Ecological and Evolutionary Physiology of Sexual ... John Alder - Ecological and...Department of Ecology, Evolution, and Natural Resources . ... 5 A. Log Male Density (n/hectare) Log

Ecological and Evolutionary Physiology of Sexual Dimorphism in Body Size in Eastern Fence Lizards

(Sceloporus undulatus)

Henry John-Alder

Department of Ecology, Evolution, and Natural Resources

School of Environmental and Biological Sciences

Morphology, Performance, and Fitness

-S. Arnold, Am. Zool. , 1983

Ultimate goal of integrative biology is to reveal the adaptive significance of phenotypic traits through their functional linkages

to fitness.

Morphology, Performance, and Fitness

-S. Arnold, Am. Zool. , 1983

“PERFORMANCE” is what animals do in nature. It is about all that

they do to work and succeed.

Statistical Relationships

“P” = phenotypic covariance

Endocrine Integration

H = hormonal pleiotropy

H14

H4K

H

H

H

H

H

H

H H

Hormones are biological agents of phenotypic covariance.

Hormones can regulate performance.

“… endocrine system interprets environmental variation to produce a range of phenotypes from the same genotype.”

Dufty, Clobert, and Møller, 2002

Sceloporus undulatus

Home Range Analysis:

Spacing Patterns and Reproductive Success

Sceloporus undulatus Eastern Fence Lizard

Unique Paint Mark for

Identification

Male Sceloporus undulatus

Home ranges are large and overlapping.

Home range area of males is 10X greater than females.

-1 0 1 2 3 40

1

2

3

4

5A.

Log Male Density (n/hectare)

Log

HR (m

2 )

Home ranges of males are large and overlapping.

Home range area depends on population density.

Home range area is an order of magnitude

greater in NJ than in other populations.

-1 0 1 2 3 40

1

2

3

4

5A.

Log Male Density (n/hectare)

Log

HR (m

2 )

Male home range

Female home ranges

Male movements

Spatial distribution of females drives movement and home range behavior of males.

Male Endurance

Apr May Jun Jul Aug Sep0

10

20

30

19941995

a

a a a a

β

α

α α α

Month

Tim

e on

Tre

adm

ill (m

in)

Running Endurance


10

20

30

FemaleMale

p=0.009

p<0.001

Month

Tim

e on

Tre

adm

ill (m

in) … and is greater in males

than in females during the breeding season.

Exercise endurance in males is greatest during the

breeding season …

Environmental Variation:

A “Natural Experiment”

Mar Apr May Jun Jul Aug Sep Oct0

15

30

45

60

TBMale

a

b

b,c

cb,c b,c

b,cb,c

γ γ γ γ

α

β ,γβ

γ

Month

Plas

ma

[T] o

r [B

](n

g/m

l)Male Endurance


10

20

30

19941995

a

a a a a

β

α

α α α

Month

Tim

e on

Tre

adm

ill (m

in)

Testosterone and corticosterone vary roughly in parallel with endurance.

Environmental Variation:

A “Natural Experiment”


Exogenous testosterone ↑ endurance.

(But corticosterone has no effect.)

Experimental Manipulation

Surgical Castration

+

Testosterone Replacement

TESTOSTERONE promotes home range acquisition.

C A C O T E0

400

800

1200

1600

a

b

cHo

me R

ange

Are

a (m

2 )

1.74 1.76 1.78 1.80 1.82 1.842.5

3.0

3.5

4.0

4.5

Log Snout-Vent Length (mm)

Log

Hom

e Ra

nge

(m2 ) R2 = 0.25

p=0.016

HR area increases with body size …

1.74 1.76 1.78 1.80 1.82 1.842.5

3.0

3.5

4.0

4.5

Log Snout-Vent Length (mm)

Log

Hom

e Ra

nge

(m2 ) R2 = 0.25

p=0.016

-0.02

-0.01

0.00

0.01

0.02

2-Yr. Old

≥3-Yr. Old

Age Classp=0.003

Res

idua

l Hom

e R

ange

Are

a

… and with age. HR area increases with body size …

-0.75 -0.50 -0.25 0.00 0.25 0.50 0.75-0.50

-0.25

0.00

0.25

0.50P=0.017

Residual Home Range Area

Res

idua

l No.

of F

emal

es

Males increase their HR area by searching for females.

