“Why some species disappear and other expand? The example of the minks and the European otter ”

“Why some species disappear and

other expand? The example of the

minks and the European otter ”

MICHAUX Johan

Conservation Genetics Laboratory, University of Liège, Belgium

It is estimated that the current species extinction rate is between 1,000 and 10,000 times higher than it would

Millions d’années 600 400 200 N o m b re d e f am ill e s 2 0 0 4 0 0 6 0 0 500 300 Paléozoic Mésozoïc Cénozoïc

Species having the less chances to survive to

global changes

• Specialist (diet, habitat..) species;

• Species with narrow habitat requirements;

• Species of large size, especially predators, and/or those intolerant of humans or vice versa;

• Species having limited numbers of offspring per

breeding, long gestation periods, or those requiring extensive parental care;

• Species who are overhunted; • Species with low effective sizes;

• Species with a low genetic diversity

:

• Higher risk of inbreeding depression;

• Higher sensibility to diseases;

• Lower adaptive potentialities;

• Fecondity problems;

Some exceptions…

• Invasive species : considered as coming from a

low number of founders, with low genetic

diversity;

American mink (Neovison vison)

Canadian beaver (Castor canadensis) Invasive Asian clam (Corbicula fluminea)

- Recovery of some nearly extinct species

from a low number of individuals (ex.

Pacific Sea Elephant; European bison,

Prewalski horse etc)

Questions :

-What is really the importance of genetic diversity for the survival of a species?

- Can species survive with a low genetic diversity for a long time?

- How genetic diversity have to be considered for conservation managements, particularly for

Case studies : 3 close mustelid species

The European Otter (Lutra

Lutra)

The American mink (Neovison

Vison)

The European mink (Mustela

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The European mink (Mustela lutreola)

- Semi aquatic Mustelid; - Medium size species; - European species; - Critically endangered (IUCN red list).

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The American mink (Neovison vison)

Semi aquatic Mustelid; Native to North America;

Introduced into Europe in 20th _{century (fur farms);}

 Feral populations;

 Exotic invasive species;

The Eurasian otter (Lutra lutra)

Semi aquatic Mustelid; Native to Europe;

Nearly extirpated in 20th _{century in Europe;}

 Legal protection (France : from 1972)  Natural recolonization (>1980)

SFEPM

• Specialist (diet, habitat..) species : YES!

Semi aquatic species adapted to water ecosystems with specialised diet (fishes, amphibians..); • _{Species with narrow habitat requirements : YES!}

Aquatic habitat requirements ;

• Species of large size, especially predators, and/or those intolerant of humans or vice versa :

YES!

Medium size carnivores but considered as competitors for humans since centuries;

• Species having limited numbers of offspring per breeding, long gestation periods, or those requiring extensive parental care : YES

Offsprings : otter (1 to 3), European mink (2 to 7), American mink (2 to 7); • Species who are overhunted : YES

Yes, species that have been overhunted since the beginning of the 20th _century;

• Species with low population sizes : Yes and No

American mink : invasive species with high population sizes; Otter : previously, important population sizes; today : low population sizes; European mink : very low population size;

Are they good candidates for extinction?

Similar biological traits and extinction risks However…

• One is threatened;

• One is stable (North America ) or invasive (Europe);

• One is recovering after almost extinction.

Material

- Tissues collected on road kill animals; - Non invasive material (faeces, hairs..).

Methods

- Use of genetic markers (mitochondrial DNA and microsatellites); - Next Generation Sequencing approach (diet study);

- Phylogenetic analyses; - F statistic analyses;

- Clustering analyses (STRUCTURE software etc).

Study of the population genetics and genetic

diversity of these three species

Michaux et al., Biol. Conservation, 2004, Molecular Ecology, 2005, Cabria et al., BMC Genetics, 2015.

Phylogenetic reconstructions based on mitochondrial DNA markers

Michaux et al., Biol. Conservation, 2004, Molecular Ecology, 2005, Cabria et al., 2015.

1 single haplotype for all Western European

Inbreeding coefficient (Fis)

-_{Fis significatively positive for the Western European}

population : Lack of Heterozygotes and high inbreeding

depression risks.

Analyses based on the program Bottleneck (Cornuet & Luikart, 1996)

- _{Non significative for North East Europe;}

F-statistic Results

American mink (Neovison vison)

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4 Genetic clusters

No geographic patterns

Admixture within some individuals Links with breeding farms??

