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The coevolution of social learning and sensitivity to changing environments

AO_SCPLOWBSTRACTC_SCPLOWThere is widespread agreement that social and individual learning are adaptations to varying environments. However, existing theory assumes that organisms cannot detect changes in the environment and instead adapt to averages. This paper develops the first analytical model that allows for the simultaneous coevolution of socially learned traditions, reliance on social learning, and signal detection for environmental change. There are numerous conditions under which detection can be stable once common but cannot invade the population when rare. When signal detection is maintained by selection, it always leads to pure separating equilibria at which organisms always learn individually when they believe the environment has recently changed and otherwise always learn socially. Detection can increase mean fitness at equilibrium, but it may also reduce it.

evolutionary biology

Bayesian Analysis of Evolutionary Divergence with Genomic Data Under Diverse Demographic Models

We present a new Bayesian method for estimating demographic and phylogenetic history using population genomic data. Several key innovations are introduced that allow the study of diverse models within an Isolation with Migration framework. For the Markov chain Monte Carlo (MCMC) phase of the analysis, we use a reduced state space, consisting of simple coalescent trees without migration paths, and a simple importance sampling distribution without demography. Migration paths are analytically integrated using a Markov chain as a representation of genealogy. The new method is scalable to a large number of loci with excellent MCMC mixing properties. Once obtained, a single sample of trees is used to calculate the joint posterior density for model parameters under multiple diverse demographic models, without having to repeat MCMC runs. As implemented in the computer program MIST, we demonstrate the accuracy, scalability and other advantages of the new method using simulated data and DNA sequences of two common chimpanzee subspecies: Pan troglodytes troglodytes (P. t.) and P. t. verus.

Evolutionary Biology

Effect of error and missing data on population structure inference using microsatellite data

Missing data and genotyping errors are common in microsatellite data sets. We used simulated data to quantify the effect of these data aberrations on the accuracy of population structure inference. Data sets with complex, randomly-generated, population histories were simulated under the coalescent. Models describing the characteristic patterns of missing data and genotyping error in real microsatellite data sets were used to modify the simulated data sets. Accuracy of ordination, tree-based, and model-based methods of inference was evaluated before and after data set modifications. The ability to recover correct population clusters decreased as missing data increased. The rate of decrease was similar among analytical procedures, thus no single analytical approach was preferable. For every 1% of a data matrix that contained missing genotypes, 2-4% fewer correct clusters were found. For every 1% of a matrix that contained erroneous genotypes, 1-2% fewer correct clusters were found using ordination and tree-based methods. Model-based procedures that minimize the deviation from Hardy-Weinberg equilibrium in order to assign individuals to clusters performed better as genotyping error increased. We attribute this surprising result to the inbreeding-like nature of microsatellite genotyping error, wherein heterozygous genotypes are mischaracterized as homozygous. We show that genotyping error elevates estimates of the level of genetic admixture. Overall, missing data negatively impact population structure inference more than typical genotyping errors.

evolutionary biology

Topological features of gene regulatory networks predict patterns of natural diversity in environmental response

Molecular interactions affect the evolution of complex traits. For instance, adaptation may be constrained by pleiotropic or epistatic effects, both of which will be reflected in the structure of molecular interaction networks. To date, empirical studies investigating the role of molecular interactions in phenotypic evolution have been idiosyncratic, offering no clear patterns. Here, we investigated the network topology of genes putatively involved in local adaptation to two abiotic stressors--drought and cold--in Arabidopsis thaliana. Our findings suggest that the gene-interaction topologies for both cold and drought stress response are non-random, with genes that show genetic variation in drought response (GxE) being significantly more peripheral and cold response genes being significantly more central than genes not involved in either response. We suggest that the observed topologies reflect different constraints on the genetic pathways involved in the assayed phenotypes. The approach presented here may inform predictive models linking genetic variation in molecular signaling networks with phenotypic variation, specifically traits involved in environmental response.\n\nSignificance StatementOur study focuses on genes whose transcriptional activity exhibits genetic variation in response to the environment, or \"GxE.\" GxE is a widely observed phenomenon of critical importance to understanding the genotype-to-phenotype map, the evolution of natural populations, medical genetics, population response to climate change, and agricultural improvement. We investigated expression GxE in plant responses to two abiotic cues: cold and drought. We found that genes showing genetically variable response to cold stress are centrally located in regulatory networks whereas genes showing genetically variable response to drought stress are peripherally located in regulatory networks. This result suggests that selection is presented with vastly different mutational landscapes for shaping evolutionary or breeding response to these two important climatic factors

