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bioRxiv2016

Soft selective sweeps in evolutionary rescue

Evolutionary rescue occurs when a population that is declining in size because of an environmental change is rescued by genetic adaptation. Evolutionary rescue is an important phenomenon at the intersection of ecology and population genetics. While most population genetic models of evolutionary rescue focus on estimating the probability of rescue, we focus on whether one or more adaptive lineages contribute to evolutionary rescue. We find that when evolutionary rescue is likely, it is often driven by soft selective sweeps where multiple adaptive mutations spread through the population simultaneously. We give full analytic results for the probability of evolutionary rescue and the probability that evolutionary rescue occurs via soft selective sweeps in our model. We expect that these results will find utility in understanding the genetic signatures associated with various evolutionary rescue scenarios in large populations, such as the evolution of drug resistance in viral, bacterial, or eukaryotic pathogens.

Evolutionary Biology↗

bioRxiv2016

Resource limitation reveals a twofold benefit of eusociality

Explaining the evolution and maintenance of cooperative breeding or eusociality remains a challenge. Surprisingly, fundamental ecological factors, specifically competition for limited resources and resource variance, are frequently ignored in models of animal sociality. We here develop a mathematical model that includes density-dependent population growth and quantify the influence of cooperative foraging on resource use efficiency. We derive optimal resource sharing strategies, ranging from egalitarian to cooperatively breeding and eusocial groups. We find that, while egalitarian resource sharing is a risk-reducing foraging strategy, eusociality yields additional benefits: like egalitarian strategies, eusocial groups can reduce their members starvation risk by reducing resource variance. Additionally, eusocial groups increase their reproductive output by increasing intra-group variance in resources allocated to reproduction. This allows reproduction even when resources are so scarce that solitary animals would not be able to reproduce. In a majority of environmental situations and life-histories, this twofold benefit of eusociality increased resource use efficiency and led to supersaturation, that is, to a strong increase in carrying capacity. Supersaturation provides indirect benefits to group members even for low intra-group relatedness and represents one potential explanation for the evolution and maintenance of eusociality and cooperative breeding.

Evolutionary Biology↗

bioRxiv2016

Seed size and its rate of evolution correlate with species diversification across angiosperms

Species diversity varies greatly across the different taxonomic groups that comprise the Tree of Life (ToL). This imbalance is particularly conspicuous within angiosperms, but is largely unexplained. Seed mass is one trait that may help clarify why some lineages diversify more than others because it confers adaptation to different environments, which can subsequently influence speciation and extinction. The rate at which seed mass changes across the angiosperm phylogeny may also be linked to diversification by increasing reproductive isolation and allowing access to novel ecological niches. However, the magnitude and direction of the association between seed mass and diversification has not been assessed across the angiosperm phylogeny. Here, we show that absolute seed size and the rate of change in seed size are both associated with variation in diversification rates. Based on the largest available angiosperm phylogenetic tree, we found that smaller-seeded plants had higher rates of diversification, possibly due to improved colonisation potential. The rate of phenotypic change in seed size was also strongly positively correlated with speciation rates, providing rare, large-scale evidence that rapid morphological change is associated with species divergence. Our study now reveals that variation in morphological traits and, importantly, the rate at which they evolve can contribute to explaining the extremely uneven distribution of diversity across the ToL.

Evolutionary Biology↗

bioRxiv2016

The cryptic origins of evolutionary novelty: 1,000-fold-faster trophic diversification rates without increased ecological opportunity or hybrid swarm

Ecological opportunity is frequently proposed as the sole ingredient for adaptive radiation into novel niches. Alternatively, genome-wide hybridization resulting from hybrid swarm may be the trigger. However, these hypotheses have been difficult to test due to the rarity of comparable control environments lacking adaptive radiations. Here I exploit such a pattern in microendemic radiations of Caribbean pupfishes. I show that a sympatric three-species radiation on San Salvador Island, Bahamas diversified 1,445 times faster than neighboring islands in jaw length due to evolution of a novel scale-eating adaptive zone from a generalist ancestral niche. I then sampled 22 generalist populations on seven neighboring islands and measured morphological diversity, stomach content diversity, dietary isotopic diversity, genetic diversity, lake/island areas, macroalgae richness, and Caribbean-wide patterns of gene flow. None of these standard metrics of ecological opportunity or gene flow were associated with adaptive radiation, except for slight increases in macroalgae richness. Thus, exceptional trophic diversification is highly localized despite myriad generalist populations in comparable environmental and genetic backgrounds. This study provides a strong counterexample to the ecological/hybrid-swarm theories of adaptive radiation and suggests that diversification of novel specialists on a sparse fitness landscape is constrained by more than ecological opportunity and gene flow.