-0.75 -0.50 -0.25 0.00 0.25 0.50 0.75-0.50

-0.25

0.00

0.25

0.50P=0.017

Residual Home Range Area

Res

idua

l No.

of F

emal

es

Males compete for females, not for HR area per se.

Larger males sire more and larger clutches.

CORTICOSTERONE “Successful” home range behavior is strenuous

and may require high endurance.

Plasma [CORT] is correlated with

endurance:

r = 0.414, p = 0.0002, n = 76

Attainment of high fitness can be stressful.

Size Distributions of All Adults

55 60 65 70 75 800

5

10

15FemalesMales

Snout-Vent Length (mm)

p << 0.0001N

umbe

r of

Liz

ards

Index of SSD = 0.124

Sexual dimorphism in body size (SSD): an expression of body size in males relative to body size in females.

Photograph: Lukáš Kratochvíl

RMCox

Sexual Size Dimorphism (SSD) ♀ > ♂ ♂ > ♀

… while males are larger than females in many others?

Why are females larger than males in some species …

Cox, Stenquist, & Calsbeek, 2009

SSD in lizards and snakes

Aga

mid

aeC

rota

phyt

idae

Igua

nida

eP

hryn

osom

atid

aeP

olyc

hrot

idae

Tro

pidu

ridae

Var

anid

aeA

ngui

dae

Gym

noph

thal

mid

aeT

eiid

aeLa

cert

idae

Sci

ncid

aeG

ekko

nida

eP

ygop

odid

ae

-0.6

00.

60.

40.

2-0

.4-0

.2

Mal

e-b

iase

d S

SD

Fem

ale-

bias

ed S

SD

M FM FM M M M M

Nat

ricin

aeX

enod

ontin

aeC

olub

rinae

Ela

pida

eV

iper

idae

Acr

ocho

rdid

aeB

oida

eS

cole

coph

idia

-1.2

01.

20.

80.

4-0

.8-0

.4

F F F F FM

LIZARDS SNAKES

Aeluroscalabotes felinus

Paroedura picta

Crotalus atrox

Cox, Butler, & John-Alder, 2007; John-Alder, Cox, & Taylor, 2007; Cox, Stenquist, and Calsbeek, 2009; Kratochvil, Kubicka, Golinski, & John-Alder, unpubl.

S. undulatus

S. virgatus

Anolis sagrei S. jarrovii

S. magister

http://gsnb.rutgers.edu/

No Sexual Difference in Neonatal Body Size

22 25 28 31 34 37

1

3

5

7 Females Male

p=0.366


Num

ber o

f Liz

ards

Laboratory Hatchlings:

♀: 24.44 ± 0.08 mm

♂: 24.23 ± 0.08 mm

n = 339, p=0.063

Size Distributions of 2-Yr. Olds

55 60 65 70 75 800

5

10FemalesMales


p << 0.0001N

umbe

r of

Liz

ards

Index of SSD = 0.102

0.00

0.03

0.06

0.09

0.12

Index of SSD

40

60Snout-Vent (mm)

*

**

8 9 10 11 12 130.1

0.2

0.3

Growth Ratemm/day

Age (Months)

Females are larger than males by 11 months of age.

Growth rates diverge sharply between 10 and 11 months of age.

Development of SSD

0

0.02

0.04

0.06

0.08

0.1

0.12

Augus

tOct

Dec Feb

April

June

Augus

tOct

Dec Feb

April

Sexual divergence in growth is correlated with:

• ↑ Male coloration • ↑ Male aggression • ↑ Male activity

♂ ♀


Correlated effects of testosterone ??

