Nature, causes and evolutionary significance of variation Jean-François Le Galliard M1 – Evolutionary Ecology - 2017
Preamble 1. Kinds of variation 2. Life history traits 3. Case study
Preamble: hierarchical structure of life
Increasing levels of biological and spatial complexity Interdependencies and feedbacks (rules of thermodynamics, genetics, ecology and evolution) Emergent properties and collective dynamics Organisms: self-organized beings or « individuals » that exhibit the properties of life (self replication, growth-development, inheritance)
Preamble: growth and development of organisms
Fig. 3. Continuous suboptimal PD0325901 treatment prevents zebrafish BRAFCFC phenotypes. (A) Wildtype embryos were injected with human BRAFWT, the kinase-activating and most common CFC allele BRAFQ257R, or the kinase-inactivating BRAFG596V, and imaged at the indicated developmental time post-fertilisation. (B) Images of untreated control zebrafish (top panel) and a zebrafish expressing the kinase-inactivating BRAFG596V allele under the melanocyte-specific mitfa promoter (bottom panel). Insert image depicts a high-magnification image of ectopic melanisation and nevi formation. (C) Continuous treatment of BRAFWT- and BRAFCFCinjected embryos with a suboptimal dose (0.2 μM) of PD0325901 from 4 hpf through 4 dpf. (D) Western blot of 10-hpf wild-type [uninjected (Un)] or BRAFCFC embryos treated with 0.2 μM of PD0325901 from 4 hpf, and immunostained with anti-phospho-ERK1/2 and anti-ERK1/2 antibodies.
Preamble: phenotypes are variable and complex Variation and polymorphism
Development and growth
Integration and syndromes
Phenotypes: “visible” characteristics/traits of an organism/individual including morphology, physiology, behavior. Variation: occurrence of different states-trait values, Polymorphism: occurrence of different morphs or forms Phenotypic integration: correlation among several functionally-related traits
Preamble: examples of inter-individual variation “Variation among individuals in (average) phenotype in a specified environment at a given age after controlling for differences due to sex”
From Fitze & Le Galliard, Ecology Letters, 2008
Preamble: individual variation at one life stage
Significant variation among neonates (ICC = 70%) with broad-sense heritability of ca. 40% From Le Galliard et al., Nature, 2004
Preamble: individual variation across age stages
Significant individual variation in growth rate and asymptotic body size From Baron, Tully & Le Galliard, Oecologia, 2010
Preamble: individual variation in flexible traits
Correlated individual variation in intercept and slope (positive correlation) From Artacho, Jouanneau & Le Galliard, Phys. Biochem. Zool.
Preamble: phenotypic integration in lizards
Preamble: classical ecology tends to ignore variation Population biology
Kausrud et al., Nature, 2004
Neutral theory of biodiversity
http://www.nature.com/scitable/knowledge/library/neutral -theory-of-species-diversity-13259703
Community ecology
http://csls-text2.c.u-tokyo.ac.jp/inactive/12_02.html
Ecosystem ecology
Preamble: individual behavior can influence macro-ecology
From Duckworth & Badyaev, Proc. Nat. Acad. Sci. USA, 2007
Preamble: functional properties are relevant at all scales Population biology
Community ecology
Kinlan & Gaines, Ecology, 2003
Niche theory
Trait-based ecosystem models
(c) Barry Sinervo
Allison, Ecol. Letters, 2012 Araujo et al., Ecol. Letters, 2013
Preamble: agenda of evolutionary ecology A discipline at the cross-road between evolutionary biology and ecology An approach of evolutionary biology that accounts for the “ecological theater”, i.e. interactions between organisms and their environment and social / trophic / non-trophic interactions among organisms A sub-discipline of ecology which takes into account the evolutionary history and evolvability of organisms and the interaction between ecological and evolutionary processes
1. Three kinds of variation 1. 2. 3. 4.
Genetic variation Environmental variation Genotype-By-Environment interaction Comprehensive view and more complexity
1) Genetic variation • Genetic variation consists of differences among individuals that are encoded in the genome and transmitted from parents to offspring.
Chromosome: long DNA molecule that contain many genes
Locus: location of a gene along a chromosome
PTC = Phenylthiocarbamide
Alleles: variants of a given gene
Genotype: in a diploid organism, the pairs of alleles at one or a given set of loci
With tools of population genetics, we can measure the frequencies of alleles and genotypes, and analyze how they vary through time and across different regions.