Evolutionary Biology↗

bioRxiv2016

Corticosteroid and progesterone transactivation of mineralocorticoid receptors from Amur sturgeon and tropical gar

The response to a panel of steroids by the mineralocorticoid receptor (MR) from Amur sturgeon and tropical gar, two basal ray-finned fish, expressed in HEK293 cells was investigated. Half-maximal responses (EC50s) for transcriptional activation of sturgeon MR by 11-deoxycorticosterone, corticosterone, 11-deoxycortisol, cortisol and aldosterone, and progesterone were between 13 pM and 150 pM. For gar MR, EC50s were between 8 pM and 55 pM. Such low EC50s support physiological regulation by these steroids of the MR in sturgeon and gar. Companion studies with human MR and zebrafish MR found higher EC50s compared to EC50s for sturgeon and gar MR, with EC50s for zebrafish MR closer to gar and sturgeon MR than was human MR. For zebrafish MR, EC50s were between 75 pM and 740 pM; for human MR, EC50s were between 65 pM and 2 nM. In addition to progesterone, spironolactone and 19nor-progesterone were agonists for all three fish MRs, in contrast to their antagonist activity for human MR, which is hypothesized to involve serine-810 in human MR because all three steroids are agonists for a mutant human Ser810Leu-MR. Paradoxically, sturgeon, gar and zebrafish MRs contain a serine corresponding to serine-810 in human MR. Our data suggests alternative mechanism(s) for progesterone, spironolactone and 19nor-progesterone as MR agonists in these three ray-finned fishes and the need for caution in applying data for progesterone signaling in zebrafish to human physiology.

Evolutionary Biology↗

bioRxiv2016

Range overlap drives chromosome inversion fixation in passerine birds

Chromosome inversions evolve frequently but the reasons why remain largely enigmatic. I used cytological descriptions of 410 species of passerine birds (order Passeriformes) to identify pericentric inversion differences between species. Using a new fossil-calibrated phylogeny I examine the phylogenetic, demographic, and genomic context in which these inversions have evolved. The number of inversion differences between closely related species was highly variable yet consistently predicted by a single factor: whether the ranges of species overlapped. This observation holds even when the analysis is restricted to sympatric sister pairs known to hybridize, and which have divergence times estimated similar to allopatric pairs. Inversions were significantly more likely to have fixed on a sex chromosome than an autosome yet variable mutagenic input alone (by chromosome size, map length, GC content, or repeat density) cannot explain the differences between chromosomes in the number of inversions fixed. Together, these results support a model in which inversions in passerines are adaptive and spread by selection when gene flow occurs before reproductive isolation is complete.

Evolutionary Biology↗

bioRxiv2016

Excess of mutational jackpot events in growing populations due to gene surfing

One of the hallmarks of spontaneous mutations in growing populations is the emergence of mutational jackpot events - large mutant clones arising from mutations that by chance occur early in the development of a cellular population so that their progenitors benefit from prolonged growth. Due to their sheer size, these jackpot events, first discovered by Luria and Delbruck [1], are thought to have momentous roles in short-term evolutionary processes, including the adaptation from standing variation [2-4], evolutionary rescue [5], drug resistance evolution [6-10], and the somatic evolution of genetic diseases [11, 12]. However, because the emergence of jackpot events has been understood only in uniformly growing populations [1, 10, 13], it is currently impossible to predict their impact on the evolution of many naturally structured populations. To study jackpot events in spatially structured populations, we tracked mutant clones in microbial populations using fluorescent microscopy and population sequencing. High-frequency mutations were massively enriched in microbial colonies compared to well-shaken liquid cultures, as a result of late-occurring mutations surfing at the edge of range expansions [14-16]. We provide a mathematical theory that explains the observed excess of jackpot events and predicts their role in promoting rare evolutionary outcomes. In particular, we show that resistant clones generated by surfing can become unleashed under high selection pressures, and thus represent a drug resistance hazard for high-dose drug treatments. An excess of mutational jackpot events is shown to be a general consequence of non-uniform growth and, therefore, could be relevant to the mutational load of developing biofilm communities, solid tumors and multi-cellular organisms.

