Bruno Ernande, NMA Course, Bergen On the Evolution of Phenotypic Plasticity In Spatially Structured Environments Bruno Ernande Fisheries Department IFREMER

Bruno Ernande, NMA Course, Bergen

On the Evolution of Phenotypic Plasticity In Spatially Structured Environments

Bruno Ernande

Fisheries Department

IFREMER

Port-en-Bessin, France


Definitions

∎Phenotypic plasticity Phenotype = Genotype + Environment

zij = gi + Ej

a single genotype can produce different phenotypes according to the environment where it develops and lives

this holds for both spatial and temporal environmental variation

∎Reaction normthe systematic profile of phenotypes zij

expressed by a single genotype gi in response to a given range of environments Ej

∎Phenotypic plasticity may be an active process allowing short term adaptation. Can it be selected for?

Environment E

g1

degree ofplasticity

reaction norm

Phen

otyp

e z

g2


Prerequisites for phenotypic plasticity to evolve

∎To be selected for, phenotypic plasticity needs toenhance fitness of plastic genotypes relative to non-plastic onesbe under genetic controlexhibit sufficient additive genetic variance in the population

∎Requirements are met in both plants and animals: Schlichting 1986; Sultan 1987; Scheiner 1993; Pigliucci 1996

Vp = Vg + VE + VgE

Vg

Vp = Vg + Ve

Ve

g1

g2

Environment E

Phen

otyp

e z

g1

g2

Environment E

Ve

Vp


How to represent reaction norms in models?

∎Character-state reaction norm{zi1, zi2, zi3, zi4, zi5}: the different

character-states are evolving under the constraints imposed by correlations across environments

Falconer 60’s, Via and Lande 1985, Kawecki and Stearns 1993

∎Polynomial reaction norm{zi0 , s}: intercept and slope are

considered as the evolving traits.Gavrilets and Scheiner 1993a,b

E

gi

1 2 3 4 5

zi1

zi2

zi3

zi5

zi4

z

Slope, s

E

z

gi

intercept

E0

zi0


How to represent reaction norms in models?

∎Reaction norm as a functional traitzi(E): reaction norm is represented by a flexible function which can evolve like a trait

Gomulkiewicz & Kirkpatrick 1992This of course the most flexible way to model a reaction norm

E

gi

z

zi(E)


Previous models of phenotypic plasticity evolution

∎Optimality Theory: Ecologically oriented models

Geared toward identifying the selective pressures favouring or preventing the evolutionary emergence of phenotypic plasticity

― from explicit ecological scenarios and― a priori trade-offs

Based on population dynamics, no genetics: phenotypic evolutionLong-term evolution but no evolutionary transients, only evolutionary equilibriaNo density- nor frequency-dependent populations: interactions between individuals

are not accounted forStearns and Koella 1986; Houston and McNamara 1992; Kawecki and Stearns 1993;

Sasaki & de Jong, 1999


Previous models of phenotypic plasticity evolution

∎Quantitative genetics: Genetically oriented models

Aim at identifying the implications of the underlying genetics for the evolutionary emergence of phenotypic plasticity, focusing mainly on genetic constraints such as

― the lack of additive genetic variance or ― genetic correlations

Based on a statistical description of the population, no detailed ecologyEvolutionary transients together with equilibria, but short term evolution (constant

additive genetic (co-)variance matrix)No density- nor frequency-dependent populations: interactions between individuals

are not accounted forVia and Lande 1985, 1987; Van Tienderen 1991, 1997;Gomulkiewicz and Kirkpatrick

1992; Gavrilets and Scheiner 1993


Under-investigated aspects

∎Density-dependent population dynamics and frequency-dependent selectionWould allow to account for phenotypic plasticity triggered by interactions between

individuals such as competition for food resources or mates, predation,…

∎Accounting for different types of costs of phenotypic plasticityMaintenance costs: expenses incurred by maintaining the potential for being plasticProduction costs: costs paid by a plastic genotype actually producing a given

phenotype in excess to those incurred by a fixed genotype producing the same phenotype

∎The consequence of alternative distribution patternsAre individuals distributed randomly across environments or do they select it?

∎The evolutionary implications of a precise environmental settingFrequency of the different environments, the quality of the resource they offer…

How these factors are driving the potential evolution of phenotypic plasticity, how do they interact and what is their relative importance?


The modelling approach

∎We use adaptive dynamics theory (Metz et al. 1992; Dieckmann & Law 1996; Metz et al. 1996; Geritz et al. 1998) and its recent extension to function-valued traits

∎Properties and assumptions:Selection gradient derived from explicit ecological scenariosPhenotypic model (clonal model), no geneticsLong term evolution of phenotypic plasticity: mutation driven (slow mutation rate,

small mutational steps)Describes adaptive transient states together with evolutionary equilibriaAllows to account for interactions between individuals

― density-dependent population dynamics and― frequency-dependent selection

Ernande & Dieckmann 2004 JEB


The basics

∎ Individuals are living across a range of environments e that can represent:abiotic parameters (temperature, salinity, amount of nitrates…)biotic characteristics (species or densities of preys, of predators, types of

competitors )

∎The phenotype p can vary across environmental types e according to a function p(e) which is a reaction norm

∎Determinants of environmental heterogeneity:

How frequent are the different environmental types? Frequency of occurence o(e)

What is the quality of the different environments? Intrinsic carrying capacity k(e)

How sensitive to phenotypic variation is the performance of organisms in each type of environment? Sensitivity to maladaptation s(e)



Model structure

Phenotype

REACTION NORM

Environment

FITNESS Long term growth rate of a

rare mutant in a resident population

Costs ofPhenotypic PlasticityMaintenance, production

+

Population Growth rate

Resource utilization efficiency

Competition:-Asymmetry-Realized carrying capacity

Distribution strategyof the individuals

Environment




Phenotype

REACTION NORM

Environment





∎ In each environment e, a matching phenotype m(e) maximizes efficiency of resource utilization Ep(e) (harvesting, handling, digestibility,…)

in a given environment e

Effic

ienc

y, E

p(e)

Phenotype, p(e)m(e)0

1

along an environmental gradient

s(e)mat

chin

g, m

(e)

p(e)

s(e)

sensitivity



Resource competition

Phenotype

REACTION NORM

Environment



Environment



Com

petit

ion

coef

ficie

nt, A

(E

)

Difference in efficiency, E

degree of asymmetry

E<0

E>0

2

1

00

Resource competition

∎Competition for resources

logistic density-dependence with a coefficient of competition A(E) and a realized carrying

capacity kp(e), both depending on the resource utilization efficiency.