evolutionary biology

Grow with the flow: a latitudinal cline in physiology is associated with more variable precipitation in Mimulus cardinalis

Local adaptation is commonly observed in nature: organisms perform well in their natal environment, but poorly outside it. Correlations between traits and latitude, or latitudinal clines, are among the most common pieces of evidence for local adaptation, but identifying the traits under selection and the selective agents is challenging. Here, we investigated a latitudinal cline in growth and photosynthesis across 16 populations of the perennial herb Erythranthe cardinalis (Phrymaceae). Using machine learning methods, we identify interannual variation in precipitation as a likely selective agent: Southern populations from more variable environments had higher photosynthetic rates and grew faster. We hypothesize that selection may favor a more annualized life history - grow now rather than save for next year - in environments where severe droughts occur more often. Thus our study provides insight into how species may adapt if Mediterranean climates become more variable due to climate change.

evolutionary biology

Evolutionary rescue in randomly mating, selfing, and clonal populations

Severe environmental change can drive a population extinct unless the population adapts in time to the new conditions (\"evolutionary rescue\"). How does bi-parental sexual reproduction influence the chances of population persistence compared to clonal reproduction or selfing? In this paper, we set up a one-locus two-allele model for adaptation in diploid species, where rescue is contingent on the establishment of the mutant homozygote. Reproduction can occur by random mating, selfing, or clonally. Random mating generates and destroys the rescue mutant; selfing is efficient at generating it but at the same time depletes the heterozygote, which can lead to a low mutant frequency in the standing genetic variation and also affects the establishment probability of the mutation. Due to these antagonistic effects, we find a non-trivial dependence of population survival on the rate of sex/selfing, which is strongly affected by the dominance coefficient of the mutation before and after the environmental change. Importantly, since mating with the wildtype breaks the mutant homozygote up, a slow decay of the wildtype population size can impede rescue in randomly mating populations.

evolutionary biology

Pervasive adaptation in Plasmodium-interacting proteins in mammals

The protozoan genus Plasmodium causes malaria in dozens of mammal species, including humans, non-human primates, rodents, and bats. In humans, Plasmodium infections have caused hundreds of millions of documented deaths, imposing strong selection on certain populations and driving the emergence of several resistance alleles. Over the deep timescale of mammalian evolution, however, little is known about host adaptation to Plasmodium. In this work, we expand the collection of known Plasmodium-interacting-proteins (PIPs) in mammalian hosts from ~10 to 410, by manually curating thousands of scientific abstracts. We use comparative tests of adaptation to show that PIPs have experienced >3 times more positive selection than similar mammalian proteins, consistent with Plasmodium as a major and long-standing selective pressure. PIP adaptation is strongly linked to gene expression in the blood, liver, and lung, all of which are clinically relevant tissues in Plasmodium infection. Interestingly, we find that PIPs with immune functions are especially enriched for additional interactions with viruses or bacteria, which together drive a 3.7-fold excess of adaptation. These pleiotropic interactions with unrelated pathogens, along with pressure from other Plasmodium-like Apicomplexan parasites, may help explain the PIP adaptation we observe in all clades of the mammalian tree. As a case study, we also show that alpha-spectrin, the major membrane component of mammalian red blood cells, has experienced accelerated adaptation in domains known to interact specifically with Plasmodium proteins. Similar interactions with Plasmodium-like parasites appear to have driven substantial adaptation in hundreds of host proteins throughout mammalian evolution.