Evolutionary Biology↗

bioRxiv2016

Characterization by Next Generation Sequencing Reveals the Molecular Mechanisms Driving the Faster Evolutionary rate of Cassava brown streak virus Compared with Ugandan cassava brown streak virus

Cassava is a major staple food for about 800 million people in the tropics and subGtropical regions of the world. Production of cassava is significantly hampered by cassava brown streak disease (CBSD), which is caused by Cassava brown streak virus (CBSV) and Ugandan cassava brown streak virus (UCBSV). The disease is suppressing cassava yields in eastern Africa at an alarming rate. Previous studies have documented that CBSV is more devastating than UCBSV because it more readily infects both susceptible and tolerant cassava cultivars, resulting in greater yield losses. Using whole genome sequences from NGS data, we produced the first coalescentGbased species tree estimate for CBSV and UCBSV. This species framework led to the finding that CBSV has a faster rate of evolution when compared with UCBSV. Furthermore, we have discovered that in CBSV, nonsynonymous substitutions are more predominant than synonymous substitution and occur across the entire genome. All comparative analyses between CBSV and UCBSV presented here suggest that CBSV may be outsmarting the cassava immune system, thus making it more devastating and harder to control.

Evolutionary Biology↗

bioRxiv2016

Model selection in statistical historical biogeography of Neotropical insects-the Exophthalmus genus complex (Curculionidae: Entiminae)

Statistical historical biogeographical methods rely on the use of models that assume various biogeographic processes. Until recently model selection remains an explored topic and the impacts of using different models on inferring biogeographic history are poorly understood. Focusing on the Neotropical weevils in the Exophthalmus genus complex (Insecta: Curculionidae: Entiminae), we compare three commonly used biogeographic models - DIVA (Dispersal-Vicariance Analysis), DEC (Dispersal-Extinction-Cladogenesis) and BayArea (Bayesian Analysis of Biogeography), and examine the impact of modeling founder-event jump dispersal on biogeographic history estimation. We also investigate the biogeographic events that have shaped patterns of distributions, diversification, and endemism in this group of weevils. We sample representatives of 65 species of the Exophthalmus genus complex and 26 outgroup terminals from the Neotropics including Caribbean islands and mainland. We reconstruct a molecular phylogeny based on six genes and performed molecular dating using a relaxed clock with three fossil calibration points. We conduct biogeographic history estimations and compare alternative biogeographic models with the R package BioGeoBEARS. Model selection strongly favors biogeographic models that include founder-event jump dispersal. Without modeling jump dispersal, estimations based on the three biogeographic models are dramatically different, especially at early diverging nodes. When jump dispersal is modeled, however, the three biogeographic models perform similarly. Accordingly, we show that the Neotropical mainland was colonized by Caribbean species in the early Miocene, and that in situ diversification accounts for a majority (~75%) of the biogeographic events in the Exophthalmus genus complex. Our study highlights the need for testing for wide-ranging historical biogeographic processes in the study of Caribbean biogeography and the importance of comparing and selecting the best-fitting model in statistical biogeographic inferences. We demonstrate that modeling founder-event jump dispersal significantly improves the fit of the biogeographic history estimation of Caribbean and Neotropical mainland weevils. We establish that in situ diversification acts as a dominant biogeographic force in the evolution of the Exophthalmus genus complex. The colonization of the Neotropical mainland from Caribbean islands reinforces the notion that islands can be an important source of continental diversity.

Evolutionary Biology↗

bioRxiv2016

Excess of deleterious mutations around HLA genes reveals evolutionary cost of balancing selection

Deleterious mutations are expected to evolve under negative selection and are usually purged from the population. However, deleterious alleles segregate in the human population and some disease-associated variants are maintained at considerable frequencies. Here we test the hypothesis that balancing selection may counteract purifying selection in neighboring regions and thus maintain deleterious variants at higher frequency than expected from their detrimental fitness effect. We first show in realistic simulations that balancing selection reduces the density of polymorphic sites surrounding a locus under balancing selection, but at the same time markedly increases the population frequency of the remaining variants, including even substantially deleterious alleles. To test the predictions of our simulations empirically, we then use whole exome sequencing data from 6,500 human individuals and focus on the most established example for balancing selection in the human genome, the major histocompatibility complex (MHC). Our analysis shows an elevated frequency of putatively deleterious coding variants in non-HLA genes localized in the MHC region. The mean frequency of these variants declined with physical distance from the classical HLA genes, indicating dependency on genetic linkage. These results reveal an indirect cost of the genetic diversity maintained by balancing selection, which has hitherto been perceived as mostly advantageous, and have implications both for the evolution of recombination and also for the epidemiology of various MHC-associated diseases.

