Evolutionary Physiology
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1 Evolutionary Physiology Yves Desdevises Observatoire Océanologique de Banyuls Physiology Physiology: how organisms work Lot of diversity of living organisms and the different ways they function Multiple solutions to a given problem (such as living in arid environment) 3 Animals possess different physiological ways to cope with their environment Some (but not all!) are adaptations How did animal physiological traits came the way they are? "Why" organisms are designed to work in particular ways? Need to put that in an evolutionary context Investigation in an hypothetico-deductive framework ( inductive, although preliminary obervations are necessary) Evolutionary physiology 4
2 Outline Definition of adaptation Some methods to investigate physiological adaptations Examples 5 Adaptation Adaptation = trait, or set of traits, increasing fitness, then leading individuals to produce more descendants than those without this trait Trait which origin (and maintenance) is associated to an increase of functional efficiciency favoured by natural selection Product of natural selection Difficult to reveal: must be tested 6 Test of adaptation: correlation of the putative adaptative trait with an environmental variable it is supposed to adapted for Test of the appearance of the trait in the new environment (not only its presence in a given environment) 7 Adaptation acts on design, and/or reproduction Must be investigated in an evolutionary context Adaptation appears (and is maintained) in a lineage inherited from an ancestor 8
3 Example: adaptation = hydrodynamic shape 9 Adaptation/ Acclimatization/ Phenotypic plasticity Adaptation: evolution via natural selection, in a species, many generations. Modification of the genotype. Often not reversible Acclimatization: physiological, biochemical, anatomical change, in an individual, due to the exposure to a new environment. Often reversible Phenotypic plasticity: ability of a genotype to produce different phenotypes related to an environmental change, in an individual. Plasticity can be adaptive. 10 Acclimatization Adaptation Time Phenotypic plasticity 11 A component of evolution Evolution adaptation. Evolution is: Adaptation (selection) Genetic drift Structure (physics) By-product of another trait (linkage) Phylogenetic inertia (traits from ancestor) Vestigial structure Constraints (everything is not possible) Organism = trade-offs 12
4 Gradual (Darwin) or punctuational changes Gradual: many transitional steps Punctuational changes Rapid evolution in small localized populations Regulatory genes: small genetic modification = big phenotypic change Polypoïdy (plants) Combination of several elements: different structures, genes, organisms (endosymbiosis) 13 Adaptation perfection Time lag between adaptation and environmental change: imperfections, maladaptation Constraints Genetic: e.g. persistence of deleterious homozygous if heterozygous have a superior fitness Development: development influences the possibility of variations 14 Historical Adaptation arises on existing state: the possible solution may not be optimal Do not infer abusive adapative interpretations!! Spandrelism 15 Study of adaptation Theoretical approach: models, predictions Observational approach: in the field Experimental approach: alteration of potentially adaptive structure Comparative approach: correlation between structures or structure/function in several lineages (usually species), taking phylogeny into account. Comparative method/analysis 16
5 Comparative analysis Study of character correlated evolution Search for adaptations via a cross-species correlative approach Link: trait/trait or trait/environment Size / longevity Metabolism / temperature BMR / altitude 17 Example Chlorophylle b vs depth in Ostreococcus Picoalgae (< 1 µm), several strains, found at different depths Strains contain different concentrations in Chloropyll b Chl b 1,4 1,3 1,2 1,1 1,9,8,7, Depth Y = 0, ,004 * X; R^2 = 0,779 Chloropyll b = adaptation to depth? P = 0, Some key dates 1985: Felsenstein 1991: Harvey & Pagel; Brooks & McLennan Closely related species tend to be similar, and are not independent observations (pseudoreplication) Phylogenetic constraints (morphology, physiology, genetic, development,...): inertia Phylogeny = confounding variable 19 Example Hypothesis: Hb affinity is an adaptation to altitude Species Altitude Hb aff. A 5 2 B 6 6 C 8 6 D 12 7 E F G H I Hb aff. Altitude J correlation: adaptation? 20
6 Problem Phylogeny makes data non independent Species Altitude Size A 5 2 B 6 6 C 8 6 D 12 7 E F G H I J Hb aff. Altitude 21 Solution Control phylogenetic constraints Hb aff. (corrected) Altitude (corrected) no correlation Comparative analysis 22 Classical statistics requires independance of observation, then assume a "star" phylogeny, which is not true Take phylogenetic relationships into account in the analysis (at least use taxonomy) 23 Is preferred body temperature positively correlated to optimal temperature for sprint running speed in 12 species of lizards? Computation of observed correlation Test against random data simulated along the species tree S NS Observed value: r = NS 24
7 Several methods exist to take phylogeny into account in analyses Most known: independent contrasts (Felsenstein, 1985), first fully phylogenetic method Trait variation partitionning: Environment Phylogeny? 100 % of trait variation Westoby et al. (1995) 25 Models of character evolution Two basic models Brownian motion (BM): variance is a linear function of (proportional to) time = branch lengths on tree 26 Brownian motion Character variance increases with time Time Trait (x) 27 Addition of constraints (adaptive,...) and estimation of corresponding parameters: different relationships between branch lengths and character variances (e.g. Ornstein- Uhlenbeck model: OU) Divergence genetic drift (BM) BM + stabilizing selection Time 28