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American mink: clustering

farms samples included (F16, F24, F64))

F16 Charente F24 Dordogne F64 Pyr-Atl

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American mink: diversity indexes

Ar Fis [CI] Cluster1 3.34 0.0505 [-0.02 ; 0.12] Cluster2 2.97 0.4099 [0.17 ; 0.55] Cluster3 3.35 0.1435 [0.06 ; 0.22] Cluster4 3.72 0.2124 [0.05 ;- 0.36] Charente (F16) 3.52 -0.0054 [-0.11 ; 0.08] Dordogne (F24) 3.26 -0.1672 [-0.35 ; -0.06] Pyr-Atlantiques (F64) 4.03 0.2055 [0.01 ; 0.33] fa rm s

Allelic richness Inbreeding index

cluster/farm cl 1 cl 2 cl 3 cl 4 F16 F24 F64 cluster 1 - - - -cluster 2 0.1254 - - - -cluster 3 0.0730 0.1417 - - - - -cluster 4 0.1391 0.1196 0.1641 - - - -F16 0.0956 0.1117 0.0504 0.1305 - - -F24 0.1204 0.1349 0.0392 0.1594 0.019 - -F64 0.1374 0.1077 0.1343 0.042 0.0814 0.0963

-American mink : Evidence of gene flow

between populations

Fixation index (Fst)

from 0 to 1 (0 = complete sharing of genetic material ; 1 = no sharing)

Colonisation of American mink in South

Western France

European otter (Lutra lutra)

5 genetic clusters 5 refugia ?

Pigneur et al. in prep.

Eurasian otter : genetic diversity

within studied populations

Inbreeding coefficient (Fis) and mean allelic richness (Ar) with Confidence Intervals (CI) Ho : observed heterozygosity / He : expected heterozygosity

Pigneur et al. in prep.

Cluster F_IS [CI] Ar [CI] Ho / He Pyrenees 0.0451 [-0.05-0.1385] 3.54 [1.95-4.88] 0.52 / 0.55

Massif Central 0.0500 [0.1375-0.2111] 3.70 [2.65-4.85] 0.59 / 0.62

Limousin -0.0683 [-0.1784-0.1324] 3.01 [1.49-4.42] 0.54 / 0.5

Britany 0.0600 [-0.0098-0.1324] 2.47 [1.97-4.25] 0.45 / 0.48

Eurasian otter : gene flow between populations

Pyrenees Massif Central Limousin Brittany Atlantic Pyrenees 0.1658 0.1951 0.3009 0.1818 Massif Central 0.1661 0.1233 0.2327 0.1408 Limousin 0.1827 0.0982 0.2318 0.1940 Brittany 0.2913 0.2217 0.1828 0.2335 Atlantic 0.1501 0.1455 0.1439 0.1821 F_ST D Jo st Fixation index

A question of history

• European mink : Western Europe : possible past introduction from a low number of individuals, no links with other populations;

• American mink : invasive species, with different inoculations and mixing, increasing genetic

diversity;

• European otter : survival in different refuges

during the 20 th century, recent mixing of these populations, increasing genetic diversity.

Impact on the immune system

Study of the Major Histocompatibility genes

MHC molecules

Antigene

Lymphocyte T

MHC Antigene

Extremely low genetic diversity on the MHC genes for the European mink (Max 2 different alleles)

Extreme sensibility to pathogens

• Aleoutian virus (imported from American

minks);

• Distemper virus : recent eradication of

important European mink populations in

Spain.

Presently, the most important impact

concerns the European mink.

A question of effective population sizes and

time

• Species can recover from a limited number of individuals;

• But their global genetic diversities can be very low : higher risks for diseases or maladaptation to environmental changes;

• The only solution to recover enough genetic diversity : to maintain important effective size during a long time enough, to re-create genetic diversity (Thevenon et al. 2002).

If not enough time : high risks of extinction

A species will not be saved until it re-create enough genetic diversity.

e.g. the case of the European bison: - founders : n= 13;

- now, more than 1700;

But recently, appearance of a new disease (balanoposthite) contaminating males of different populations.

In general, the success of conservation projects from a small number of number is very weak.

Following Beck et al. (1994), the success rate of mammal reintroduction was of 11%.

Towards an extinction vortex

Decrease of population densities lead to : • Hybridization processes (e.g. European

mink/European polecat;

• Higher Inbreeding depression risks; • Higher individual movements :

- increase of road kill risks;

- increase of destruction by predators (foxes, dogs..); - increase of competition with American mink;

The best solution to conserve

species is to manage them when

they still have abundant

populations with a good genetic

diversity and to conserve their

Acknowledgements

• Lise Marie Pigneur for her work on the American mink and European otter; • All sample collectors (PNA-Loutre, Réseau de Collecte vison d’Amérique,

etc). • GREGE;

• French National Plan for the conservation of the European otter; • Conservatoire Espaces Naturels Midi-Pyrénées;