Example: single genes can change mating system-behavior
Prairie voles: a rodent species characterised by lifelong bonds and a monogamous mating system with highly “social” behaviors
Montane voles: a rodent species characterised by promiscuity and a solitary life style (typical of the taxonomic group) with more aggressive social interactions
Example: single genes can change mating system-behavior The two species differ in spatial binding pattern with V1a receptors and sensitivity to AVP release in the brain
V1a = Vassopressin receptor 1A
Mices engineered with V1aR from prairie voles respond the same to AVP than this species
CSF = placebo, AVP = injection of AVP in the brain
Arginin vasopressin (AVP): a peptidic hormone released by hypophyse and regulating water balance and arterial blood pressure + has also direct brain effects on social behaviors Young LJ, Nilsen R, Waymire KG, MacGregor GR, Insel TR, 1999. Increased affiliative response to vasopressin in mice expressing the V-1a receptor from a monogamous vole. Nature 400:766-768.
Example: single genes can change mating system-behavior Male prairie voles vary in their mating-social style
Typical monogamous males with a resident territory and stable pair bonds Typical wandering males with a overlapping territories Same morphology Trend for smaller territories in resident than wandering males Spatial patterns of V1aR density with little variation in limbic regions (Vpall and LS) and strong variation in cortex and dorsal thalamus
Ophir AG, Wolff JO, Phelps SM, 2008. Variation in neural V1aR predicts sexual fidelity and space use among male prairie voles in semi-natural settings. Proc Natl Acad Sci U S A 105:1249-1254.
Example: single genes can change mating system-behavior High V1aR expression in posterior cortex associated with successful wanderer and more sexual fidelity – residents have high values High V1aR expression in laterodorsal thalamus associated with successful wanderer and more sexual fidelity as well – residents have high values
Results more or less in accordance with patterns of variation seen across species IPF = intrapair fertilisation, EPF = extrapair fertilisation
Example: single genes can change mating system-behavior Quantification of microsatellite length polymorphism at V1aR gene locus in male prairie voles Genetic polymorphism in V1aR microsatellite length not correlated with social monogamy Genetic polymorphism in V1aR microsatellite length correlated with genetic monogamy: males with smaller microsatellites have more sexual partners (in accordance with lab based studies) Solomon NG, Richmond AR, Harding PA, Fries A, Jacquemin S, Schaefer RL, Lucia KE, Keane B, 2009. Polymorphism at the avpr1a locus in male prairie voles correlated with genetic but not social monogamy in field populations. Molecular Ecology 18:4680-4695.
2) Environmental variation • Environmental variation consists of differences among individuals due to exposure to different environments. • One way environments can influence phenotype is by altering gene expression.
Daphnia (waterfleas) are tiny Cladocera crustaceans spread in ponds worldwide
Genetically identical individuals can change morphology, physiology, and behavior when exposed to different environments – for exemple when juveniles smell predators… What happens then is that the expression level of many genes is altered
Environmentally dependent polyphenism in various taxa. (a) The water flea Daphnia longicephala develops protective crests and tail spines in response to its water bug predator, Notonecta. Differences in coat colour and texture are produced in Arctic fox (Vulpes lagopus) in response to seasonal change. (b) When a bluehead wrasse (Thalassoma bifasciatum) male (blue morph) is removed from his harem, a female (yellow morph) will change phenotype completely and become a male. The gaudy commodore, Precis octavis, is seasonally dimorphic. In the wet season, it has an orange wing and in the dry season the wings are bluish purple in colour. Onthophagus nigriventris dung beetles metamorphose as horned major males or hornless sneaker males in response to ample or insufficient larval feeding resources, respectively. (c) The tiger salamander (Ambystoma tigrinum) only metamorphoses if its aquatic environment becomes uninhabitable. Larval nutrition determines major and minor worker development in Pheidole rhea. The morphology of white water-buttercup (Ranunculus aquatilis) leaves depends on their environment. Submerged leaves are branched into 20 or more thread-like segments. Floating or exposed leaves are scalloped.
Moczek AP, Sultan S, Foster S, Ledón-Rettig C, Dworkin I, Nijhout HF, Abouheif E, Pfennig DW, 2011. The role of developmental plasticity in evolutionary innovation. Proc R Soc B-Biol Sci 278:2705-2713.
Example: developmental plasticity and hormones
Maternal effects: influence of the maternally provided environment on offspring phenotype Dufty AM, Clobert J, Moller AP, 2002. Hormones, developmental plasticity and adaptation. Trends Ecol Evol 17:190-196.