Skelly & John-Alder, Unpubl.

Experimental Enclosure

Rutgers University Pinelands Research Center, New Lisbon, NJ


0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 150

10

20

30

40

50

MaleFemale

Oct May Jul Oct

11

3

11

5

A

10 114

3

Age (months)

Pla

sma

T (n

g m

l-1)

45 d 418 d0

10

20

30

40

50 (7,2) Testosterone(7,5) Castrated(6,4) Control(11) Female

F2,17 = 40.25; P < 0.001

a b b

F2,8 = 37.58; P < 0.001

a b b

F1,15 = 0.21P = 0.326

B

(age 12 mo) (age 24 mo)

Measurement Date (d post-release)

Pla

sma

T (n

g m

L-1

)

Testosterone is implicated in the development of SSD.

8 9 10 11 12 130.1

0.2

0.3

Growth Ratemm/day

Age (Months)

Cox, Skelly, & John-Alder, 2005

Castrated Female Castrated + T Intact

One Year: ~1 ng / h

300 µg

~175 µg

Scanned images of live lizards

Cox, Skelly, Leo, & John-Alder, 2005

0 10 20 30 40 50 6040

42

44

46

48

50

52

54

56

Testosterone

ControlCastrated

A (2001)

Elapsed Time (d post-release)

SV

L (m

m)

0 10 20 30 40 50 6042

44

46

48

50

52

54

56

58

Testosterone

ControlCastrated

Female

B (2002)

Elapsed Time (d post-release)

SV

L (m

m)

Testosterone Castrated Control Female0.0

0.1

0.2

0.3

a b bF3,40 = 13.71; P < 0.001

C F1,16 = 3.24; P = 0.040

8 8 9 6 6 12

Treatment/Sex Group

Gro

wth

Rat

e (m

m d

-1)

Testosterone inhibits growth in Sceloporus undulatus.


38 40 42 44 46 48 50 52 5456

58

60

62

64

66

68

CastratedControl

Testosterone

F = 41.11P < 0.001

Initial 2002 SVL (mm)

Fina

l 200

3 S

VL

(mm

)

Castration Growth; Testosterone Growth



Growth Growth

Growth

Acquisition / Allocation?

↓ Food Consumption

∆ Energy Distribution

♂ ♀ ♀

♂ ♂

Smaller Pie Smaller Piece

T and Energy Acquisition

F+U estimates C in the lab.

0 1 2 3 40.00

0.05

0.10

0.15 FemaleMale ControlMale + T

Food Intake (crickets/d)

Feca

l Dry

Mas

s (g

/d)

Lab: r2 = 0.65 P < 0.001

12 10 6

T does not reduce Consumed Energy in the field or lab.

T and Energy Acquisition

F+U estimates C in the lab.

T does not affect F+U in the field.

0 1 2 3 40.00

0.05

0.10

0.15 FemaleMale ControlMale + T

Food Intake (crickets/d)

Feca

l Dry

Mas

s (g

/d)

Lab: r2 = 0.65 P < 0.001

Female Control Male Male+T0.00

0.01

0.02

0.03

0.04

Feca

l Dry

Mas

s (g

/d)

Field: F = 0.41 P = 0.67

12 10 6

T does not reduce Consumed Energy in the field or lab.

Energetic Cost of 1.5 h Activity (% Cost of Growth)

0 25 50 75 100 125 150 175 200

S. undulatus

S. graciosus

S. occidentalis

S. variabilis

S. virgatus

S. occidentalis

S. variabilis

S. virgatus

S. virgatus

S. virgatus

Mean

a

a

Summer Juveniles

Summer Adults

Spring Adults

Spring Juveniles

Fall Adults

Bastonal Adults

Monte Pio Adults

Spring Males

Spring Females

Summer Males

Summer Females

S. occidentalis

ThermalIncrement in RMR

Cost ofFree Existence

0 20 40 60 80 100 120 140

Energetic Cost of Growth

Energetic Cost of 1.5 h Activity (J)

Sce

lopo

rus

Spe

cies

Testosterone stimulates activity and a 1.5 h extension in active day length.

