oe rat
r r
H .Lo ner
oc hn
hw e
Ju an r
Ju .No g
. rd
Ju Sue
st d
M ista
M ac l
M eso un
is c
c c
M hab o
uv e
N er l
uf an
e
O Ob ne
be e n
Pi rb ra
er au lp
r.G e
um st
P m
Pl ilat
R eu us
h
R ein reu
Sc oth w r
hw .W ald
m eis
oe s
n
Ta ch
Te T nay
rz as
a. na
U Ses
Va mb v
l.B ra
e il
W Ver ver
e e
W iss ina
ei ho
W ss rn
e m
W tter ies
itt ho
en rn
be
rg
NumberNum
of alleles
Genetic diversity in Alpine ibex is low
Low potential to adapt to changing environments
Domestic goat
breeds
5
4
3
2
1
Alpine ibex
Gran Paradiso
Alpine ibex
Switzerland
Genetic structure of Swiss ibex
Switzerland
Austria
Italy
(Biebach and Keller 2009, Molecular Ecology)
Reintroductions shaped the genetic diversity
Albris
Brienzer
Rothorn
Gran Paradiso
Zoos
Mont
Pleureur
Genetic diversity
Reintroductions shaped the genetic diversity
p=0.001, coeff: 0.29
p=0.003, coeff: 0.57
Number of founders
Source diversity
(scaled)
(scaled)
Both number of founders and number of source populations
positively affected genetic diversity
(Biebach and Keller 2012, Biological Conservation)
Relationship between neutral and
selected diversity?
http://www.tunturisusi.com/saarikettu.html
Low diversity at the MHC
(important for immune response)
Ovis aries
Capra
hircus
Ovis
aries
Domestic
sheep
Rupicapra
rupicapra
Capra
hircus
Domestic
goat
Rupicapra pyrenaica
rupicapra
Ovis canadensis
Rupicapra
pyrenaica
Ovis dalli
Ovis canadensis
Capra pyrenaica
Ovis dalli
Hemitragus
Caprajemlahicus
pyrenaica
Capra
nubiana
Hemitragus
jemlahicus
Bosnubiana
taurus
Capra
2 alleles
Capra
ibex
Bos taurus
Ovibos Capra
moschatus
ibex
Oreamnos
Ovibosamericanus
moschatus
Oreamnos americanus 0
50
0
50
100
Number of Alleles
100
Number of Alleles
150
150
al
Ale ris
t.B
i
Alp et
ste
in
Ar
o
Bir
e.O lla
Br. esch
Ro
tho
r
Ca n
l
Ca anda
peM
o
Ch ine
ur
Cr first
ap.
De Flem
nts
.Mi
di
Fer
re
Flu t
ebr
ig
Flu
e
Fo ela
o
Go stock
rne
Gr rgrat
.Ho
er
Gr ner
.Lo
h
Ho ner
chw
an
Ju.N g
ord
Ju.S
ue
Jus d
tist
al
Ma
Mis cun
cha
b
Mu el
ver
an
N
Ob
ufe
erb
n
aue en
Pie stock
rr.G
um
m
Pila
t
Ple us
ur
Rh eur
ein
Ro wald
th
Sch .Wei
wm ss
oe
nch
Tan
a
Um y
b
Val rail
.B
We ever
issh
We orn
is
We smie
s
tte
rho
W
itte rn
nbe
rg
Alb
.Vi
Ad
High extent of inbreeding
0.30
0.25
0.20
0.15
0.10
0.05
0.00
(Biebach and Keller 2010, Conservation Genetics)
al
Ale ris
t.B
i
Alp et
ste
in
Ar
o
Bir
e.O lla
Br. esch
Ro
tho
r
Ca n
l
Ca anda
peM
o
Ch ine
ur
Cr first
ap.
De Flem
nts
.Mi
di
Fer
re
Flu t
ebr
ig
Flu
e
Fo ela
o
Go stock
rne
Gr rgrat
.Ho
er
Gr ner
.Lo
h
Ho ner
chw
an
Ju.N g
ord
Ju.S
ue
Jus d
tist
al
Ma
Mis cun
cha
b
Mu el
ver
an
N
Ob
ufe
erb
n
aue en
Pie stock
rr.G
um
m
Pila
t
Ple us
ur
Rh eur
ein
Ro wald
th
Sch .Wei
wm ss
oe
nch
Tan
a
Um y
b
Val rail
.B
We ever
issh
We orn
is
We smie
s
tte
rho
W
itte rn
nbe
rg
Alb
.Vi
Ad
High extent of inbreeding
Average total inbreeding = 0.125
0.30
(mating between half siblings!)