evolutionary biology

The hidden elasticity of avian and mammalian genomes

Genome size in mammals and birds shows remarkably little interspecific variation compared to other taxa. Yet, genome sequencing has revealed that many mammal and bird lineages have experienced differential rates of transposable element (TE) accumulation, which would be predicted to cause substantial variation in genome size between species. Thus, we hypothesize that there has been co-variation between the amount of DNA gained by transposition and lost by deletion during mammal and avian evolution, resulting in genome size homeostasis. To test this model, we develop a computational pipeline to quantify the amount of DNA gained by TE expansion and lost by deletion over the last 100 million years (My) in the lineages of 10 species of eutherian mammals and 24 species of birds. The results reveal extensive variation in the amount of DNA gained via lineage-specific transposition, but that DNA loss counteracted this expansion to various extent across lineages. Our analysis of the rate and size spectrum of deletion events implies that DNA removal in both mammals and birds has proceeded mostly through large segmental deletions (>10 kb). These findings support a unified accordion model of genome size evolution in eukaryotes whereby DNA loss counteracting TE expansion is a major determinant of genome size. Furthermore, we propose that extensive DNA loss, and not necessarily a dearth of TE activity, has been the primary force maintaining the greater genomic compaction of flying birds and bats relative to their flightless relatives.

evolutionary biology

Asexual but not clonal: evolutionary processes in populations with automictic reproduction

Many parthenogenetically reproducing animals produce offspring not clonally but through different mechanisms collectively referred to as automixis. Here, meiosis proceeds normally but is followed by the fusion of meiotic products that restores diploidy. This mechanism typically leads to a reduction in heterozygosity among the offspring compared to the mother. Following a derivation of the rate at which heterozygosity is lost at one and two loci, depending on the number of crossovers between loci and centromere, a number of models are developed to gain a better understanding of basic evolutionary processes in automictic populations. Analytical results are obtained for the expected equilibrium neutral genetic diversity, mutation-selection balance, selection with overdominance, the rate of spread of beneficial mutations, and selection on crossover rates. These results are complemented by numerical investigations elucidating how associative overdominance (two off-phase deleterious mutations at linked loci behaving like an overdominant locus) can in some cases maintain heterozygosity for prolonged times, and how clonal interference affects adaptation in automictic populations. These results suggest that although automictic populations are expected to suffer from the lack of gene shuffling with other individuals, they are nevertheless in some respects superior to both clonal and outbreeding sexual populations in the way they respond to beneficial and deleterious mutations. Implications for related genetic systems such as intratetrad mating, clonal reproduction, selfing as well as different forms of mixed sexual and automictic reproduction are discussed.

evolutionary biology

Challenging the Raunkiaeran shortfall and the consequences of using imputed databases