This bar is our literature-based estimate of the

cost of 1.5 h of activity.


Energetic Cost of 1.5 h Activity (% Cost of Growth)

0 25 50 75 100 125 150 175 200

S. undulatus

S. graciosus

S. occidentalis

S. variabilis

S. virgatus

S. occidentalis

S. variabilis

S. virgatus

S. virgatus

S. virgatus

Mean

a

a

Summer Juveniles

Summer Adults

Spring Adults

Spring Juveniles

Fall Adults

Bastonal Adults

Monte Pio Adults

Spring Males

Spring Females

Summer Males

Summer Females

S. occidentalis

ThermalIncrement in RMR

Cost ofFree Existence

0 20 40 60 80 100 120 140

Energetic Cost of Growth

Energetic Cost of 1.5 h Activity (J)

Sce

lopo

rus

Spe

cies

Our estimate of energy expenditure is validated by these doubly-labeled water measurements of field metabolism in lizards.


Female-larger S. undulatus

Testosterone increases:

Maintenance Growth Activity, Movement, etc.

Maintenance Growth Activity, Movement, Home Range

Maintenance Growth Activity, Movement, etc.

Available Energy

TEST CON

CAST

Energy Allocation Trade-Off

CAST CON TEST0

2

4

6

8

10

12

a ab

Daily

Act

ivity

Per

iod

(h d

-1)

CAST CON TEST0

20

40

60

80

a a

b

Daily

Mov

emen

t (m

d-1

)

CAST CON TEST0

400

800

1200

1600

a

b

c

Hom

e Ra

nge

Area

(m2 )

Activity Period Movement Home Range Area

Cox, Skelly, & John-Alder (2005) Physiol. Biochem. Zool.

Female-larger Sceloporus virgatus

37 39 41 43 45 47 49 51 53

0.00

0.05

0.10

0.15

0.20

0.25

0.30

TESTCAST

Initial SVL (mm)

Gro

wth

Rat

e (m

m/d

)

p

S. virgatus S. jarrovii

b

a

α

β

Species

Male-larger Sceloporus jarrovii

48 50 52 54 56 58 60 62

TEST

CAST

0.00

0.05

0.10

0.15

0.20

0.25

0.30

Initial SVL (mm)

Grow

th Rate (m

m/d)

S. virgatus

SSD: ♀ > ♂

S. jarrovii

SSD: ♂ > ♀

Bipotential Growth Regulation Hypothesis

SSD Effect of T

none

Species Study

Psammodromus algirus

Thamnophis sirtalis

Anolis sagrei

Urosaurus ornatus


Sceloporus virgatus

Sceloporus jarrovii

Salvador & Veiga 2000

Crews et al. 1985 Lerner & Mason 2001

Cox et al. 2009

Hews et al. 1994 Hews & Moore 1995

Klukowski et al. 1996 Cox et al. 2005

Abell 1998 Cox & John-Alder 2005

Cox & John-Alder 2005

Cox, Stenquist, & Calsbeek, 2009

Photograph: Lukáš Kratochvíl

Special thanks to: Bob Cox (UVa), Christine Duncan (Fresno State), Greg

Haenel (Elon Univ), Linda Smith (Richard Stockton College)

Major funding from: National Science Foundation Society for Integrative and Comparative Biology Rutgers University

Documents

Ecological and Evolutionary Physiology of Sexual ... John Alder - Ecological and...Department of Ecology, Evolution, and Natural Resources . ... 5 A. Log Male Density (n/hectare) Log