When studying the dynamics of trait distribution of populations in a heterogeneous environment, classical models from quantitative genetics choose to look at its system of moments, specifically the first two ones. Additionally, in order to close the resulting system of equations, they often assume that the trait distribution is Gaussian (see for instance Ronce and Kirkpatrick 2001). The aim of this paper is to introduce a mathematical framework that follows the whole trait distribution (without prior assumption) to study evolutionary dynamics of sexually reproducing populations. Specifically, it focuses on complex traits, whose inheritance can be encoded by the infinitesimal model of segregation (Fisher 1919). We show that it allows us to derive a regime in which our model gives the same dynamics as when assuming a Gaussian trait distribution. To support that, we compare the stationary problems of the system of moments derived from our model with the one given in Ronce and Kirkpatrick 2001 and show that they are equivalent under this regime and do not need to be otherwise. Moreover, under this regime of equivalence, we show that a separation bewteen ecological and evolutionary time scales arises. A fast relaxation toward monomorphism allows us to reduce the complexity of the system of moments, using a slow-fast analysis. This reduction leads us to complete, still in this regime, the analytical description of the bistable asymmetrical equilibria numerically found in Ronce and Kirkpatrick 2001. More globally, we provide explicit modelling hypotheses that allow for such local adaptation patterns to occur.
Sexual selection theory models evolution of sexual signals and preferences using simple life histories. However, life-history models predict that males benefit from increasing sexual investment approaching old age, producing age-dependent sexual traits. Age-dependent traits require time and energy to grow, and will not fully mature before individuals enter mating competition. Early evolutionary stages pose several problems for these traits. Age-dependent traits suffer from strong viability selection and gain little benefit from mate choice when rare. Few males will grow large traits, and they …
The adaptation of biological species to their environment depends on their traits. When various biological processes occur (survival, reproduction, migration, etc.), the trait distribution may change with respect to time and space. In the context of invasions, when considering the evolution of a heritable trait that encodes the dispersive ability of individuals, the trait distribution develops a particular spatial structure that leads to the acceleration of the front propagation. That phenomenon is known as spatial sorting. Many biological examples can be cited like the bush cricket in Britain…
Divergence between populations for a given trait can be driven by natural or sexual selection, interacting with migration behaviour. Mating preference for different phenotypes can lead to the emergence and persistence of differentiated populations. Dominance between alleles encoding for divergent phenotypes can interfere in such processes. Using a diploid model of trait determining both mating success and migration rate, we explored differentiation between two connected populations, assuming either co-dominance or strict dominance between alleles. The model assumes that individuals prefer mati…
Same-sex sexual behavior is ubiquitous in the animal kingdom, but its adaptive origins remain a prominent puzzle. Here I suggest the possibility that same-sex sexual behavior arises as a consequence of the competition between an evolutionary drive for a wide diversity in traits, which improves the adaptability of a species, and a drive for sexual dichotomization of traits, which promotes opposite-sex attraction and increases the rate of reproduction. A simple analytical "toy model" is proposed for describing this tradeoff. The model exhibits a number of interesting features, and suggests a sim…
The question as to why most higher organisms reproduce sexually has remained open despite extensive research, and has been called "the queen of problems in evolutionary biology". Theories dating back to Weismann have suggested that the key must lie in the creation of increased variability in offspring, causing enhanced response to selection. Rigorously quantifying the effects of assorted mechanisms which might lead to such increased variability, and establishing that these beneficial effects outweigh the immediate costs of sexual reproduction has, however, proved problematic. Here we introduce…
A proper understanding of the links between varying gene expression levels and complex trait adaptation is still lacking, despite recent advances in sequencing techniques leading to new insights on their importance in some evolutionary processes. This calls for extensions of the continuum-of-alleles framework first introduced by Kimura (1965) that bypass the classical Gaussian approximation. Here, we propose a novel mathematical framework to study the evolutionary dynamics of quantitative alleles for sexually reproducing populations under natural selection and competition through an integro-di…
We study a birth and death model for the adapatation of a sexual population to an environment. The population is structured by a phenotypical trait, and, possibly, an age variable. Recombination is modeled by Fisher's infinitesimal operator. We prove the existence of principal eigenelements for the corresponding eigenproblem. As the infinitesimal operator is 1-homogeneous but nor linear nor monotone, the general Krein-Rutman theory cannot be applied to this problem.
