Genetic Rewilding :how connectivity can rescue small populations

Sarah W. FitzpatrickKellogg Biological StationDepartment of Integrative BiologyMichigan State University

• geographic distribution

• range size

• population dynamics

• evolutionary trajectory of species

Why does connectivity matter?

Charley Harper

Connectivity shapes biodiversity patterns through gene flow

gene flow = genetic connectivity

Connectivity shapes biodiversity patterns through gene flow

Dispersal patterns of ancient humans out of Africa

Why does gene flow matter for conservation?

- Gene flow can decrease fitness

- Gene flow can increase fitness

Why does gene flow matter for conservation?

fitness = a measure of reproductive success

- Gene flow can decrease fitness

- Gene flow can increase fitness

Why does gene flow matter for conservation?

- Gene flow can decrease fitness

- Gene flow can increase fitness

high lowfitness

gene flow

Why does gene flow matter for conservation?

- Gene flow can decrease fitness

- Gene flow can increase fitness

high lowfitness

gene flow

Why does gene flow matter for conservation?

- Gene flow can decrease fitness

- Gene flow can increase fitness

high lowfitness

Why does gene flow matter for conservation?

- Gene flow can decrease fitness

- Gene flow can increase fitness

Why does gene flow matter for conservation?

- Gene flow can decrease fitness

- Gene flow can increase fitness

fitness

gene flow

high low

Why does gene flow matter for conservation?

- Gene flow can decrease fitness

- Gene flow can increase fitness

fitnesshigh low

Why does gene flow matter for conservation?

- Gene flow can decrease fitness

- Gene flow can increase fitness

fitnesshigh low

• increase genetic variation• facilitate local adaptation• rescue small populations

Why does gene flow matter for conservation?

• risks of inbreeding depression

• reduced adaptive potential

• little buffer to withstand environmental disturbance

Cheetah Scrub mint Bighorn sheepDevil’s hole pupfish

Problems with small populations

historical range (green)current range (red)

habitat loss

severe population declines

signs of inbreeding depression• 49 % of male panther’s suffered

from cryptorchidism (undescended testes)

• kinked tail phenotype

By 1994, only 20-30 adult panthers remained in Florida

Inbreeding exposes deleterious alleles

historical range (green)current range (red)

8 female panthers from Texas introduced to Florida

1995

Johnson et al 2010 Science

genetic diversity increasedGreat.What about population size?

Johnson et al 2010 Science

population size increased too!genetic diversity increased

Johnson et al 2010 Science

population size increasedgenetic diversity increased

Genetic rescue: increase in population growth by more than the demographic contribution of immigrants

How does connectivity, or lack thereof, affect evolution and persistence

of small populations?

How does connectivity, or lack thereof, affect evolution and persistence

of small populations?

How does connectivity, or lack thereof, affect evolution and persistence

of small populations?

1. Effects of a rapidly changing landscape

on natural patterns of connectivity

in a threatened fish

Rest of talk

1. Effects of a rapidly changing landscape

on natural patterns of connectivity

in a threatened fish

Rest of talk

2. Genetic rescue in guppies:

a model system for evolution,

conservation, and education

1. Effects of a rapidly changing landscape

on natural patterns of connectivity

in a threatened fish

Rest of talk

2. Genetic rescue in guppies:

a model system for evolution,

conservation, and education

Arkansas darter (Etheostoma cragini)

Characterizing gene flow in an imperiled species

Arkansas darter (Etheostoma cragini)

