Evolution of life history traits

Jean-François Le Galliard

CNRS, UMR 7625, Ecologie-Evolution

CNRS, UMS 3194, CEREEP – Ecotron Ile de France

Course program

Section 1 – A quick guide to life history evolution

Section 2 – Life history variation in reptiles

Section 3 – Observed reproductive strategies in the meadow viper

Section 4 – Evolution of reproductive effort and breeding frequencies

in the meadow viper

Section 1 – A quick guide to life history

evolution

Section 1 – Life history evolution

Life history evolution: A general framework based on quantitative genetics, population ecology and physiology to understand variation and adaptation in life

history strategies.

Life history strategies (demographic tactics): Ensemble of life history traits of a

given individual, population, species or higher taxa.

Life history traits: Traits that are directly involved into a characteristic equationdescribing individual fitness; such age at maturity, survival and reproduction (Roff

2002). Life history traits are coupled into a life cycle and their interactions

determine individual fitness, population growth or the species growth/competitive ability.

Standard life history traits

Pre-maturation traitsBody growth early in lifeJuvenile and sub-adult survival

Age and size at sexual maturation

Natal dispersal

Post-maturation traitsBody growth during adult lifeReproductive effort (number and quality of offspring)

Adult survival

Breeding dispersal

Post-reproductive traitsLength of post-reproductive life spanAging

http://images.google.fr

A scheme for life history evolution

Parental generation

LHS(t) = {E(LH1),E(LH2), …}

Parental generation

LHS(t) = {E(LH1),E(LH2), …}

Phenotypic variation and covariation / local conditions ?

LHS(parent,i) = {LH1(i),LH2(i), …}

LHS(offsprings,i) = {LH1(i),LH2(i), …}

Differential reproduction and inheritance ?

Differential survival ?

External conditions ?

External conditions ?Phenotypic and evolutionary changes ?

Basic concepts in life history evolution

Variation, inheritance and response to selection

Most traits vary but only part of the variation is “inherited” from one generation to another

Response to selection (S) is given by the breeder equation:

Fitness surfaces, multivariate selection and geneti c variances

Fitness surfaces can be used to describe natural and sexual selection on traitsLinear models can be used to assess the strength of selection on traits: s

Response to selection then depends on variance and covariance of traits

Example of trait variation & fitness surfaces

Le Galliard et al. Nature 2004

Another example of fitness surfaces

Preziosi & Fairbairn. Evolution 1997.

http://images.google.fr

Correlational selection & fitness surfaces

Sinervo & Svensson. Heredity 2002.

Basic concepts in life history evolution

Life-history trade-offs & external conditions act a s the main driver of life history evolution

Trade-offs result from allocation rules of limited energy and competing demands of organismal functions, such as maintenance, growth or reproduction. They result in negative phenotypic correlation between traits and can be expressed as negative genetic correlations as well (e.g. costs of reproduction).

Ecological and social conditions (e.g. background mortality at the adult stage) influence the costs and benefits of alternative life history strategies

Ecological and social conditions vary substantially in time and space

Spatial variation is important to understand the evolution of dispersal and local adaptation (see dispersal evolution)

Temporal variation is important for the evolution of phenotypic plasticity and bet-hedging (variance reduction strategy)

Illustration of a phenotypic trade-off

Roff et al. Evolution 2002

http://godofinsects.com/

Adaptive radiation and life history evolution

Schluter. TREE. 2001 Reznick. Evolution 1982

Rivulus communitiesLow predation

Low reproductive effortLong brood intervals and delayed maturity

Large embryos and smaller litters

Crenicichla communitiesHigh adult predation

High reproductive effortShort brood intervals and early maturity

Small embryos and large litters

http://images.google.fr

http://images.google.fr

Section 2 – Life history variation in reptiles

Phylogeny of squamata reptiles

Zardoya & Meyer. PNAS. 1998

TREE of LIFE web project Conrad. 2008

Squamata reptiles (lizards, snakes and amphisbenians)Diapsid amniotes close to « lizards » typeDistributed throughout the world with diverse taxa in tropics and desertic/semi-desertic habitatsSeveral thousands of species on earth

Reproductive strategies in squamate reptiles

Frequent breeding, iteroparousFlexible clutch size and reproductive effortShort life, early age at sexual maturitySmall body size

Infrequent breeding, semelparousConstant clutch size and reproductive effort

Long life, late sexual maturationLarge body size

Uta stransburianaEgg-laying species, high adult and juvenile mortalityMultiple clutches per year (2-3)Variable litter sizes and offspring sizeActive foragersSmall adult body size (< 4g) but relatively large size-independent reproductive effort

Eunectes murinusViviparous species, high adult survivalOne litter per year or every other year

Ambush predatorsLarge adult body size (<45 kg) but relatively

small size-independent reproductive effort

Income breedingActive foraging strategies

Capital breedingSit-and-wait foraging strategies

http://images.google.fr

Comparison of reproductive strategies

Shine & Charnov. Am Nat. 1992 Pike et al. Ecology 2008

Comparative analysis of snakes (16 sp) and lizards (20 sp)Extremely poor and biased taxonomic sampling

