Evolution of body-size - École Normale SupérieureCope's rule (1896) Kingsolver & Pfennig (Evolution 2004): a meta-analysis of selection (linear selection gradient ) on individual

Evolution of body-size

Eric Edeline: [email protected]

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RotifersSize: 0.1-0.5 mmLifespan: 10 days

Molluscs (Arctica islandica)Size: 13 cmLifespan: 400 years

Among animals

Introduction : correlates of body size

Body size variation and covariation with life history traits

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Among animals



N = 1700 species (http://genomics.senescence.info/species/)

http://genomics.senescence.info/species/

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Sequoia sempervirensHeight: 115 mLifespan: 2,200 y

ChlamydomonasSize: 10μmLifespan: minutes to days (sexual and asexual reproduction)

Among plants



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White-toothed pygmy shrew (Suncus etruscus)6 cm, 2 gGestation: 27 dClutch size: 6Weaning: 17dMaturity: 2yLifespan: 3y

Blue whale (Balaenoptera musculus)20 to 34 m, 100 to 190 tGestation: 12 moClutch size: 1 every 3 yearsWeaning:Maturity: ~5 yLifespan: >100 y

Among mammals



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Gasterosteus aculeatusLength: 5-14 cmMaturity: 1yLifespan: 1-8yClutch size: 60-400 eggs

Whale shark Rhincodon typusSize: 20 m, 34 t Clutch size: few hundreds (ovoviviparity)Maturity: 30yLifespan: 100-150y

Among fish Body size variation and covariation with life history traits


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Intraspecific variability

Southern France:Body size: 3-6 cmlifespan: 1 year

Drizzle Lake in Queen Charlotte Islands:Body size: 7-10 cmlifespan: 8 year

Most of the range: Body size: 4-7 cmlifespan: 2-4 year



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Hippoglossoides platessoides

Scotland:Max size: 25 cmMax age: 6 yearsMaturity: 20 cm and 3 years

Grand banks of Newfoundland:Max size: 60 cmMax age: >20 yearsMaturity at 40 cm and 15 years

Intraspecific variability



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Y=Y 0Mb

log (Y )=log(Y 0)+ b log(M )

Body size is crucial to a number of physiological and ecological processes


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Body size is crucial to a number of physiological and ecological processes


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Individual body-sizes

Food-web structure

Ecosystem function and stability

Introduction : body size and eco-evolutionary feedbacks

Sel

ect

ion

Nic

he c

ons

truc

tion

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Cope's rule (1896)

LIFE HISTORY AND BODY SIZE EVOLUTION

Cope's rule is the tendency of lineages to increase in size over macroevolutionary time.

While the rule has been demonstrated in many instances, it does not hold true at all taxonomic levels, or in all clades.

Cope's rule necessitates that a directional selection favoring a larger size constantly operates on organisms.

Cope's rule (1896)

LIFE HISTORY AND BODY SIZE EVOLUTION

Cope's rule (1896)

1. Evolutionary benefits to being large

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Cope's rule (1896)

Kingsolver & Pfennig (Evolution 2004): a meta-analysis of selection (linear selection gradient ) on individual body size (plant and animal) and other morphological traits (wingspan, flower size...) supports the view that selection is positive on body size while other traits are at equilibrium.

(n=854, 32 species, 49 studies)


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Cope's rule (1896)


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Survival increases with body size in invertebrates, fish, birds, mammals and reptiles (Effects of predation?)

Roff 1992, p118


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Survival increases with body size in invertebrates, fish, birds, mammals and reptiles


(Sinclair et al. 2003 Nature)

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Survival increases with body size in invertebrates, fish, birds, mammals and reptiles



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Diet width increases with body size



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Diet width increases with body size


(Claessen et al. 2004, PRSB)

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Increased predator attack rate (from speed and range) and decreased handling time (from larger

manipulation and digestion capacities)


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Fecundity increases with body size in plants and ectotherms


Sexual size-dimorphism and fecundity selection in spiders.