Evolutionary Biology↗

bioRxiv2016

Eusociality and other improbable evolutionary outcomes can be accelerated by trait hitchhiking in boom-bust feedback loops

Here I analyze the brush-fire cycle behind the brushy frontier of a grassland, seeking evolutionary feedback loops for large grazing animals and their hominin predators. Several months after a lightning strike, the burn scar grows enough new grass to expand the carrying capacity for grass-specialized herbivores,which evolved from mixed feeders in Africa during the early Pleistocene. The frontier subpopulation of grazers that discovers the auxiliary grassland quickly multiplies,creating a secondary boom for its hominin predators as well. Following this boom, a bust occurs several decades later when the brush returns; it squeezes both prey and predator populations back into the core grassland. This creates a feedback loop that can repeatedly shift the cores gene frequencies toward those of the frontier subpopulation until fixation occurs. Any brush-relevant allele could benefit from this amplifying feedback loop, so long as its phenotypes concentrate near where fresh resources can suddenly open up, back in the brush. Thus, traits concentrated in the frontier fringe can hitchhike; improved survival is not needed. This is natural selection but utilizin selective reproductive opportunity instead of the usual selective survival. Cooperative nurseries in the brushs shade should concentrate the alleles favoring eusociality, repeatedly increasing their proportion via trait hitchhiking in the feedback loop.

Evolutionary Biology↗

bioRxiv2016

Comparing the Statistical Fate of Paralogous and Orthologous Sequences

Since several decades, sequence alignment is a widely used tool in bioinformatics. For instance, finding homologous sequences with known function in large databases is used to get insight into the function of non-annotated genomic regions. Very efficient tools, like BLAST have been developed to identify and rank possible homologous sequences. To estimate the significance of the homology, the ranking of alignment scores takes a background model for random sequences into account. Using this model one can estimate the probability to find two exactly matching subsequences by chance in two unrelated sequences. The corresponding probability for two homologous sequences is much higher allowing to identify them. Here we focus on the distribution of lengths of exact sequence matches in protein coding regions pairs of evolutionary distant genomes. We show that this distribution exhibits a power-law tail with exponent = --5. Developing a simple model of sequence evolution by substitutions and segmental duplications, we show analytically that paralogous and orthologous gene pairs contribute differently to this distribution. Our model explains the differences observed in the comparison of coding and non-coding parts of genomes, thus providing with a better understanding of statistical properties of genomic sequences and their evolution.

Evolutionary Biology↗

bioRxiv2016

Time-dependent fitness effects can drive bet-hedging populations extinct

To survive unpredictable environmental change, many organisms adopt bet-hedging strategies that trade short-term population growth for long-term fitness benefits. Because the benefits of bet-hedging may manifest over long time intervals, bet-hedging strategies may be out-competed by strategies maximizing short-term fitness. Here, we investigate the interplay between two drivers of selection, environmental fluctuations and competition for limited resources, on different bet-hedging strategies. We consider an environment with frequent disasters that switch between which phenotypes they affect in a temporally-correlated fashion. We determine how organisms that stochastically switch between phenotypes at different rates fare in both competition and survival. When disasters are correlated in time, the best strategy for competition is among the worst for survival. Since the time scales over which the two agents of selection act are significantly different, environmental fluctuations and resource competition act in opposition and lead populations to evolve diversification strategies that ultimately drive them extinct.

Evolutionary Biology↗

bioRxiv2016

Landscape connectivity of a noxious invasive weed: human-aided or natural dispersal?

Examining how the landscape may influence gene flow is at the forefront of understanding population differentiation and adaptation. Such understanding is crucial in light of ongoing environmental changes and the elevated risk of ecosystems alteration. In particular, knowledge of how humans may influence the structure of populations is imperative to allow for informed decisions in management and conservation as well as to gain a better understanding of anthropogenic impacts on the interplay between gene flow, genetic drift and selection. Here we use genome-wide molecular markers to characterize the population genetic structure and connectivity of Ipomoea purpurea, a noxious invasive weed. We likewise assess the interaction between natural and human-driven influences on genetic differentiation among populations. Our analyses find that human population density is an important predictor of pairwise population differentiation, suggesting that the agricultural and/or horticultural trade may be involved in maintaining some level of connectivity across distant agricultural fields. Climatic variation appears as an additional predictor of genetic connectivity in this species. We discuss the implications of these results and highlight future research needed to disentangle the mechanistic processes underlying population connectivity of weeds.