Example: maternal effects
With odors of predators during gestation (P+)
Without odors of predators during gestation (P-)
Bestion E, Teyssier A, Aubret F, Clobert J, Cote J, 2014. Maternal exposure to predator scents: offspring phenotypic adjustment and dispersal. Proc R Soc B-Biol Sci 281.
Example: condition-dependence of dispersal behavior
Le Galliard J-F, Rémy A, Ims RA, Lambin X, 2012. Patterns and processes of dispersal behaviour in arvicoline rodents. Molecular Ecology 21:505-523.
Example: silver-spoon effects in rodents
Habitat manipulation
Litter size manipulation
Example: silver-spoon effects in rodents High habitat quality (1) Influences positively female fitness (2) Promotes natal philopatry in females (3) Accelerates settlement behavior in females (4) No effect on male dispersal Increased litter size (1) Influences consistently structural size but not female fitness (2) Has no effect on natal dispersal and movement behavior (3) Does not interact with habitat quality
Permanent effects of peri-natal conditions on body size but reproduction and survival more importantly influenced by direct effects of habitat Phenotypic engineering (litter size manipulation)
From Rémy, Le Galliard et al., J. Anim Ecol., 2011
2) Environmental variation • Environmental variation is often NOT inherited, or it can be passed from mother to offspring over one or a few generations, but not many. – Inheritance over one or a few generations happens for example when epigenetic factors control the change in gene expression (or mRNA translation) – These epigenetic factors can be inherited over one or a few generations, but not many; and for many species and genes they are reset in the offspring.
A heritable epigenetic variant !! (a) Typical flowers of common toadflax (Linaria vulgaris). (b) Radially symmetrical flowers from a plant of the same species. This variant was described by Linnaeus over 250 years ago and has been inherited since (Paun et al. 2010). It is caused by epigenetic marks that prevent expression of a gene called Lcyc (Cubas et al. 1999). From Grant-Downton and Dickinson (2006)
Example: trans-generational epigenetic inheritance
Trans-generational epigenetic inheritance: transgenerational transmission of information without change in nucleotides sequences of DNA from parents to offspring
3) Genotype-by-Environment interaction • Genotype-by-Environment interactions consists of differences among individuals, encoded in the genome, in the way the environment influences phenotype. Genetic variation No environmental variation
Environmental variation No genetic variation
Genotype 1 Phenotype (size, color, shape, behavior…)
Genotype 2
Environment 1
Environment 2
Genotype 1 Genotype 2
Environment 1
Environment 2
3) Genotype-by-Environment interaction • Genotype-by-Environment interactions consists of differences among individuals, encoded in the genome, in the way the environment influences phenotype. Environmental AND genetic variation No Genotype-by-Environment interaction
Genotype-by-Environment interaction Genotype 1
Genotype 1 Phenotype (size, color, shape, behavior…)
Genotype 2
Environment 1
Environment 2
Phenotype (size, color, shape, behavior…)
Genotype 2
Environment 1
Environment 2
• Example of Genotype-by-Environment interaction in humans Encodes expression of gene for serotonin transporter, which mops up neurotransmitter serotonin after neurons used it. Genotype ll expresses more, which erases the memory of the early environment
• Example of Genotype-by-Environment interaction in humans Encodes expression of gene for serotonin transporter, which eliminate neurotransmitter serotonin after neurons used it. Genotype ll expresses more, which erases the memory of the early environment
• Example of Genotype-by-Environment interaction in humans Encodes expression of gene for serotonin transporter, which mops up neurotransmitter serotonin after neurons used it. Genotype ll expresses more, which erases the memory of the early environment
In many reptiles, such as this leopard gecko, the offspring gender is determined both by genotype and environment (temperature) Eggs incubated at intermediate temperature are more likely to become males!
Each line is the reaction norm of the offspring sex ratio of a given father (with distinct genotype) in response to different incubation temperatures. The reaction norms cross: G x E interaction!
• The reaction norm gives a measure of phenotypic plasticity: how different the phenotype can develop in different environments.
Black individuals vary in their sensitivity (plasticity) to heat shock Black mutants may turn green, if they are heatshocked just before molting. This is plasticity
• The tobacco hornworm shows phenotypic plasticity: under different environmental conditions, different phenotypes develop. • The tobacco hornworm shows heritable variation in phenotypic plasticity.
• Can greater or lesser plasticity evolve by natural selection? Every generation, the most sensitive caterpillars are selected in one line, and the least sensitive are selected in another
By so doing, we cause evolution of a steep stepwise reaction norm in one line, and evolution of a rather flat reaction norm in the other
4) Comprehensive view and more complexity
Danchin E, 2013. Avatars of information: towards an inclusive evolutionary synthesis. Trends Ecol Evol 28:351-358.
