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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

An assessment of phylogenetic tools for analyzing the interplay between interspecific interactions and phenotypic evolution

Much ecological and evolutionary theory predicts that interspecific interactions often drive phenotypic diversification and that species phenotypes in turn influence species interactions. Several phylogenetic comparative methods have been developed to assess the importance of such processes in nature; however, the statistical properties of these methods have gone largely untested. Focusing mainly on scenarios of competition between closely-related species, we assess the performance of available comparative approaches for analyzing the interplay between interspecific interactions and species phenotypes. We find that currently used statistical methods largely fail to detect the impact of interspecific interactions on trait evolution, that sister taxa analyses often erroneously detect character displacement where it does not exist, and that recently developed process-based models have more satisfactory statistical properties. In weighing the strengths and weaknesses of different approaches, we hope to provide a clear guide for empiricists testing hypotheses about the reciprocal effect of interspecific interactions and species phenotypes and to inspire further development of process-based models.

evolutionary biology

Fractal model of emergence of a proto-plant

The extension of the sectional model of the spruce crowns dynamics into diapason (0, 1) of the fractal parameter has demonstrated the existence of green biomass on branches of three orders in form of photosynthesizing (green) points. We investigated the growth of point sets on an interval as a model of the origin of proto-plants, which are formed due to endosymbiosis of cyanobacteria and protists. The fractal properties of the sets of evenly placed points and group sets were studied using the box-counting method. For the group sets, the character of dependence on the growing total number of points changes radically differently depending on whether the number of the points per group or the number of groups was fixed. As the host does not have the initial infrastructure needed for an increase in cyanobacteria per group, the first path is implemented and decreases from 1 to 0.25 when groups consist of two points per group. If and when the host develops necessary anatomical features (infrastructure), the second pathway is realized and grows to 1. The combined trajectory of initially demonstrates a slow growth of the size of the photosynthetic system and then an exponential growth after the development of the hosts infrastructure. Similar fractal peculiarity also characterizes trees and is an innate property of plants. Assumptions on the morphological recapitulation of proto-plant in higher plants ontogenesis (embryogenesis and seed germination) and also a possibility to fix the number of cyanobacteria per group are discussed.

evolutionary biology

Bacterial but not protist gut microbiota align with ecological specialization in a set of lower termite species

The role of microbes in adaptation of higher organisms to the environment is becoming increasingly evident, but remains poorly understood. Protist and bacterial microbes facilitate that lower termites thrive on wood and are directly involved in substrate break down. During the course of evolution lower termites adapted to different diets and lifestyles. In order to test whether there are changes of the termite gut microbiota that co-occur and hence could be related to diet and lifestyle adaptation, we assessed the bacterial and protist communities in a multispecies framework profiling three wood-dwelling and two foraging lower termite species using 16S and 18S rRNA gene amplicon sequencing. Termites were kept under controlled conditions on the same diet to minimize environmental effects on their gut microbiota. We found that protist communities group according to host phylogeny while bacterial communities group according to lifestyle. The change from the ancestral wood-dwelling to a foraging lifestyle coincides with exposure to more diverse and higher concentrations of pathogens as well as a more diverse diet. Accordingly, we identified bacteria that are associated with foraging termites of the genus Reticulitermes and could function as probiotics or be metabolically important on a more diverse diet. Furthermore, protist and bacterial diversity are correlated, suggesting not only that many termite gut bacteria are associated with protists, but also suggesting a role of protist diversity in the evolution of bacterial diversity in the termite gut or vice versa.

evolutionary biology

A defensive body plan was pre-adaptive for termitophily in the rove beetle tribe Termitohospitini (Staphylinidae: Aleocharinae)

Termitophily--the symbiosis of organisms with termite societies--has evolved a disproportionate number of times within the rove beetle subfamily Aleocharinae (Staphylinidae). Among aleocharine termitophiles, defensive (limuloid) and mimetic (physogastric & physothoracic) body forms have evolved convergently, but due to lack of a comprehensive aleocharine phylogeny, the context in which termitophily and associated adaptations evolve is unknown. We present the first example of a robust, morphology-based phylogenetic placement of an exclusively termitophilous tribe, the Termitohospitini. Termitohospitini is recovered to be nested within Myllaenini sensu nov, and sister to Myllaena (new synonymy). Furthermore, we also recovered the small tribe Masuriini nested within Myllaenini sensu nov (new status).\n\nReconstructing ecological transitions within this clade, we present evidence that the stem lineage of Myllaenini sensu nov invaded intertidal marine habitats, the common ancestor for Myllaena + Termitohospitini then transitioned to freshwater riparian habitats, with Termitohospitini alone subsequently shifting to termitophily. We conclude that: (1) Termitohospitini was ancestrally a limuloid-bodied riparian inhabitant; (2) a limuloid form may have been pre-adaptive for defense against host attack during the evolution of termitophily; (3) the strongly tapered abdomen of an ancestral limuloid body was a constraint on the evolution of physogastry, leading to the emergence of the unusual physothoracic body form observed in termitohospitines that likely integrates these obligate termitophiles to life inside termite colonies.\n\n\"one of the most astonishing spectacles in all natural history.\" -- Richard Dawkins