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Sexual selection for a larger male size

The “good genes” hypothesis

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Benefits from being larger:

• Increased defense against predation (not always true) → reduced mortality selecting for longer life span (positive feedback).● Increased predation success (not always true).● Larger diet breadth.● Increased success in mating and intraspecific competition (contest sexual selection and competition).● Increased success in interference competition.● Increased resistance to starvation.


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2. Evolutionary costs to being larger

But... Small species are more abundant (EER)

Global size–density relationship plot combining mammals (red circles) and assorted ectotherms (blue squares)

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Energy requirements increase with body size

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Energy requirements increase with body size

(Oksanen et al. 1982)

Food-chain length is predicted to increase with increasing nutrient level

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Energy allocation trade-offs

Resources

Survival for future reproduction

Immediate reproduction

Where does body size come into play here?


Development time to maturity increases with body size

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● The trade-off between growth and (immediate) reproduction is “the best confirmed broad-sense phenotypic trade-off” (Stearns 1992) ● Increased body size increases survival and future fitness at the cost of reducing present fitness.

Resources

Survival for future reproduction


Maintenance and GROWTH



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● Longer generation times.● Reduced ability of populations to persist if mortality increases. ● Slower rate of evolution and, consequently, a reduced ability to adapt to sudden change. ● Extinction risk increases with body size.

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Extinction risk increases with body size

Clauset & Erwin 2008 Science

A schematic illustrating a simple cladogenetic diffusion model of species body-size evolution, where the size of a descendant species xD is related to its ancestor's size xA by a multiplicative factor λ>0 (reflecting Cope's rule).

Diffusion vs. increased extinction trade-off fits mammal body size distribution

The model reproduces the distribution of 4002 mammal species from the late Quaternary.

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Latitudinal Variation in White-Tailed Deer (Odocoileus virginiaus) (Cervidae)

• Heat loss of an organism is proportional to its surface-to-volume ratio.

• There is a selective advantage to a smaller size and associated higher body surface-to-volume ratio in warm areas, and vice versa.

• Works fine for endotherms (mammals and birds)...


Bergmann's rule: smaller is better in warm habitatsKarl Georg Lucas Christian Bergmann (1814 – 1865)

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Angiletta 2009, after Atkinson 1994.

… but also applies well to ectotherms (99% of species on earth): temperature-size rule.


Bergmann's rule: smaller is better in warm habitatsKarl Georg Lucas Christian Bergmann (1814 – 1865)

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From Vasseur & McCann Am Nat 2005

{I= f I a I T 0mc−0.25eE I T−T 0/ kTT 0

M=aM T 0mc−0.25eE M T−T 0/ kTT 0

Temperature-size rule and the thermal dependency of metabolic rates

I = ingestionM = maintenancef = realized fraction of the maximal ratesa(T

0) = intercepts of the allometric relationships,

maximum sus-tainable rates (physiological maxima) measured at T

0.

E = activation energiesk = Boltzmann constant

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Ohlberger et al. Am Nat 2011

Temperature-size rule and the thermal dependency of metabolic rates

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Other costs

Increased parasitism with increased growth rate (well documented trade-off).

Reduced agility:

Reduced swimming efficiency in faster growing individuals

Menidia menidia

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Costs from being larger:

• Increased energy requirements → reduced population densities (EER) → higher demographic stochasticity and extinction risk.

● Increased development time → reduced population growth rate and ability to tolerate increased mortality (increased extinction risk).

● Lower energetic efficiency under warming climate (see also below)

● Increased energy allocation to somatic growth and decreased allocation to maintenance (immunity, see below).


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Resources

Survival and future reproduction and growth


Increased mortality from predation selects for increased investment and reproduction at a smaller size.

Increased mortality from predators induces earlier maturity and reduced body

size in guppies (Reznick & Ghalambor CJFAS 2005)

Poecilia reticulataCrenicichla alta

3. Body size evolution in food webs : predation

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Wild-caught guppies (Reznick & Ghalambor CJFAS 2005)


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Fishery for cod (Gadus morhua) in Newfoundland and Labrador

Stock collapse was concomitant with a drop in size at maturity.

