Adaptation to Change

Donal T. ManahanProfessor of Biological Sciences

University of Southern California

Adaptation to Change

Genotype plus Environment = Phenotype

Genetics = Change over longer timePhysiology = Change over short time

Climate Change in the News a Lot

Comprehensive study of ~400 taxa, from 1958 to 2002.(>115,000 samples)

Sir Alister Hardy Foundation for Ocean Science, The Laboratory, Citadel Hill, Plymouth, UK

Impact of climate change on marine pelagic phenology and trophic mismatch. Edwards, M. and A.J. Richardson, 2004. Nature, 430: 881.

Climate impact on plankton ecosystems in the Northeast Atlantic. Richardson, A.J. and D.S. Schoeman, 2004. Science, 305: 1609.

Warming of oceans: life history and trophic mismatch

Time

Am

oun

tTrophic Match

“Plant” “Animal”

Time

Am

oun

tTrophic Mismatch

“Phytoplankton”“Larvae”

Physiology – The Science of “How Organisms Work”

Complex Life Histories

The Larval Biology “Black Box” Food limitation, predation, transport, dispersal etc.

EggsRecruitment

<<1%Larval

Mortality

Phenotype(Variation in Survival and Growth)

Genetic Crosses

Genomics Physiology

Complex Traits:Life Span

Feeding, MetabolismMeasure & Predict?

Themes for Today’s Presentation

0 5 10 15 20

2 & 3

2 & 5

3 & 5

1 & 3

1 & 5

3 & 5

2 & 5

2 & 6

5 & 6

2 & 3

2 & 5

3 & 5

Growth rate (µm day-1)

Lar

val f

amili

es c

ross

edDifferent growth rates in similar environment of

food and temperature (N = 35 different larval families)

Up to a 4-times faster growth rate

Data from Pace et al., 2006J. Exp. Mar. Biol. Ecol.

Large-scale Culturing Experiments (200-liter vessels x 20 units = 4,000 liters)

~2 million individuals of same larval family

per culture vessel

Physiological bases of growth differencesunder same environmental conditions

Growth = [Energy In] minus [Energy Out]

feeding metabolism & excretionParticulate (algae)

Dissolved nutrients (transport rate)

Energy consumption - metabolic rate - growth efficiency - aerobic capacity

(citrate synthase) - ion regulation

(ATPase)

Loss of ingested food - absorption efficiency

Difference in slow andfast growing larvae

No difference

Condition index - mass - volume

Data from Pace et al., 2006J. Exp. Mar. Biol. Ecol.

Fast growing larvae possess higher size-specific feeding rates

Shell length (µm)

150 180 220 260 320

Cle

aran

ce r

ate

(µl l

arva

-1 h

r-1)

2

4

6

10

20

5x25x52x2

2x2 5x5 5x2

Gro

wth

rat

e (µ

m d

ay-1

)0

2

4

6

8

10

12

14

16

Physiological scaling of ~2-fold higher feeding rates set genetically

Shell length (µm)

150 180 220 260 320

2

4

6

10

20

40

60

Shell length (µm)

150 180 220 260 320

Cle

aran

ce r

ate

(µl l

arva

-1 h

r-1)

2

4

6

10

20

40

60

Fast-growing larval families)

Slow-growing larval families)

Shell length (µm)

150 180 220 260 320

Cle

ara

nce

ra

te (

µl l

arva

-1 h

r-1)

2

4

6

10

20

40

60

Average feeding rate at 220 µm (N = 332)

Fast-growers = 21.7 µl larva-1 h-1

Slow-growers = 11.4 µl larva-1 h-1

~ 2-times faster

Similar size-specific metabolic ratesNot ‘simple’ reduction in rate

53

3533

3x3 5x3 3x5

Sh

ell gro

wth

(µm

day

-1)

0

4

8

12

16

Fast-growing larvae

Slow-growing larvae

2522

55

2x2 5x5 2x5

Sh

ell gro

wth

(µm

day

-1)

0

4

8

12

16

Fast-growing larvae

Slow-growing larvae

Similar size-specific metabolic ratesNot ‘simple’ reduction in rate

Physiological regulation of differential growth rates

1. Feeding: ~ 50% of growth rate variation

2. Metabolic regulation: Not total metabolic rate, but differential energy allocation efficiency (mechanism?)

The high cost of growth (protein)

Age (days)

4 6 8 10 12 14 16 18

ng

pro

tein

day

-1

0

50

100

150

200

250

Protein growth

Age (days)

4 6 8 10 12 14 16 18

ng

pro

tein

day

-1

0

50

100

150

200

250

Protein synthesis

Age (days)

4 6 8 10 12 14 16 18

ng

pro

tein

day

-1

0

50

100

150

200

250

Protein degradation

From Pace and Manahan, 2006J. Exp. Biol.

(sea urchin larvae)

Fed larva percent metabolism

Protein synthesis

75%

38 ng protein day-1

Shell length (µm)

150 180 220 260 320

Cle

aran

ce r

ate

(µl l

arva

-1 h

r-1)

2

4

6

10

20

40

60

Feeding rate

How to grow faster in the same environment?

50%

50%Metabolism: Protein depositional efficiency

Biological Variation[e.g., growth; size; feeding; physiological rates; etc.]

• Vast majority of adaptive traits show complex inheritance –

i.e., likely many genes contributing to a complex trait

• Hard to unravel the connections between

genes, complex traits, and adaptation.

Genomic Analysis of Differential Growth

♂Line 3

♀Li

ne 5

♂Line 5

♀Li

ne 3

3x3 5x3

3x5 5x5

Reciprocal cross between parental lines

Larval families with differential growth

ANOVA, P<0.05

Gro

wth

Rat

e (µ

m d

ay-1

)

5

6

7

8

9

10

3x3 3x5 5x3 5x5

Transcriptome analysis

‘Slow-growthgenes’

‘Fast-growthgenes’

Sharedgenes

cDNAs cloned on beads

(MegaCloneTM)

Sequences read & counted

(MPSS: Massively ParallelSignature SequencingTM)

Slow-growing Fast-growing

Advantages of MPSS:

High sensitivity ( 3 tpm.)No a priori sequence neededGene ID by ‘signature sequence’

Brenner et al, 2000 Nature Biotech. 18:630

Matches to genes annotated in Gene Ontology

Its more than environment, and its more than simple additive genetics

Functional Category

Protein SynthesisChromosome OrganizationElectron Transport

ATP Synthesis

EndocytosisProtein FoldingRegulation of MetabolismResponse to Oxidative Stress

62%

http://www.GeneOntology.org/

60%

“Building the Organism”

Growth Physiology(Variation in Size)

Number of genes = ? 10? 100? 1,000? 10,000?

Developmental Biology(Egg to Larva)

Requires 1000s of genes

Highly complex metabolismWhat to measure? How to predict?

Food from the ocean – Hybrid animal protein production

Worldwide production of C.gigas = 4.4 M metric tons ($3.7 billion)FAO Yearbook of Fishery Statistics, 2003

Phenotype(Variation in Survival and Growth)

Genomics Physiology

Physiological Genomics

Define mechanisms of growth and survival based on known Phenotypic Contrasts

Recruitment: Population Connectivity and Dynamics, Species Management …

RECRUITMENT BIOLOGY

Ecology, Evolution

Physiology, Biochemistry

Cellular, Molecular

Chemical EnvironmentNutritional; chemo-sensory

Physical EnvironmentCurrents; hydrography