Phylogenetic signal not well resolved

Demographic tactics in reptiles

Investigation of axis of variation in demographic t raitsEarly analysis by Dunham & Miles (Am Nat 1985)

Includes 61 lizards and 10 snakes species. Traits: adult size, clutch size, age at maturity, reproductive frequencies, reproduction mode

Demographic tactics in lizards

Investigation of axis of variation in demographic t raitsLater analysis by Clobert et al. (JEB 1998)

Includes 90 lizards. Traits: adult body size, clutch size*brood frequency = annual fecundity, age at maturity, adult mortality

Iguania Scleroglossa

Typical slow-fast continuumAtypical slow-fast continuum

Fecundity variation

Reproductive trade-offs in lizards

Warner & Charnov. Am Nat. 2008

Comparative analysis of lizards (20 sp)

Large samples including several families of lizardsPhylogenetic signal accounted for

Y-axis = size-independent annual reproductive effortX-axis = offspring size

Reproductive patterns in Viperine snakes

Family Viperidae (pit vipers, true vipers and Fea’s vipers)(~ 30 genera, ~ 250 species)

Venomous snakes from Europe, Asia and AfricaOvoviparous (and also oviparous) reproduction mode

Various foraging tactics (e.g. vipers in France versus night adders in Africa)

Genus Vipera (26 species)Small vipers from North Africa to Northern Europe (Paleartic)

Inhabitants of “cool” and highly seasonal environmentsInfrequent feeding (reliance on large preys) and typical capital breeders

Delayed sexual maturation, biennal reproduction and small litter size (2-8)→ Model species with a slow and seasonal life history

Saint-Girons Bull Soc Zool Franc 1992Ineich et al. Biol J Linn Soc 2006

http://en.wikipedia.orghttp://images.google.frhttp://zoltantakacs.com/

Section 3 – Observed reproductive strategies

in the meadow viper

What do we know about demographic tactics

in true vipers ?

Short-term field studies of two viper species in Eu ropeVipera aspis (Asp viper) and Vipera berus (Common adder)

Species characterised by relatively high and constant adult survivalSmall litters of large offspring with fluctuations due to food supplies (mammals)

and climate conditions (thermal environment)Importance of body size is controversialInfrequent reproduction and storage of energyStrong costs of reproduction are postulatedJuvenile survival and growth unknown

Long-term field study of an endangered viper specie s in southern FranceVipera ursinii ursinii (Meadow viper), fieldwork by J.-P. Baron

Investigation of reproductive tactics and costs of reproductionInvestigation of juvenile performancesAnalysis of an optimisation model

Natural history of meadow vipers

Gasc et al. 1997

High altitude karstic habitats in Southern France Endangered species with ~14 populations in France

Listed under Bern Convention, Washington Convention (annex I), Habitat Directory (annex II) and fully protected in

France

Feeds on insects (crickets, grasshoppers) from June to September

Small viper species with small litter sizes (2-4)Infrequent reproduction (2-3 years)

Age at sexual maturation around 3-5 years old

Saint Girons & Naulleau 1981Baron et al. Rev Ecol 1992

Baron et al. CRAS 1996

Study site (1979-2009)

A

B

100 m

Source google.maps

Photo: J.-P. Baron

Reproductive cycles at the Mont Serein

Hibernation

May June August September

Mating

Ovulation

Gestation

Parturition

Feeding

“Breeding decisions”

Reproductive outputs

Baron et al. Rev Ecol 1992Baron et al. CRAS 1997

Summer survival and growth Winter survival

Monitoring program

Hibernation

May August September

Spring capturesLate summer

captures

Robust capture-mark recapture programPermanent and temporary marks

Morphological and individual measurementsBody length and mass, age, sex and reproductive statusStomach contentLocation, body temperature, behaviour and climate conditions

Reproductive characteristics (laboratory)Litter size, mass and successOffspring mass and length; individually marked since 1997

Tissue sampling (genetic study)

Standardised protocol (with some missing years) sin ce 1981

Age and size at sexual maturation

Baron, Le Galliard et al. In prep.

Raw data for age and size at maturation (females)

Analysis of recruitment with MCR techniques

Capture probabilities that increased linearly with age from 0.15 [0.08, 0.24] at age 1 to 0.80 [0.62, 0.92] at age 7

Constant annual survival = 0.69 [0.63, 0.74]Annual maturation probability = 0.80 [0.59, 0.92] from age 4

to age 6 years old

/* MRC data for female meadow vipers at the Mont Ventoux, France *//* Maturation data : I = immature, A = mature, 0 = not seen*//* Zone coded as group variables */0I0I0000 1 1 0;I00A0AAA 1 0 1;00000A00 1 0 1;0I000000 1 0 1;

Fat reserves and breeding decisions

Reproductive status of ca. 80 adult females (ca. 50 % NR)

threshold body condition

χ2 = 57.78, df = 1, p < 0.0001

F1,34 = 6.11, p = 0.02

Positive correlation between body condition and total litter mass

Baron, Le Galliard et al. In prep.