Conclusions about the three kinds of individual variation • Because of their heritable component, genetic variation and genotypeby-environment interaction are raw material for evolution by natural selection. • Despite its ubiquity, environmental variation supplies no raw material for evolution. • It has now become clear that variation and information can be transmitted in non-genetic ways, including epigenetic and nonepigenetic mechanisms, which tends to complexify the picture and make it possible for evolutionary dynamics despite no or little genetic variation
What we have learned (1) • What genetic variation, environmental variation, and Genotype-byEnvironment interaction are, and the differences between them. • How phenotypic plasticity can evolve, when a phenotypic trait is affected by a Genotype-by-Environment interaction.
2. Life history traits 1. Life history evolution and variation 2. Patterns and speed of life history variation
1) Life history evolution and variation 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 equation describing 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 and the species growth or competitive ability. Questions: how do life history traits evolve ? can we predict the evolutionary dynamics of life history traits ? what are the drivers of natural variation in life history ?
Examples of life history traits Pre-maturation traits Body growth early in life Juvenile and sub-adult survival Age and size at sexual maturation Natal dispersal Post-maturation traits Body growth during adult life Reproductive effort (number and quality of offspring) Semelparity versus iteroparity Adult survival Post-reproductive traits Length of post-reproductive life span Aging
Optimization and life history trade-offs Optimization: under certain strict assumptions (e.g., no density and frequency dependence), we can predict the evolution of life history traits by searching for fitness optima (the “optimization principle”).
Life history trade-offs: constraints on optimisation of multiple life history traits such that increasing the values of one trait leads to lower values of the other trait due to “constraints” such as mechanical, physical or thermodynamic rules (e.g., energy allocation rules). Examples include costs of early growth, costs of reproduction, number versus mass of offspring, early life versus late life performances
The growth – reproduction life history trade-off
http://godofinsects.com/
Roff DA, Mostowy S, Fairbairn DJ, 2002. The evolution of trade-offs: Testing predictions on response to selection and environmental variation. Evolution 56:84-95.
Allocation and acquisition rules: difficulties
A
R
S
van Noordwijk AJ, de Jong G, 1986. Acquisition and allocation of resources: their influence on variation in life history tactics. Am Nat 128:137-142.
Costs of reproduction in birds revealed by clutch size manip.
Higher reproductive effort implies No change in adult survival Increased number of fledglings but number of recruits maximized at ca. initial clutch size Lower clutch size one year later Clutch size of offspring maximized at ca. -1 clutch size
Gustafsson L, Sutherland WJ, 1988. The costs of reproduction in the collared flycatcher Ficedula albicollis. Nature 335:813-815.
Life history trade-offs revealed by egg size manipulation
Sinervo B, Doughty P, Huey RB, Zamudio K, 1992. Allometric engineering : a causal analysis of natural selection on offspring size. Science 258:1927-1930.
2) Patterns and speed of life history variation
2) Life history continuum in plants
Roberto Salguero-Gómez et al. PNAS 2016;113:230-235
PC1: T: generation time, γ: rate of progressive growth, ϕ: sexual reproduction, H: longevity, L: age at maturation PC2: S: iteroparity (frequency of reprod. during life), R0: net reproductive rate, ρ: retrogressive growth
2) Life history continuum in mammals Larger species are characterised by • higher maximum lifespan • lower annual reproductive outputs • delayed age at maturation • longer generation time
Turbill C, Bieber C, Ruf T, 2011. Hibernation is associated with increased survival and the evolution of slow life histories among mammals. Proc R Soc B-Biol Sci 278:3355-3363.
2) Life history continuum in mammals
After body mass scaling is accounted for, we still observe a negative correlation between reproductive output and maximum lifespan/annual survival.
2) Life history continuum in reptiles
Frequent breeding, iteroparous Flexible clutch size and reproductive effort Short life, early age at sexual maturity Small body size
Income breeding Active foraging strategies Uta stransburiana Egg-laying species, high adult and juvenile mortality Multiple clutches per year (2-3) Variable litter sizes and offspring size Active foragers Small adult body size (< 4g) but relatively large size-independent reproductive effort
Infrequent breeding, semelparous Constant clutch size and reproductive effort Long life, late sexual maturation Large body size
Capital breeding Sit-and-wait foraging strategies Eunectes murinus Viviparous species, high adult survival One litter per year or every other year Ambush predators Large adult body size (