O_LIGiven the prevalence of missing data on species traits - Raunkiaeran shorfall -- and its importance for theoretical and empirical investigations, several methods have been proposed to fill sparse databases. Despite its advantages, imputation of missing data can introduce biases. Here, we evaluate the bias in descriptive statistics, model parameters, and phylogenetic signal estimation from imputed databases under different missing and imputing scenarios.\nC_LIO_LIWe simulated coalescent phylogenies and traits under Brownian Motion and different Ornstein-Uhlenbeck evolutionary models. Missing values were created using three scenarios: missing completely at random, missing at random but phylogenetically structured and missing at random but correlated with some other variable. We considered four methods for handling missing data: delete missing values, imputation based on observed mean trait value, Phylogenetic Eigenvectors Maps and Multiple Imputation by Chained Equations. Finally, we assessed estimation errors of descriptive statistics (mean, variance), regression coefficient, Morans correlogram and Blombergs K of imputed traits.\nC_LIO_LIWe found that percentage of missing data, missing mechanisms, Ornstein-Uhlenbeck strength and handling methods were important to define estimation errors. When data were missing completely at random, descriptive statistics were well estimated but Morans correlogram and Blombergs K were not well estimated, depending on handling methods. We also found that handling methods performed worse when data were missing at random, but phylogenetically structured. In this case adding phylogenetic information provided better estimates. Although the error caused by imputation was correlated with estimation errors, we found that such relationship is not linear with estimation errors getting larger as the imputation error increases.\nC_LIO_LIImputed trait databases could bias ecological and evolutionary analyses. We advise researchers to share their raw data along with their imputed database, flagging imputed data and providing information on the imputation process. Thus, users can and should consider the pattern of missing data and then look for the best method to overcome this problem. In addition, we suggest the development of phylogenetic methods that consider imputation uncertainty, phylogenetic autocorrelation and preserve the level of phylogenetic signal of the original data.\nC_LI

evolutionary biology

De-novo emergence and template switching of SINE retroposons during the early evolution of passerine birds

Passeriformes (\"perching birds\" or passerines) make up more than half of all extant bird species. Here, we resolve their deep phylogenetic relationships using presence/absence patterns of short interspersed elements (SINEs), a group of retroposons which is abundant in mammalian genomes but considered largely inactive in avian genomes. The resultant retroposon-based phylogeny provides a powerful and independent corroboration of previous indications derived from sequence-based analyses. Notably, SINE activity began in the common ancestor of Eupasseres (passerines excl. the New Zealand wrens Acanthisittidae) and ceased before the rapid diversification of oscine passerines (songbirds). Furthermore, we find evidence for very recent SINE activity within suboscine passerines, following the emergence of a SINE via acquisition of a different tRNA head as we suggest through template switching. We propose that the early evolution of passerines was unusual among birds in that it was accompanied by activity of SINEs. Their genomic and transcriptomic impact warrants further study in the light of the massive diversification of passerines.

evolutionary biology

Natural selection and maladaptive plasticity in the red-shouldered soapberry bug

Natural selection and phenotypic plasticity can both produce locally differentiated phenotypes, but novel environments or gene combinations can produce plasticity that works in opposition to adaptive change. The red-shouldered soapberry bug (Jadera haematoloma) was locally adapted to feed on the seeds of an introduced and a native host plant in Florida in the 1980s. By 2014, local differentiation was lost and replaced by phenotypically similar populations all adapted to the introduced host, likely as a result of gene flow. Here, I quantify the effects of these two host plants on individual performance, natural selection, and phenotypic plasticity. I find that the seed coat and seedpod of the native host have strong negative effects on juvenile survival and adult reproduction compared to the introduced host. I find support for the hypothesis that the seedpod is driving diversifying natural selection on beak length, which was previously locally adapted between hosts. I also find maladaptive plasticity induced by host plant: bugs develop beak lengths that are mismatched with the seedpod size of the host they are reared on. This plasticity may be the result of gene flow; hybrids in the 1990s showed the same pattern of maladaptive plasticity, and plasticity is stronger in the present in areas with high gene flow. Although ongoing natural selection has produced locally adapted genotypes in soapberry bugs, maladaptive plasticity has masked the phenotypic difference between populations in the field.

evolutionary biology

Transposable elements reveals punctuated patterns of evolution in Mammals

Transposable elements (TEs) play an essential role in shaping eukaryotic genomes and generating variability. Our \"Cold Genome\" hypothesis postulates that speciation and TEs activity are strongly related in mammals. In order to test this hypothesis, we created two new parameters: the Density of Insertion (DI) and the Relative Rate of Speciation (RRS). The DI is the ratio between the number of TE insertions in a genome and its size, whereas the RRS is a conditional parameter designed to identify potential speciation bursts. Thus, by analyzing TEs insertions in mammals, we defined the genomes as \"hot\" (low DI) and \"cold\" (high DI). Then, comparing TEs activity among 16 intra-order pairs of mammalian species, 4 superorders of Eutheria and 29 taxonomical families of the whole Mammalia class, we showed that taxa with positive RRS correlate with \"hot\" genomes, whereas taxa with negative RRS correlate with \"cold\" genomes. In addition, our study supports the \"Punctuated Equilibria\" theory in mammals for both adaptive radiation and stasis.