Breeding decisions and fat reserves

Body mass change, initial mass and breeding status of adult females

F1,58 = 224.9, p < 0.0001, n = 62

Baron, Le Galliard et al. In prep.

Non-breeding females

Breeding females

Reproductive effort: patterns of variation

Measurement of reproductive effort ?

Litter size (fecundity)Litter mass or clutch mass relative to the post-parturition body mass (RCM)Post-parturition body condition

Potential sources of variation in reproductive effo rt

Female body sizeAnnual conditionsHabitat (A and B)

Statistical tests

LMM models with fixed effects (e.g. female body size) and random effects (e.g. year)

Litter size and relative clutch mass

χ2 = 1.30, df = 1, p = 0.25, ICC = 7%, n = 116

χ2 = 2.26, df = 1, p = 0.13, ICC = 17%, n = 181

Baron, Le Galliard et al. In prep.

Scaling of energetic costs of reproduction

with energetic investment in offspring

Short-term energetic costs of reproduction (clutch mass)

Long-term energetic costs of reproduction (annual m ass loss)Baron, Le Galliard et al. In prep.

Fitness costs of reproduction

Costs of reproductionIntra-generational components

direct survival and growthfuture survival and reproduction

Intergenerational componentsdecreased growth or survival of juveniles

Example of costs of reproduction following brood si ze manipulations in blue tits

Pettifor JAE 1993

A scenario for the meadow viper

Breeding year

Energetic effort of reproduction (vitellogenesis and embryogenesis)

Increased thermoregulation

High burden of gestation and lower locomotor abilities

Direct survival cost Direct growth cost & low future reproduction

Emaciation & low future survival

Emaciation & low future reproduction

A scenario for the meadow viper

Breeding year

Offspring number

Reproductive effort

Offspring quality

Offspring survival and growth

Intra-generational effects: growth

Breeding year = growth cessation

Non-breeding year = growth opportunities

Baron, Le Galliard et al. In prep.

Intra-generational effects: survival and future

reproduction

Baron, Le Galliard et al. In prep.

* MRC data for adult meadow vipers at the Mont Ventoux, France *//* Reproductive data : 0 = not seen, R = seen reprod, N = seen not reprod,

data grouped by years*//* Zone A and B coded as groups */

R0R00R000N0000000000000000000 1 0;00N00000000000000000000000000 1 0;00R00000000000000000000000000 1 0;00R00000000000000000000000000 1 0;

000000000000000000000RNR00000 1 0;00RRNR00000000000000000000000 1 0;00000R00000000000000000000000 1 0;

0000R0R0RNR000000000000000000 1 0;

Inter-generational effects: trade-off

Baron, Le Galliard et al. In prep.

Acquisition and allocation of resources

Van Noordwjick & de Jong. Am Nat. 1986

Inter-generational effects: juvenile fitness

Baron, Le Galliard et al. Submitted.

BBirth date

Offspring condition

Juvenile growth

Birth year

Mother sizeLitter size

Offspring mass

Juvenile survival

Birth year

BBirth date

Offspring condition

Juvenile growth

Birth year

Mother sizeLitter size

Offspring mass

Juvenile survival

Birth year

AMaternal traits

Offspring traits

Juvenile performances

Annual conditions

AMaternal traits

Offspring traits

Juvenile performances

Annual conditions

Inter-generational effects: juvenile fitness

Baron, Le Galliard et al. Submitted.

Overview of observed patterns

The meadow viper is a capital breeding speciesReproductive decisions depend on body condition prior to ovulation

Infrequent reproduction in meadow vipers can not be explained by fecundity-independent costs→ Energetic investment in reproduction scales with energetic investment in offspring→ An intra-generational trade-off involves body mass loss, and therefore loss of breeding opportunities, but no direct survival costs → Another intra-generation trade-off involves body growth repression, and therefore loss of fecundity future in life→ An inter-generational trade-off involves fecundity-dependent quality reduction in offspring, which affects their future survival and growth

Temporal variation in reproductive effort weaker th an variation within a given year→ Weak variation in food acquisition→ Adaptive strategy to maintain reproductive effort rather than post-parturition body condition

Section 4 – Evolution of reproductive

strategies in meadow vipers

Life cycle and reproductive strategies

Skip breeding

Breeds

TLM

Offspringmass

Offspringnumber

Offspring quantity and quality trade-off

Gustaffsson & Sutherland Nature 1988

Quantity and quality trade-off in vipers

Le Galliard Unpub. results

Breeding frequencies in vipers

Field parameters

Intermittent breeding usually explained by large fe cundity-independent costs of reproduction

Optimisation model based on 7 age class / reproduct ion after age 7 and a reproduction-growth trade-off

Field parameters + 60% reduction in breeding survival