The addition of a top predator (human) at the top of the food-web induces a drop in body sizes of the (former) top predator.


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Reinforcement feedback between life history evolution and the trophic position

Instantaneous rate of natural mortality (M) of cod in the southern Gulf of St. Lawrence. Heavy horizontal line is an assumed value; circles are estimates for the periods delimited by light horizontal lines. Vertical lines are ±2 SE. Grey lines show the trend in length at 50% maturity for females (solid line) and males (dashed line).

Swain 2011

"The current high natural mortality of SGSL cod appears to be primarily a cause, rather than a consequence, of the continued early maturation in this population, now replacing fishing mortality as the agent of selection favouring early maturity."


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Lower trophic status

Small body-size

Results on cod suggest a positive feedback loop between life history evolution and the trophic position:

Evolutionary response to predation tends to increase predation mortality and thus further lower the trophic position

High predation mortality


Small size ↔ low trophic level : cause and consequence?

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Crenicichla altaRivulus hartii

Feeds on any guppy and induces reduced growth and increased reproduction in guppies

Occasionally feeds on juvenile guppy and tends to select for fast growth, but confounding effects of habitat productivity (see work by Reznick et al.)

When predators select for a smaller body size by preying on immature prey: fast growth to size refuge


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Cannibals and fishermen in Windermere pike

Cannibals select against small body size (preying on immature fish), while gillnets select against large body size (preying on mature fish)

(Carlson et al. Ecol Lett 2007)

Antagonistic selection from two predators in Windermere


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(Carlson et al. Ecol. Lett. 2007)

FISHERYdirectional selection for being smaller and growing slower

NATURALdirectional selection for being larger and growing faster (CANNIBALISM)



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Presumably increased cannibalism Decreased fishing pressure

→ At the start of the time series fishery selection was likely dominant→ At the end of the time series natural selection was likely dominant

→ Expectation of nonlinear changes in pike somatic growth rate with first a decrease and then an increase in somatic growth rate



46Growth rate responded to the dominant selective force

Nonlinear trend in individual lifetime somatic growth

corrected for the effects of basin productivity, sex,

temperature, pike numbers and perch abundance [estimated

from back-calculated length-at-age for ~14,000 individual pike

using a generalized additive mixed-effects model, GAMM,

mgcv library of R (Wood, 2006)]



(Edeline et al. PNAS 2007)

47Reproductive investment decreased in proportion to the relaxation of

fishing pressure



(Edeline et al. PNAS 2007)

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Antagonistic selection from predators and parasites In Windermere


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INTRAGUILD PREDATION + cannibalism



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(1963) 1976106 perch killed

INTRAGUILD PREDATION + cannibalism

+ antagonistic selection from pike and pathogen on perch

51By 1977, perch showed no external sign of the disease



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N=

The pike/perch ratio has increased before pathogen expansion



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Raw age and size data support the prediction that predators and pathogens induced antagonistic selection on perch body size and

life history



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BLiyc

=β 0+ f 1( Ai)+ β1 Basi+ β 2 S i+ β3T i+ β4 Phi+ β 5P i+ β6 Ph i×T i+ β7 P i×T i+ f 2(YC )+ε i



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Perch body size

Fre

quen

cy

Pike Pathogen

What may be the consequences in terms of food-web interactions?



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Paradoxically, pathogen expansion favored pike



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Pike recruitment rate increased after pathogen expansion, and the effect of perch on juvenile pike changed from – to +



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Pathogen expansion coincided with a peak in the predation pressure in both basins



Pike might have favored pathogen expansion by increasing the proportion of large, fast-growing but pathogen-sensitive perch!

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Food-web structure

Perch body size and life history

Population dynamics

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3

SelectionNiche construction

Trophic interactions


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Immature prey Mature prey

Resource

Predator 1 Predator 2

Reproduction

GrowthStage-structured biomass model

Mortality Mortality

Resource

De Roos et al. PNAS 2008

Modeling antagonistic selection from predators and parasites:Non-evolutionary, competition-mediated effects


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Case 1: competition among juvenile prey only

Invasion of an adult-specialized predator (Pa) is only successful after establishment of a juvenile-specialized predator (Pj). Pj reduces competition in J and allows increased growth and reproduction (increased A): predator-induced density-dependent life-history change in prey generates mutualism among specialized predators.