Evolutionary Biology↗

bioRxiv2016

Coalescent inferences in conservation genetics: should the exception become the rule?

Genetic estimates of effective population size (Ne) are an established means to develop informed conservation policies. Another key goal to pursue the conservation of endangered species is keeping the connectivity across fragmented environments, to which genetic inferences of gene flow and dispersal greatly contribute. Most current statistical tools for estimating such population demographic parameters are based on Kingman's coalescent (KC). However, KC is inappropriate for taxa displaying skewed reproductive variance, a property widely observed in natural species. Coalescent models that consider skewed reproductive success-called multiple merger coalescent (MMCs)-have been shown to substantially improve estimates of Ne when the distribution of offspring per capita is highly skewed. MMCs predictions of standard population genetic parameters, including the rate of loss of genetic variation and the fixation probability of strongly selected alleles, substantially depart from KC predictions. These extended models also allow studying gene genealogies in a spatial continuum, providing a novel theoretical framework to investigate spatial connectivity. Therefore, development of statistical tools based on MMC's should substantially improve estimates of population demographic parameters with major conservation implications.

Evolutionary Biology↗

bioRxiv2016

A full characterization of evolutionary tree topologies

The shapes of evolutionary trees are influenced by the nature of the evolutionary process, but comparisons of trees from different processes are hindered by the challenge of completely describing tree shape. We present a full characterization of the shapes of rooted branching trees in a form that lends itself to natural tree comparisons. The resulting metric distinguishes trees from random models known to produce different tree shapes. It separates trees derived from tropical vs USA influenza A sequences, which reflect the differing epidemiology of tropical and seasonal flu. We extend the shape metric to incorporate summary features such as asymmetry, or statistics on branch lengths. Our approach allows us to construct addition and multiplication on trees, and to create a convex metric on tree shapes which formally allows computation of average trees.

Evolutionary Biology↗

bioRxiv2016

Identifying outlier loci in admixed and in continuous populations using ancestral population differentiation statistics

Finding genetic signatures of local adaptation is of great interest for many population genetic studies. Common approaches to sorting selective loci from their genomic background focus on the extreme values of the fixation index, FST, across loci. However, the computation of the fixation index becomes challenging when the population is genetically continuous, when predefining subpopulations is a difficult task, and in the presence of admixed individuals in the sample. In this study, we present a new method to identify loci under selection based on an extension of the FST statistic to samples with admixed individuals. In our approach, FST values are computed from the ancestry coefficients obtained with ancestry estimation programs. More specifically, we used factor models to estimate FST, and we compared our neutrality tests with those derived from a principal component analysis approach. The performances of the tests were illustrated using simulated data, and by re-analyzing genomic data from European lines of the plant species Arabidopsis thaliana and human genomic data from the population reference sample, POPRES.

Evolutionary Biology↗

bioRxiv2016

Population structure and coalescence in pedigrees: comparisons to the structured coalescent and a framework for inference

Contrary to what is often assumed in population genetics, independently segregating loci do not have completely independent ancestries, since all loci are inherited through a single, shared population pedigree. Previous work has shown that the non-independence between gene genealogies of independently segregating loci created by the population pedigree is weak in panmictic populations, and predictions made from standard coalescent theory are accurate for populations that are at least moderately sized. Here, we investigate patterns of coalescence in pedigrees of structured populations. We find that the pedigree creates deviations away from the predictions of the structured coalescent that persist on a longer timescale than in the case of panmictic populations. Nevertheless, we find that the structured coalescent provides a reasonable approximation for the coalescent process in structured population pedigrees so long as migration events are moderately frequent and there are no migration events in the recent pedigree of the sample. When there are migration events in the recent sample pedigree, we find that distributions of coalescence in the sample can be modeled as a mixture of distributions from different initial sample configurations. We use this observation to motivate a maximum-likelihood approach for inferring migration rates and mutation rates jointly with features of the pedigree such as recent migrant ancestry and recent relatedness. Using simulation, we show that our inference framework accurately recovers long-term migration rates in the presence of recent migration events in the sample pedigree.

Evolutionary Biology↗