0.25
0.20
0.15
0.10
0.05
0.00
(Biebach and Keller 2010, Conservation Genetics)
Population size alone does not explain
observed level of inbreeding
0.14
Observed
inbreeding
split inbreeding
0.12
0.1
0.08
0.06
0.04
0.02
0
0.00
0.02
0.04
0.06
0.08
0.10
0.12
hm(fluctuating)
Fst
Inbreeding explained by
population size
(Biebach and Keller 2010, Conservation Genetics)
140
120
100
80
60
40
20
0
vb
jn
ar
rw
um
mu
ma
fu
js
hw
cf
ca
rh
ju
mi
wh
ob
dm
pi
bo
fo
ty
Number
individuals
number of
of individuals
Not every released individual is a founder
Population
individuals released
genetic founders
(Biebach and Keller 2012, Biological Conservation)
Only a few males reproduce
(Willisch et al. 2012)
140
120
100
80
60
40
20
annuli.mm per year
horn growth
Genetic effects on horn growth?
2
4
6
8
10
12
14
age
annuli.age
No effect of inbreeding on horn growth
Significant effect of genotype at MHC (immune gene) on
horn growth of male ibex older than ~6 years.
(Anina Knauer)
Population size
Population size over time
Time since first reintroduction
Density dependence
Inbred populations react stronger to
changes in density
Inbreeding
(Claudio Bozzuto)
Inbreeding in variable environments
Inbreeding in variable environments
(Keller et al. 2002,
Evolution)
Inbreeding in variable environments
(Keller et al. 2002,
Evolution)
Inbreeding in variable environments
Extent of inbreeding depression
depends on environmental
conditions
(Keller et al. 2002,
Evolution)
Effective number of alleles
ul
a.
V
Al Alb ial
e r
Al t.B is
ps ie
t
Artein
Bi B ol
r i l
Br e.Onnt a
.R es al
o
Br thoch
u
C Ca nn rn
ap la is
e n t
C Mo da
a i
C togne
C hu n
r
D ap rfir e
D en .Fle st
ue ts m
ss .M
. id
Fe F Toe i
rg alk d
e. ni
Se s
Fl Fer et
u re
F eb t
Fo lue rig
os el
G Ga toca
o
G rn ste k
r.H er rn
G oe gra
H r.Lo rne t
oc h r
h n
Ju wa er
Ju .Nong
.S rd
J
Lo us ue
et tis d
sc ta
h l
M Ma en
M es cu
M isc occn
ue ha o
ns be
M ti l
u g
N ver er
u a
O O fen n
be be en
rb ra
Pi P au lp
er an es
r.G ix t
u e
P mr
Pl ila m
eu tu
R R reus
he a r
in wy
w
ScRot Ro aldl
hwh.W bi
m e ei
oe iss
T nc
Te Tanah
rz as y
a. n
US a
Va m esv
l.Bbra
ev il
e
W Ve Va r
l
W eissrein s
W eis ho a
e s r
W tte mien
itt rh s
en or
be n
G G Zinrg
P. P. a
R O l
G he rco
P. m
Va es
l
AL sav
ALP1
G P2
R
PC S
SGG
VB B
N
Ad
Summary
Strong genetic footprint of the reintroduction history in Swiss
Alpine ibex populations
Genetic variation (also at the MHC) is low and inbreeding is
high
3
2
1
No effect of inbreeding but significant effect of genotype at
MHC on horn growth
Populations with particularly high inbreeding show stronger
density dependence
What do we learn for future translocations?
Many individuals should be released (better 100 than 10)
Translocate individuals from several different source populations
Take into account genetic relatedness among founder populations
Thank you!
Lukas Keller
Iris Biebach
Christian Willisch
Anina Knauer
Claudio Bozzuto
Game keepers and
Jagdinspektorate
Achaz von Hardenberg
Flurin Filli
Heinz Maag