Juvenile prey

Adult prey



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Left panels (competition for resources among J): Pj mortality influences the extent to which Pj facilitates A and Pa. Right panel: competition for resources among A.



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Coexistence of 3 stage-specific predators on a 4-stage prey species. Conclusions are not sensitive to the number of prey stages and specialized predators.



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● Predators specializing on prey developmental stages that experience little competition may be able to persist only in the presence of another predator species that attacks and reduces the food limitation in the prey life stage which suffers most from scramble competition.

● Coexistence of two predator species is then possible for considerable ranges of their background mortalities for which one of them could not survive on its own.

● Just as in the Windermere example, negative effects of density-dependent competition are overwhelmed by the positive effects of size-dependent selection.



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Interspecific competition induces character displacement and favors constant size ratios

4. Body size evolution in food webs : exploitative competition

Large niche overlap Small niche overlap

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Tropical pigeons


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(Jones 1997)

4. Body size and competition



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Interaction between temperature and competition on body size

A test using 50 river fish species


71{I= f I a I T 0mc−0.25eE I T−T 0/ kTT 0

M=aM T 0mc−0.25eE M T−T 0/ kTT 0



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Edeline et al. 2013

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Edeline et al. 2013

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Edeline et al. 2013

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Production rate per unit mass f

Mortality rate per unit mass m

Predation rate from species in the interval 10-14 on a species of size 10

Evolutionary emergence of size-structured food webs(Loeuille & Loreau 2005)

Predation rate from species of size 10 on species in the interval 6-10

Interference competition rate between a species of size 10 and other species

f x= f 0 x−0.25

m x=m0 x−0.25

5. Evolutionary emergence of size-structured food-webs

Can we explain the emergence of size-structured food webs from simple, size-dependent processes?

d

s

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• The initial population consumes inorganic nutrient.

• At each time step, a mutation (new species) is produced at rate 10-6 per unit mass.

• The newly created species has a body size drawn randomly in the interval [0.8x, 1.2x], where x is the body size of the mother population.

• The initial biomass of the mutant is 10-20, which is also the threshold biomass below which any population is assumed to go extinct.

• Mutants are eliminated if they have a low fitness or through demographic stochasticity. If a mutant invades, it may coexist with other populations or eliminate some other population(s).

• The trophic position is defined as the average trophic position of prey weighted by their nutrient proportion in the diet, plus one.

• Niche width nw is defined as s2/d, ranging from 0.5 to 5. This is the degree of predator generalism.• Competition intensity is given by α

0, ranging from 0 to 0.5.



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The evolution of simulated food webs during 108 time steps for three values of niche width (nw) and competition intensity (α

0).

Community structure rapidly emerges and stabilizes.

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● Competition strength (α0) and niche width (nw, degree of generalism of predators) are

key parameters to the final community structure.

● Predation favors the emergence vertical diversity (chain length), while competition favors the emergence of horizontal diversity (omnivory and connectance).

Food-chain

No trophic structure

Distinct trophic levels

Blurred trophic structure with ubiquitous competition and omnivory



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• The variety of emerging structures is comparable with empirical observations of real ecosystems.

• Food webs with distinct trophic levels are commonly found in freshwater ecosystems.

• Food webs with a more continuous trophic structure may be more common in soil terrestrial or marine ecosystems.

Comparisons with documented food webs. Niche width and competition intensity that lead to food-web properties (chain length, connectance, ominovory...) that best fit those of seven well documented food webs (BB, Bridge Brook Lake; CB, Chesapeake Bay; CD,Coachella Desert; LR, Little Rock Lake; SM, St. Martin Island; SP, Skipwith Pond;and YE, Ythan Estuary).

Documents

Evolution of body-size - École Normale SupérieureCope's rule (1896) Kingsolver & Pfennig (Evolution 2004): a meta-analysis of selection (linear selection gradient ) on individual