evolutionary biology

Fidelity of parent-offspring transmission and the evolution of social behavior in structured populations

The theoretical investigation of how spatial structure affects the evolution of social behavior has mostly been done under the assumption that parent-offspring strategy transmission is perfect, i.e., for genetically transmitted traits, that mutation is very weak or absent. Here, we investigate the evolution of social behavior in structured populations under arbitrary mutation probabilities. We consider populations of fixed size N, structured such that in the absence of selection, all individuals have the same probability of reproducing or dying (neutral reproductive values are the all same). Two types of individuals, A and B, corresponding to two types of social behavior, are competing; the fidelity of strategy transmission from parent to offspring is tuned by a parameter . Social interactions have a direct effect on individual fecundities. Under the assumption of small phenotypic differences (implyingweak selection), we provide a formula for the expected frequency of type A individuals in the population, and deduce conditions for the long-term success of one strategy against another. We then illustrate our results with three common life-cycles (Wright-Fisher, Moran Birth-Death and Moran Death-Birth), and specific population structures (graph-structured populations). Qualitatively, we find that some life-cycles (Moran Birth-Death, Wright-Fisher) prevent the evolution of altruistic behavior, confirming previous results obtained with perfect strategy transmission. We also show that computing the expected frequency of altruists on a regular graph may require knowing more than just the graphs size and degree.

evolutionary biology

Inference of multiple-wave population admixture by modeling decay of linkage disequilibrium with polynomial functions

To infer the histories of population admixture, one important challenge with methods based on the admixture linkage disequilibrium (ALD) is to get rid of the effect of source LD (SLD) which is directly inherited from source populations. In previous methods, only the decay curve of weighted LD between pairs of sites whose genetic distance were larger than a certain starting distance was fitted by single or multiple exponential functions, for the inference of recent single- or multiple-wave of admixture. However, the effect of SLD has not been well defined and no tool has been developed to estimate the effect of SLD on weighted LD decay. In this study, we defined the SLD in the formularized weighted LD statistic under the two-way admixture model, and proposed polynomial spectrum (p-spectrum) to study the weighted SLD and weighted LD. We also found reference populations could be used to reduce the SLD in weighted LD statistic. We further developed a method, iMAAPs, to infer Multiple-wave Admixture by fitting ALD using Polynomial spectrum. We evaluated the performance of iMAAPs under various admixture models in simulated data and applied iMAAPs into analysis of genome-wide single nucleotide polymorphism data from the Human Genome Diversity Project (HGDP) and the HapMap Project. We showed that iMAAPs is a considerable improvement over other current methods and further facilitates the inference of the histories of complex population admixtures.

evolutionary biology

Reconstruction of phylogenetic history to resolve the subspecies anomaly of Pantherine cats