Natural Averaging May Complement Known Biological Constraints in Bi-parental Reproduction's Advantages Over Mono-parental in Conserving Species Quantitative Traits
In many species, females are hypothesised to obtain 'good genes' for their offspring by mating with males in good condition. However, female preferences might deplete genetic variance and make choice redundant. Additionally, high-condition males sometime produce low-fitness offspring, for example because of environmental turnover and gene-by-environment interactions (GEIs) for fitness, or because fit males carry sexually-antagonistic alleles causing them to produce unfit daughters. Here, we extend previous theory by investigating the evolution of female mate choice in a spatially explicit evol…
Molecular traits, such as gene expression levels or protein binding affinities, are increasingly accessible to quantitative measurement by modern high-throughput techniques. Such traits measure molecular functions and, from an evolutionary point of view, are important as targets of natural selection. We review recent developments in evolutionary theory and experiments that are expected to become building blocks of a quantitative genetics of molecular traits. We focus on universal evolutionary characteristics: these are largely independent of a trait's genetic basis, which is often at least par…
We consider a fitness-structured population model with competition and migration between nearest neighbors. Under a combination of large population and rare migration limits we are particularly interested in the asymptotic behavior of the total population partition on supporting trait sites. For the population without mutation on a finite trait space we obtain the equilibrium configuration and characterize the right time scale for fixation. For the model with mutation on an infinite trait space a jump process-trait substitution tree model is established on a rarer mutation time scale against t…
The branching structure of biological evolution confers statistical dependencies on phenotypic trait values in related organisms. For this reason, comparative macroevolutionary studies usually begin with an inferred phylogeny that describes the evolutionary relationships of the organisms of interest. The probability of the observed trait data can be computed by assuming a model for trait evolution, such as Brownian motion, over the branches of this fixed tree. However, the phylogenetic tree itself contributes statistical uncertainty to estimates of other evolutionary quantities, and many compa…
The prevalence of sexual reproduction ("sex") in eukaryotes is an enigma of evolutionary biology. Sex increases genetic variation only tells its long-term superiority in essence. The accumulation of harmful mutations causes an immediate and ubiquitous pressure for organisms. Contrary to the common sense, our theoretical model suggests that reproductive rate can influence initiatively the accumulation of harmful mutations. The interaction of reproductive rate and the integrated harm of mutations causes a critical reproductive rate R*. A population will become irreversibly extinct once the repro…
How the neutral diversity is affected by selection and adaptation is investigated in an eco-evolutionary framework. In our model, we study a finite population in continuous time, where each individual is characterized by a trait under selection and a completely linked neutral marker. Population dynamics are driven by births and deaths, mutations at birth, and competition between individuals. Trait values influence ecological processes (demographic events, competition), and competition generates selection on trait variation, thus closing the eco-evolutionary feedback loop. The demographic effec…
Geographic ranges of communities of species evolve in response to environmental, ecological, and evolutionary forces. Understanding the effects of these forces on species' range dynamics is a major goal of spatial ecology. Previous mathematical models have jointly captured the dynamic changes in species' population distributions and the selective evolution of fitness-related phenotypic traits in the presence of an environmental gradient. These models inevitably include some unrealistic assumptions, and biologically reasonable ranges of values for their parameters are not easy to specify. As a …
This theory seeks to define species and to explore evolutionary forces and genetic elements in speciation and species maintenance. The theory explains how speciation and species maintenance are caused by natural selection acting on non-Mendelian and Mendelian variation, respectively. The emergence and maintenance of species as groups of populations are balanced by evolutionary forces including complementary mechanisms of gene flow within and between populations at population-specific rates: sexual and asexual reproduction, recombining and nonrecombining genome regions, vertical and horizontal …
The long-term growth rate of populations in varying environments quantifies the evolutionary value of processing the information that biological individuals inherit from their ancestors and acquire from their environment. Previous models were limited to asexual reproduction with inherited information coming from a single parent with no recombination. We present a general extension to sexual reproduction and an analytical solution for a particular but important case, the infinitesimal model of quantitative genetics which assumes traits to be normally distributed. We study with this model the co…