evolutionary biology

Recombination Suppression is Unlikely to Contribute to Speciation in Sympatric Heliconius Butterflies

Mechanisms that suppress recombination are known to help maintain species barriers by preventing the breakup of co-adapted gene combinations. The sympatric butterfly species H. melpomene and H. cydno are separated by many strong barriers, but the species still hybridise infrequently in the wild, with around 40% of the genome influenced by introgression. We tested the hypothesis that genetic barriers between the species are reinforced by inversions or other mechanisms to reduce between-species recombination rate. We constructed fine-scale recombination maps for Panamanian populations of both species and hybrids to directly measure recombination rate between these species, and generated long sequence reads to detect inversions. We find no evidence for a systematic reduction in recombination rates in F1 hybrids, and also no evidence for inversions longer than 50 kb that might be involved in generating or maintaining species barriers. This suggests that mechanisms leading to global or local reduction in recombination do not play a significant role in the maintenance of species barriers between H. melpomene and H. cydno.\n\nAuthor SummaryIt is now possible to study the process of species formation by sequencing the genomes of multiple closely related species. Heliconius melpomene and Heliconius cydno are two butterfly species that have diverged over the past 2 million years and have different colour patterns, mate preferences and host plants. However, they still hybridise infrequently in the wild and exchange large parts of their genomes. Typically, when genomes are exchanged, chromosomes are recombined and gene combinations are broken up, preventing species from forming. Theory predicts that gene variants that define species might be linked together because of structural differences in their genomes, such as inverted pieces of chromosomes that will not be broken up when the species hybridise. However, in this paper, we use deep sequencing of large crosses of butterflies to show that there are no long chromosome regions that are not broken up during hybridisation, and no long chromosome inversions anywhere between the two genomes. This suggests that hybridisation is rare enough and mate preference is strong enough that inversions are not necessary to maintain the species barrier.

evolutionary biology

Level-Based Analysis of Genetic Algorithms and Other Search Processes

Understanding how the time-complexity of evolutionary algorithms (EAs) depend on their parameter settings and characteristics of fitness landscapes is a fundamental problem in evolutionary computation. Most rigorous results were derived using a handful of key analytic techniques, including drift analysis. However, since few of these techniques apply effortlessly to population-based EAs, most time-complexity results concern simplified EAs, such as the (1 + 1) EA.\n\nThis paper describes the level-based theorem, a new technique tailored to population-based processes. It applies to any non-elitist process where o spring are sampled independently from a distribution depending only on the current population. Given conditions on this distribution, our technique provides upper bounds on the expected time until the process reaches a target state.\n\nWe demonstrate the technique on several pseudo-Boolean functions, the sorting problem, and approximation of optimal solutions in combina-torial optimisation. The conditions of the theorem are often straightfor-ward to verify, even for Genetic Algorithms and Estimation of Distribution Algorithms which were considered highly non-trivial to analyse. Finally, we prove that the theorem is nearly optimal for the processes considered. Given the information the theorem requires about the process, a much tighter bound cannot be proved.

evolutionary biology

Ancestry in adapting, spatially-extended populations

Selective sweeps reduce neutral genetic diversity. In sexual populations, this \"hitchhiking\" effect is thought to be limited to the local genomic region of the sweeping allele. While this is true in panmictic populations, we find that in spatially-extended populations the combined effects of many unlinked sweeps can affect patterns of ancestry (and therefore neutral genetic diversity) across the whole genome. Even low rates of sweeps can be enough to skew the spatial locations of ancestors such that neutral mutations that occur in an individual living outside a small region in the center of the range have virtually no chance of fixing in the population. The fact that nearly all ancestry rapidly traces back to a small spatial region also means that relatedness between individuals falls off very slowly as a function of the spatial distance between them.

evolutionary biology