Rea

l ized

car

ryi n

g ca

paci

t y, k

p(e)

Efficiency, Ep(e)

k(e)

0 10



Alternative distribution strategies

Phenotype

REACTION NORM

Environment




Environment



Alternative distribution strategies

∎Random Distribution:

No selective control over local habitat

Environment, e

Occurrence, o(e)Quality, k(e)Efficiency, Ep(e)

Distribution, dp(e)

∎ Ideal Free Distribution:

Individuals can detect intrinsic quality of the

different environments

∎ Optimal Foraging:

Individuals can both detect intrinsic quality

of the different environments and distribute

according to their efficiency.Ernande & Dieckmann 2004 JEB


Distribution, dp(e)


Distribution, dp(e)


Population growth rate

Phenotype

REACTION NORM

Environment





Environment



Costs of phenotypic plasticity

Phenotype

REACTION NORM

Environment


+





Environment



Costs of phenotypic plasticity

∎Costs increase with departure from the developmental base-line.

The total costs of the reaction norm are proportional to its variance around the developmental base-line.

∎Three types of costs maintenance costs independent of

the distribution of the individuals production costs depending fully on

the distribution mixed cost

Phen

otyp

e, p

(e)

Environment, e

Distribution, dp(e)

MaintenanceProduction



Invasion fitness of a mutant




+





EnvironmentPhenotype

REACTION NORM

Environment



Canonical equation

∎Fitness of a rare mutant p’ in a resident population p:

∎Adaptive dynamics of a function valued trait p are are given by:

Dieckmann & Heino 2001

with p(e,e’): the mutational variance-covariance function,

gp(e): the selection gradient in environmental type e is the functional

derivative of the fitness function f(p’,p) at trait p’ = p.

frequency-dependence

ppCostspprateGrowthppf ,, ,

edegeenepdt

dppp )(),(ˆ

2

1)( 2


00

,,,

lim

ppfppfppf

eg ee

p


Evolutionary trajectories

Phenotype

REACTION NORM

Environment




+





Environment



Evolutionary equilibria

∎Evolutionary equilibria p* or evolutionary singularities are attained when:

∎This is possible when

the selection gradient vanishes at p*, gp*(e’) = 0

Selection induced-equilibria.

the mutational variance-covariance function p*2(e,e’) is singular at p*

Covariance induced equilibria.

0 )(),( *2

* edegee pp



Selection-induced equilibria

∎Evolutionary singularities are characterized by a balance between two opposing forces:

one toward the matching phenotype m(e) with a weightthe other toward the cost-free generalist phenotype with a weight

∎The weights of the two forces depend on the distribution strategy of the individuals:

m

gp

)]()(/[*])()()([)(* eepeemeep gmgm

)()()21()( esewwrae xm )()(/)( * eKewKEwce x

pg

)()()()21()( eseKewKwrae xxm )()(/)( * eKewEwKce xx

pg

)()()()21()( * eseKewEKwrae xp

xxm )()()( * eKewwKEce xx

pg

R.D.

I.F.D.

O.F.



Evolutionary effect of the different types of costs

∎As costs are shifting from maintenance to production type (i.e. increases), the effects of:

the frequency of occurence o(e) of the different environmental types in case of all distribution strategies,

the intrinsic carrying capacity k(e) in case of Ideal Free Distribution and Optimal Foraging.

∎on the shape of the reaction norm disappear.

m(e

)

p



Evolutionary effect of the distribution strategies

∎The effect of carrying capacity differs according to the kind of distribution strategy considered:

in case of Random Distribution, better matching evolve in poor environments

in of Ideal Free Distribution and Optimal Foraging, better matching evolves in good environmental types

p

m(e)



Evolutionary branching of reaction norms

∎ If costs of plasticity and sensitivity are higher

1. Directional selection monomorphic maladapted reaction

norm

2. Selection turns disruptive evolutionarily non-stable

3. Protected dimorphism in reaction norm: Evolution of Trophic Specialization.

Monomorphic

Dimorphic 2

Dimorphic1


Conclusions

∎Evolution of phenotypic plasticity can be driven by frequency-dependent interaction between conspecifics allow for branching of reaction norms and apparition of polymorphism in the degree of phenotypic plasticity.

∎Considering different type of costs of phenotypic plasticity have a drastic effect on the shape of reaction norm: interact in an intricate manner with the environmenal setting;

∎ Distribution strategy of the individuals is a crucial factor: changes the effect of the quality of the environments and the susceptibility for branching in reaction norms

∎Promising developments:

the systematic exploration of branching points in reaction norms,

the evolutionary competition between generalist, specialist and “plasticist”: the coevolution between distribution patterns and phenotypic plasticity,

development of a model in case of a temporally fluctuating environment.

Documents

Bruno Ernande, NMA Course, Bergen On the Evolution of Phenotypic Plasticity In Spatially Structured Environments Bruno Ernande Fisheries Department IFREMER