Many biological characteristics of evolutionary interest are not scalar variables but continuous functions. Given a dataset of function-valued traits generated by evolution, we develop a practical statistical approach to infer ancestral function-valued traits, and estimate the generative evolutionary process. We do this by combining dimension reduction and phylogenetic Gaussian process regression, a nonparametric procedure which explicitly accounts for known phylogenetic relationships. We test the methods' performance on simulated function-valued data generated from a stochastic evolutionary m…
Predicting the adaptation of populations to a changing environment is crucial to assess the impact of human activities on biodiversity. Many theoretical studies have tackled this issue by modeling the evolution of quantitative traits subject to stabilizing selection around an optimum phenotype, whose value is shifted continuously through time. In this context, the population fate results from the equilibrium distribution of the trait, relative to the moving optimum. Such a distribution may vary with the shape of selection, the system of reproduction, the number of loci, the mutation kernel or …
Molecular phenotypes link genomic information with organismic functions, fitness, and evolution. Quantitative traits are complex phenotypes that depend on multiple genomic loci. In this paper, we study the adaptive evolution of a quantitative trait under time-dependent selection, which arises from environmental changes or through fitness interactions with other co-evolving phenotypes. We analyze a model of trait evolution under mutations and genetic drift in a single-peak fitness seascape. The fitness peak performs a constrained random walk in the trait amplitude, which determines the time-dep…
Adaptation often involves the acquisition of a large number of genomic changes which arise as mutations in single individuals. In asexual populations, combinations of mutations can fix only when they arise in the same lineage, but for populations in which genetic information is exchanged, beneficial mutations can arise in different individuals and be combined later. In large populations, when the product of the population size N and the total beneficial mutation rate U_b is large, many new beneficial alleles can be segregating in the population simultaneously. We calculate the rate of adaptati…
We consider a stochastic model for the evolution of a discrete population structured by a trait with values on a finite grid of the torus, and with mutation and selection. Traits are vertically inherited unless a mutation occurs, and influence the birth and death rates. We focus on a parameter scaling where population is large, individual mutations are small but not rare, and the grid mesh for the trait values is much smaller than the size of mutation steps. When considering the evolution of the population in a long time scale, the contribution of small sub-populations may strongly influence t…
We present a mathematical simplification for the evolutionary dynamics of a heritable trait within a two-sex population. This trait is assumed to control the timing of sex-specific life-history events, such as the age of sexual maturity and end of female fertility, and each sex has a distinct fitness tradeoff associated with the trait. We provide a formula for the fitness landscape of the population and show a natural extension of the result to an arbitrary number of heritable traits. Our method can be viewed as a dynamical systems generalisation of the Price Equation to include two sexes{, ag…
We study a general setting of neutral evolution in which the population is of finite, constant size and can have spatial structure. Mutation leads to different genetic types ("traits"), which can be discrete or continuous. Under minimal assumptions, we show that the marginal trait distributions of the evolutionary process, which specify the probability that any given individual has a certain trait, all converge to the stationary distribution of the mutation process. In particular, the stationary frequencies of traits in the population are independent of its size, spatial structure, and evoluti…
Evaluating Phylogenetic Comparative Methods under Reticulate Evolutionary Scenarios
Texas A&M University（德克萨斯农工大学）；Lakehead University（湖首大学）；IISD Experimental Lakes Area（国际可持续发展研究所实验湖区）；The Institute for Computational and Experimental Research in Mathematics, Brown University（布朗大学计算与实验数学研究所）；RIKEN iTHEMS（理化学研究所创新智能数学科学中心）
The Tangled Nature Model of biological and cultural evolution features interacting agents which compete for limited resources and reproduce in an error prone fashion and at a rate depending on the `tangle' of interactions they maintain with others. The set of interactions linking a TNM individual to others is key to its reproductive success and arguably constitutes its most important property. Yet, in many studies, the interactions of an individual and those of its mutated off-spring are unrelated, a rather unrealistic feature corresponding to a point mutation turning a giraffe into an elephan…
In sexual populations, selection operates neither on the whole genome, which is repeatedly taken apart and reassembled by recombination, nor on individual alleles that are tightly linked to the chromosomal neighborhood. The resulting interference between linked alleles reduces the efficiency of selection and distorts patterns of genetic diversity. Inference of evolutionary history from diversity shaped by linked selection requires an understanding of these patterns. Here, we present a simple but powerful scaling analysis identifying the unit of selection as the genomic "linkage block" with a c…
We consider a simple mathematical model of gradual Darwinian evolution in continuous time and continuous trait space, due to intraspecific competition for common resource in an asexually reproducing population in constant environment, while far from evolutionary stable equilibrium. The model admits exact analytical solution. In particular, Gaussian distribution of the trait emerges from generic initial conditions.