Characterizing gene flow in an imperiled species

Big Sandy Creeklives up to its name

COLORADO

FTN02

FTN03

BSY04

RCR05

RCR07

AFT09

AFT10

AFT11

AFT12AFT13

Arkansas River

Fountain Creek

Rush Creek

Big Sandy Creek

PerennialIntermittent

0 5 10 20 30 40 miles

RCR06

HGP08

FTN01

perennialintermittent

more than 5 darters

5 darters or less

2010 Arkansas darter sampling

COLORADO

FTN02

FTN03

BSY04

RCR05

RCR07

AFT09

AFT10

AFT11

AFT12AFT13

Arkansas River

Fountain Creek

Rush Creek

Big Sandy Creek

PerennialIntermittent

0 5 10 20 30 40 miles

RCR06

HGP08

FTN01

perennialintermittent

Totals• 12 sites

• 614 darterssampled

• genotyped at 10 microsatellite loci

2010 Arkansas darter sampling

more than 5 darters

5 darters or less

COLORADO

FTN02

FTN03

BSY04

RCR05

RCR07

AFT09

AFT10

AFT11

AFT12AFT13

Arkansas River

Fountain Creek

Rush Creek

Big Sandy Creek

PerennialIntermittent

0 5 10 20 30 40 miles

RCR06

HGP08

FTN01

perennialintermittent

Totals• 12 sites

• 614 darterssampled

• genotyped at 10 microsatellite loci

2010 Arkansas darter sampling

more than 5 darters

5 darters or less

FTN02

FTN03

BSY04

RCR05

RCR07

AFT09

AFT10

AFT11

AFT12AFT13

Arkansas River

Fountain Creek

Rush Creek

Big Sandy Creek

PerennialIntermittent

0 5 10 20 30 40 miles

RCR06

HGP08

FTN01

Fitzpatrick, S.W., H. Crockett, W.C. Funk (2014) Conservation Genetics.

Low genetic diversity within sites & connectivity among sites

Fitzpatrick, S.W., H. Crockett, W.C. Funk (2014) Conservation Genetics.

How does the landscape affect connectivity?

5.5 6.0 6.5 7.0 7.5 8.0 8.5

0.0

0.1

0.2

0.3

log Stream Distance

Mantel’s r: 0.656p-value: 0.001

Fst

overall distance

stream distance (km)

gene

tic d

ista

nce

Fitzpatrick, S.W., H. Crockett, W.C. Funk (2014) Conservation Genetics.

Stream distance lowers connectivity

5.5 6.0 6.5 7.0 7.5 8.0 8.5

0.0

0.1

0.2

0.3

log Stream Distance

Mantel’s r: 0.656p-value: 0.001

Fst

overall distance

stream distance (km)

gene

tic d

ista

nce

Fitzpatrick, S.W., H. Crockett, W.C. Funk (2014) Conservation Genetics.

Intermittency acts as a barrier to gene flow

5.5 6.0 6.5 7.0 7.5 8.0 8.5

0.0

0.1

0.2

0.3

log Stream Distance

Mantel’s r: 0.656p-value: 0.001

Fst

overall distance % intermittency

log Stream Distance % intermittencyFs

tstream distance (km)

gene

tic d

ista

nce

% intermittencyge

netic

dis

tanc

e

Fitzpatrick, S.W., H. Crockett, W.C. Funk (2014) Conservation Genetics.

Intermittency acts as a barrier to gene flow

5.5 6.0 6.5 7.0 7.5 8.0 8.5

0.0

0.1

0.2

0.3

log Stream Distance

Mantel’s r: 0.656p-value: 0.001

Fst

overall distance % intermittency

log Stream Distance % intermittency

Fst

Fst

photo credit: Kurt Fausch

FTN02

FTN03

BSY04

RCR05

RCR07

AFT09

AFT10

AFT11

AFT12AFT13

Arkansas River

Fountain Creek

Rush Creek

Big Sandy Creek

PerennialIntermittent

0 5 10 20 30 40 miles

RCR06

HGP08

FTN01

How should isolated, threatened populations be managed?

