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Adaptation to Change
Donal T. Manahan
Professor of Biological Sciences
University of Southern California
Adaptation to Change
Genotype plus Environment = Phenotype
Genetics = Change over longer time
Physiology = Change over short time
Climate Change in the News a Lot
Warming of oceans: life history and trophic mismatch
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.
Amount
Trophic Match
“Plant”
“Animal”
Time
Trophic Mismatch
Amount
“Larvae”
Time
“Phytoplankton”
Complex Life Histories
Physiology –
The Science of “How Organisms Work”
The Larval Biology “Black Box”
Food limitation, predation, transport, dispersal etc.
Eggs
Larval
Mortality
Recruitment
<<1%
Themes for Today’s Presentation
Genetic Crosses
Phenotype
(Variation in Survival and Growth)
Genomics
Physiology
Complex Traits:
Life Span
Feeding, Metabolism
Measure & Predict?
Different growth rates in similar environment of
food and temperature (N = 35 different larval families)
3&5
Larval families crossed
2&5
2&3
5&6
2&6
2&5
3&5
1&5
Up to a 4-times faster
growth rate
1&3
3&5
2&5
2&3
0
5
10
Growth rate (µm day-1)
15
20
Data from Pace et al., 2006
J. 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 differences
under same environmental conditions
Growth = [Energy In] minus
[Energy Out]
Condition index
- mass
- volume
feeding
Particulate (algae)
Dissolved nutrients
(transport rate)
Data from Pace et al., 2006
J. Exp. Mar. Biol. Ecol.
metabolism & excretion
Energy consumption
- metabolic rate
- growth efficiency
- aerobic capacity
(citrate synthase)
- ion regulation
(ATPase)
Loss of ingested food
- absorption efficiency
Difference in slow and
fast growing larvae
No difference
20
10
Growth rate (µm day-1)
Clearance rate (µl larva-1 hr-1)
Fast growing larvae possess higher
size-specific feeding rates
6
5x2
5x5
2x2
4
16
14
12
10
8
6
4
2
0
2x2
2
150
180
220
Shell length (µm)
260
320
5x5
5x2
Physiological scaling of ~2-fold higher
feeding rates set genetically
60
-1
Clearance rate (µl larva hr )
40
60
40
40
-1
-1
-1
Clearance rate (µl larva hr )
60
20
10
6
4
2
20
20
10
10
6
6
4
4
Fast-growing larval families)
Slow-growing larval families)
2
2
150
180
220
260
320
Shell length (µm)
Average feeding rate
at 220 µm (N = 332)
150
180
220
260
Shell length (µm)
320
150
180
220
260
320
Shell length (µm)
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 rates
Not ‘simple’ reduction in rate
Fast-growing larvae
Slow-growing larvae
33
250
35
100
53
16
25
12
8
10
4
5
0
3x3
80
100
150
225
Shell length (µm)
320
5x3
3x5
Shell growth (µm day-1)
Respiration rate
-1
-1
(pmol O2 larva hr )
600
Similar size-specific metabolic rates
Not ‘simple’ reduction in rate
Fast-growing larvae
Slow-growing larvae
55
250
100
22
16
25
25
12
8
10
4
5
0
2x2
80
100
150
225
Shell length (µm)
320
5x5
2x5
Shell growth (µm day -1)
Respiration rate
-1
-1
(pmol O2 larva hr )
600
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)
250
Protein synthesis
ng protein day-1
200
Protein degradation
Fed larva
percent metabolism
150
100
Protein synthesis
Protein growth
50
75%
38 ng protein day-1
0
4
6
8
10
12
Age (days)
14
16
18
From Pace and Manahan, 2006
J. Exp. Biol.
(sea urchin larvae)
How to grow faster in the same environment?
40
-1
-1
Clearance rate (µl larva hr )
60
Feeding rate
20
50%
10
6
4
2
150
180
220
260
320
Shell length (µm)
Metabolism:
Protein depositional efficiency
50%
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
Reciprocal cross
between parental lines
Line 3
Line 5
♀
♀
Line 3
3x3
3x5
♂
Line 5
5x3
5x5
10
Growth Rate (µm day -1)
♂
Larval families with
differential growth
9
8
7
6
5
3x3
3x5
5x3
5x5
ANOVA, P<0.05
Transcriptome analysis
cDNAs cloned on beads
(MegaCloneTM)
Slow-growing
Fast-growing
Sequences read & counted
(MPSS: Massively Parallel
Signature SequencingTM)
Shared
genes
‘Slow-growth
genes’
‘Fast-growth
genes’
Advantages of MPSS:
High sensitivity ( 3 tpm.)
No a priori sequence needed
Gene ID by ‘signature sequence’
Brenner et al, 2000 Nature Biotech. 18:630
Matches to genes annotated in Gene Ontology
Functional Category
Its more than environment, and its more than simple
Protein Synthesis
additive genetics
Chromosome Organization
60%
62%
Electron Transport
ATP Synthesis
Endocytosis
Protein Folding
Regulation of Metabolism
Response to Oxidative Stress
http://www.GeneOntology.org/
“Building the Organism”
Developmental Biology
(Egg to Larva)
Requires 1000s of genes
Growth Physiology
(Variation in Size)
Number of genes = ?
10? 100? 1,000? 10,000?
Highly complex metabolism
What 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
Physiological Genomics
Define mechanisms of growth and survival
based on known Phenotypic Contrasts
Phenotype
(Variation in Survival and Growth)
Genomics
Physiology
Recruitment: Population Connectivity and
Dynamics, Species Management …
Chemical Environment
Physical Environment
Nutritional; chemo-sensory
Currents; hydrography
RECRUITMENT BIOLOGY
Ecology, Evolution
Physiology, Biochemistry
Cellular, Molecular