All charismatic big cats including tiger (Panthera tigris), lion (Panthera leo), leopard (Panthera pardus), snow leopard (Panthera uncial), and jaguar (Panthera onca) are grouped into the subfamily Pantherinae. Several mitogenomic approaches have been employed to reconstruct the phylogenetic history of the Pantherine cats but the phylogeny has remained largely unresolved till date. One of the major reasons for the difficulty in resolving the phylogenetic tree of Pantherine cats is the small sample size. While previous studies included only 5-10 samples, we have used 43 publically available taxa to reconstruct Pantherine phylogenetic history. Complete mtDNA sequences were used from all individuals excluding the control region (15,489bp). A Bayesian MCMC approach was employed to investigate the divergence times among different Pantherine clades. Both maximum likelihood and Bayesian phylogeny generated a dendrogram: Neofelis nebulosa (Panthera tigris (Panthera onca (Panthera uncia (Panthera leo, Panthera pardus)))), grouping lions with leopards and placing snow leopards as an outgroup to this clade. The phylogeny revealed that lions split from their sister species leopard ~3 Mya and the divergence time between snow leopards and the clade including lions and leopards was estimated to be ~5 Mya. Our study revealed that the morphology-based subspecies designation for both lions and tigers is largely not valid. The estimated tMRCA of 2.9 Mya between Barbary lions and Sub-Saharan African lions depicts the restriction of female-mediated gene flow between the lion populations in the backdrop of the habitat fragmentation taking place from late Pliocene to early to mid-Pleistocene creating islands of forest refugia in central Africa.

evolutionary biology

Genome-level parameters describe the pan-nuclear fractal nature of eukaryotic interphase chromosomal arrangement

Long-range inter-chromosomal interactions in the interphase nucleus subsume critical genome-level regulatory functions such as transcription and gene expression. To decipher the physical basis of diverse pan-nuclear patterns of chromosomal arrangement that facilitates these processes, we investigate the scaling effects within disparate genomes and compared their total number of genes with chromosome size. First, we derived the pan-nuclear average fractal dimension of inter-chromosomal arrangement in interphase nuclei of different species and corroborated our predictions with independently reported results. Then, we described the different patterns across disparate unicellular and multicellular eukaryotes. We report that, unicellular lower eukaryotes have inter-chromosomal fractal dimension = 1 at the pan-nuclear scales, which is analogous to the multi-polymer crumpled globule model. Multi-fractal dimensions, corresponding to different inter-chromosomal arrangements emerged from multicellular eukaryotes, such that closely related species have relatively similar patterns. Using this theoretical approach, we could distinguish fractal patterns from human acrocentric versus metacentric chromosomes, implying that the multi-fractal nature of inter-chromosomal geometry facilitates viable large-scale chromosomal aberrations, such as Robertsonian translocations. We report that the nature of such an average multi-fractal dimension for nocturnal mammals is very different in diurnal mammals, which suggests a greatly enhanced plasticity in arrangement across different cell types, for example retinal versus dermal fibroblasts. Altogether, our results substantiate that genome-level constraints have also co-evolved with the average pan-nuclear fractal dimension of inter-chromosomal folding during eukaryotic evolution.

evolutionary biology

Tempo and timing of ecological trait divergence associated with transitions to coexistence in birds

Summary paragraphOrganismal traits may evolve either gradually or in rapid pulses followed by periods of stasis, but the relative importance of these evolutionary models in generating biodiversity has proven difficult to resolve1,2. In addition, while it is often assumed that pulses of trait evolution are associated with speciation events, few studies have explicitly examined how the tempo of trait divergence varies with respect to different geographical phases of speciation. Thus, we still know little about the trajectories of trait divergence over timescales relevant to speciation, or the extent to which these trajectories are shaped by variation in geographical isolation and overlap (sympatry) among incipient species. Here, we combine divergence time estimates, trait measurements, and geographic range data for avian sister species pairs worldwide to examine the tempo and timing of trait divergence during allopatric speciation. We show that divergence in two important ecological traits--?body mass and beak morphology--is best explained by a model including pulses of divergence and periods of relative stasis. We also infer that trait divergence pulses often precede sympatry, and that pulses leading to greater trait disparity are associated with earlier transitions to sympatry. These findings suggest that early pulses of trait divergence promote subsequent transitions to sympatry, rather than such pulses occurring after sympatry has been established, for example via character displacement3. Incorporating pulsed divergence models into allopatric speciation theory helps to resolve some apparently contradictory observations, including widespread instances of both rapid sympatry and prolonged geographical exclusion4-6.

evolutionary biology