8 Methods Methods based on evolutionary models Independent contrasts (FIC; Felsenstein 1985) Phylogenetic generalized least squares (PGLS; Martins 1994) Phylogenetic mixed model (PMM; Lynch et al. 2004) 29 Methods with statistical bases Autoregressive method (ARM; Cheverud et al. 1985) Phylogenetic eigenvector regression (PVR; Diniz-Filho et al. 1998) 30 Independent contrasts FIC; PIC Most used method Evolutionary model = Brownian motion: genetic drift, some selective regimes Time = branch length = variance Supposes well known phylogeny, that is fully used Ideally for quantitative variables but a variable can be qualitative 31 Correlation among traits Time ρ = 0.0 ρ = 0.9 Traits (x, y) 32
9 Y Estimation of ancestral character values (weighted means) X Y Contrasts X 2 2 Y , , , , , IC Y , X IC X Contrasts must be standardised: divided by their standard deviation ( variance) 33 Contrasts can be used in various kinds of analyses: regressions, ANOVA, ANCOVA, PCA,... Regressions (through the origin, because contrasts computation eliminates the constant term) Multivariate analyses Powerful because few parameters to estimate Model testing: contrasts vs SD Slope = 0 if BM Else: transformation of branch lengths or different model (PGLS,...) 34 Improvements to take polytomies into account Recent improvement to consider data variance (Felsenstein 2008) FIC method removes phylogeny (without explicitly quantifying it) in correlation among traits Paradox to study adaptation because supposes selection ( BM) 35 Phylogenetic generalized least square regression PGLS Generalization of FIC to other models Consider phylogenetic structure of the error term (non independent observations, heteroscedasticity) Estimation of a constraint parameter α (adaptation, stabilizing selection...) adding to BM 36
10 Consider data variances The number of parameters to estimate reduces power Allows to reconstruct ancestral character states (like IC) 37 Phylogenetic eigenvector regression PVR Statistical basis (no explicit model) Transforms phylogenetic distance matrix in principal coordinates (PCs) Versatility of distance matrices: trees, reticulograms (networks), raw distances,... Allows variation partitionning and quantification of phylogenetic niche conservatism 38 Phylogenetically structured environmental variation Phylogenetic fraction (inertia) Non historical fraction, specific (adaptation,...) We can quantify the common fraction (phylogenetic niche conservatism) Environment Phylogeny? 100 % of trait variation 39 Environment E = R 2 = a+b 1 Phylogeny P = R 2 2 = b+c a b c d 100 % of the variation of Y Environment and Phylogeny = R 2 1,2 = a+b+c Unexplained variation = d b: phylogenetically-structured physiological variation 40
11 Example Variation of resting metabolic rate due to body mass, bone growth rate, and phylogeny 41 Recent development for 3 components partitioning 42 Chlorophylle b vs depth in Ostreococcus Chl b 1,4 1,3 1,2 1,1 1,9,8,7,6 P = 0, Depth Y = 0, ,004 * X; R^2 = 0,779 Raw data,3,25,2,15,1,05 0 -,05 -,1 Chl b P = 0, Depth Y = 0 + 0,003 * X; R^2 = 0,546 Independent contrasts Variation partitioning of Chl b 28% 51% 5% 16% Depth Phylogenetic variation structured by depth Phylogeny Unexplained 43 Micromonas OT95 RCC501 RCC RCC RCC RCC Surface (0-65 m) RCC344 OS1 96 RCC RCC RCC393 Deep ( m) RCC143 44
12 Concentration in Chl b is linked to depth even after controlling for phylogeny: adaptation Phylogenetic nich conservatism very important: one or a few evolutionary events followed by a radiation under the same ecological pressure 45 Design of experiments Use phylogenetic information when choosing species Do not compare only 2 distant species, because too many uncontrolled differences Avoid comparison between very contrasted clades Ideal: several pairs of closely related species with differences for the trait under study Do not a priori exclude unusual species (e.g. snake from lizards) 46 Examples Low metabolism in desert Mouse-to-elephant curve: basal metabolic rate vs body size Environmental determinants of metabolic rate Herbivory and body size in lizards 47 Low metabolic rates, low body temperatures, and ability to become torpid would be beneficial to endotherms in hot, arid environments (minimization of energetic demands), such as deserts Test in desert caprimulgid birds (Lane et al. 2004) Test in Procyonidae (Garland and Adolph, 1994) 48
13 Birds Ability to low metabolism not restricted to desert species, but widely dispersed across the phylogeny Not an adaptation in this species 49 Racoons Species with low metabolism falls outside the confident intervall computed from other species, only in phylogenetically-corrected analysis Adaptation in this species 50 Basal metabolic rate vs body size Slope of the log-log relationship: constant for all animals (value is controversial) 51 Test in bird species 52
14 Environment and metabolism in rodents 53 Herbivory and body size in lizards Hypothesis (from observations): strict herbivory in lizards requires large body size and high temperature, interpreted as constraints on thermal requirement for digestion However, most known large-bodied herbivorous lizards from a single clade, the iguanidae 54 Need to consider phylogeny: test in Liolaemidae Phylogeny: multiple origin of herbivory, very "easy" appearance of herbivory in Liolaemidae Independent contrasts: herbivory associated with low temperature! 55
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