C$_4$ photosynthesis has independently evolved from the ancestral C$_3$ pathway in at least 60 plant lineages, but, as with other complex traits, how it evolved is unclear. Here we show that the polyphyletic appearance of C$_4$ photosynthesis is associated with diverse and flexible evolutionary paths that group into four major trajectories. We conducted a meta-analysis of 18 lineages containing species that use C$_3$, C$_4$, or intermediate C$_3$-C$_4$ forms of photosynthesis to parameterise a 16-dimensional phenotypic landscape. We then developed and experimentally verified a novel Bayesian a…
In evolutionary dynamics, a key measure of a mutant trait's success is the probability that it takes over the population given some initial mutant-appearance distribution. This "fixation probability" is difficult to compute in general, as it depends on the mutation's effect on the organism as well as the population's spatial structure, mating patterns, and other factors. In this study, we consider weak selection, which means that the mutation's effect on the organism is small. We obtain a weak-selection perturbation expansion of a mutant's fixation probability, from an arbitrary initial config…
The distribution and heritability of many traits depends on numerous loci in the genome. In general, the astronomical number of possible genotypes makes the system with large numbers of loci difficult to describe. Multilocus evolution, however, greatly simplifies in the limit of weak selection and frequent recombination. In this limit, populations rapidly reach Quasi-Linkage Equilibrium (QLE) in which the dynamics of the full genotype distribution, including correlations between alleles at different loci, can be parameterized by the allele frequencies. This review provides a simplified exposit…
Many biological characteristics of evolutionary interest are not scalar variables but continuous functions. Here we use phylogenetic Gaussian process regression to model the evolution of simulated function-valued traits. Given function-valued data only from the tips of an evolutionary tree and utilising independent principal component analysis (IPCA) as a method for dimension reduction, we construct distributional estimates of ancestral function-valued traits, and estimate parameters describing their evolutionary dynamics.
Horizontal transfer (HT) of heritable information or `traits' (carried by genetic elements, endosymbionts, or culture) is widespread among living organisms. Yet current ecological and evolutionary theory addressing HT is limited. We present a modeling framework for the dynamics of two populations that compete for resources and exchange horizontally (transfer) an otherwise vertically inherited trait. Competition influences individual demographics, affecting population size, which feeds back on the dynamics of transfer. We capture this feedback with a stochastic individual-based model, from whic…
The adaptation of large asexual populations is hampered by the competition between independently arising beneficial mutations in different individuals, which is known as clonal interference. Fisher and Muller proposed that recombination provides an evolutionary advantage in large populations by alleviating this competition. Based on recent progress in quantifying the speed of adaptation in asexual populations undergoing clonal interference, we present a detailed analysis of the Fisher-Muller mechanism for a model genome consisting of two loci with an infinite number of beneficial alleles each …
When a population inhabits an inhomogeneous environment, the fitness value of traits can vary with the position in the environment. Gene flow caused by random mating can nevertheless prevent that a sexually reproducing population splits into different species under such circumstances. This is the problem of sympatric speciation. However, mating need not be entirely random. Here, we present a model where the individually advantageous preference for partners of high fitness can lead to genetic clustering as a precondition for speciation. In simulations, in appropriate parameter regimes, our mode…
To examine the co-evolution of quantitative traits in hosts and parasites, we present and study a co-evolutionary model of a social parasite-host system that incorporates (1) ecological dynamics that feed back into their co-evolutionary outcomes; (2) variation in whether the parasite is obligate or facultative; and (3) Holling Type II functional responses between host and parasite, which are particularly suitable for social parasites that face time costs for host location and its social manipulation. We perform local and global analyses for the co-evolutionary model and the corresponding ecolo…
The evolutionary spread of cheater strategies can destabilize populations engaging in cooperative behaviors, thus demonstrating that evolutionary changes can have profound implications for populations dynamics. At the same time, the relative fitness of cooperative traits often depends upon population density, thus leading to the potential for bidirectional coupling between population density and the evolution of a cooperative trait. Despite the potential importance of these eco evolutionary feedback loops, they have not yet been demonstrated experimentally in social species and their ecologica…
Statistical analysis of alignments of large numbers of protein sequences has revealed "sectors" of collectively coevolving amino acids in several protein families. Here, we show that selection acting on any functional property of a protein, represented by an additive trait, can give rise to such a sector. As an illustration of a selected trait, we consider the elastic energy of an important conformational change within an elastic network model, and we show that selection acting on this energy leads to correlations among residues. For this concrete example and more generally, we demonstrate tha…
Mutations in a microbial population can increase the frequency of a genotype not only by increasing its exponential growth rate, but also by decreasing its lag time or adjusting the yield (resource efficiency). The contribution of multiple life-history traits to selection is a critical question for evolutionary biology as we seek to predict the evolutionary fates of mutations. Here we use a model of microbial growth to show there are two distinct components of selection corresponding to the growth and lag phases, while the yield modulates their relative importance. The model predicts rich popu…
The phenomenon of preadaptation, or exaptation (wherein a trait that originally evolved to solve one problem is co-opted to solve a new problem) presents a formidable challenge to efforts to describe biological phenomena using a classical (Kolmogorovian) mathematical framework. We develop a quantum framework for exaptation with examples from both biological and cultural evolution. The state of a trait is written as a linear superposition of a set of basis states, or possible forms the trait could evolve into, in a complex Hilbert space. These basis states are represented by mutually orthogonal…