1. Effects of a rapidly changing landscape

on natural patterns of connectivity

in a threatened fish

Rest of talk

2. Genetic rescue in guppies:

a model system for evolution,

conservation, and education

“The island of Trinidad formed the natural laboratory for the present work”

- Caryl Haskins

Venezuela

Venezuela

“The island of Trinidad formed the natural laboratory for the present work”

- Caryl Haskins

Venezuela

“The island of Trinidad formed the natural laboratory for the present work”

- Caryl Haskins

Low Mid High

LowHigh

Low predation

• small headwater populations

• isolated from gene flow

• good proxy for threatened species

low predation

high predation

Ne = 3

Ne = 2

Ne = 928

12 microsatellite lociInitial divergence between native and source populations

Ne = 3

Ne = 2

Ne = 928

12 microsatellite loci

male body shape & size traits

Initial divergence between native and source populations

- Gene flow can decrease fitness

- Gene flow can increase fitness

2 streams29 months9,590 guppies25,581 captures

photo: Andrés Lopez-Sepulcre

“Counting fish is like counting trees…except they are invisible and they keep moving.”-John Shepard

catching guppies

lab processingcatching guppies

lab processingcatching guppies

release!

Increase in migration rate

Increase in migration rate and genetic diversity

0

200

400

600

800

1000

1200

2009

upstreamintroduction

2010 2011

mark-recapture

begins

num

ber o

f cap

ture

s CaigualTaylor

Changes in population size following gene flow

0

200

400

600

800

1000

1200

2009

upstreamintroduction

2010 2011

mark-recapture

begins

num

ber o

f cap

ture

sChanges in population size following gene flow

CaigualTaylor

0

200

400

600

800

1000

1200

2009

upstreamintroduction

2010 2011

mark-recapture

begins

num

ber o

f cap

ture

sChanges in population size following gene flow

CaigualTaylor

0

200

400

600

800

1000

1200

2009

upstreamintroduction

2010 2011

mark-recapture

begins

num

ber o

f cap

ture

sChanges in population size following gene flow

CaigualTaylor

end of wet season 1

end of wet season 2

end of wet season 3

0

200

400

600

800

1000

1200

2009

upstreamintroduction

2010 2011

mark-recapture

begins

num

ber o

f cap

ture

s CaigualTaylor

Genetic rescue: increase in population growth by more than the demographic contribution of immigrants

Fitzpatrick et al. (2016) Evolutionary Applications

Estimating individual fitness with wild pedigrees

Lifetime reproductive success = 4

Estimating individual fitness with wild pedigrees

Lifetime reproductive success = 4

fitness = a measure of reproductive success

Hybrid index = 0“pure native”

Estimating individual fitness with wild pedigrees

Lifetime reproductive success = 4

Hybrids have highest individual fitness

native immigrant

fitne

ss

Hybrids have highest individual fitness

native immigrant

fitne

ss

TAKE HOME: gene flow from a divergent source caused genetic rescue in two wild populations of guppies

• introduced population came from the same drainage

Important considerations

reduced chance ofnegative impacts of gene flow!

Weese et al. (2011) Evolutionary Applications

Important considerations

• environment matters

What can we learn from the guppy?

(not to scale)

When will genetic rescue be useful in conservation?

Ozark Hellbender Channel Island fox Blue shiner

FL Scrub Jay

…that can be manipulated for managing microevolution in the face of climate change and

altered patterns of connectivity.

Gene flow plays an important, evolutionary role…

Thank you!

Funding American Society of Icthyology

& HerpetologyAmerican Society of NaturalistsColorado State UniversityKellogg Biological StationMichigan State UniversityNational Science FoundationNational GeographicSociety for the Study of

Evolution

CollaboratorsLisa AngeloniLarissa BaileyHarry CrockettChris FunkCameron GhalamborCorey HandelsmanJohn KronenbergerAndrés Lopez-SepulcreDavid ReznickJulian Torres-Dowdall

Funk-Hoke LabUndergraduate assistants

Jill GerberichBrie NixonSamantha Coisman

Questions?

photo credit: John Fitzpatrick

Venezuela

http://www.sii‐inc.org/guppy‐trailer‐3/